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{=0A= document.writeln('

3D"Click

');=0A= }=0A= =0A= function get_text_link(url, linktext)=0A= {=0A= document.writeln('' + = linktext + '');=0A= }=0A= =0A= function get_htmlftext_link(a, b) {=0A= document.writeln("" + = b + ", ");=0A= }=0A= =0A= ------=_NextPart_000_0000_01CA3DF9.47422A30 Content-Type: application/octet-stream Content-Transfer-Encoding: quoted-printable Content-Location: http://download.interscience.wiley.com/freeflow/js/personalisation.js /*=0A= * Project : Interscience Redesign=0A= * File : personalisation.js=0A= * Creation Date : 25th March 2003=0A= * Author : Jonathan Sugar=0A= *=0A= * Various functions to deliver personalisation functionality.=0A= */=0A= =0A= // Pre-declare userName so it's available when we need to test if the = page=0A= // assembler ran OK=0A= var userName =3D null;=0A= var shcrtCookie =3D null;=0A= =0A= // Browser detect globals:=0A= var uaStr =3D navigator.userAgent.toLowerCase();=0A= var uaVer =3D parseInt(navigator.appVersion);=0A= // for detecting netscape 4=0A= var netscape =3D (uaStr.indexOf("mozilla") > -1);=0A= var netscape4 =3D (netscape && uaVer < 5);=0A= =0A= // Factory Methods=0A= =0A= // Simple wraper object to encapsulate the data for a co-branding item.=0A= function coBrandingItem(image, imageAltText, href)=0A= {=0A= //alert("Making new coBrandingItem:\nImage: " + image + = "\nimageAltText" + imageAltText + "\nhref: " + href);=0A= this.image =3D image;=0A= this.imageAltText =3D imageAltText;=0A= this.href =3D href;=0A= }=0A= =0A= /*=0A= * Insert the 'Customer co-branding' section.=0A= * -----------------------------=0A= *=0A= * Author: Jonathan Sugar, March 2003.=0A= *=0A= * 1. Insert customer co branding. Loop through 'customerCoBranding' array=0A= * inserting XHTML where needed.=0A= *=0A= * NOTE: the array contains ONLY the resource location (the location of a = gif=0A= * on the file system), the required XHTML is then added where needed. = This way=0A= * we maintain the seperation between presentation and content.=0A= */=0A= function insertCustomerCoBranding(maxBranding)=0A= {=0A= if( customerCoBranding[0].image !=3D "none")=0A= {=0A= document.writeln('

');=0A= document.writeln('

');=0A= document.writeln('

' + imageAltText + '
' + imageAltText + = '
More Providers

');=0A= document.writeln('

');=0A= document.writeln('

3D""

');=0A= }=0A= }=0A= =0A= /*=0A= * Insert the 'My Area' section.=0A= * -----------------------------=0A= *=0A= * Author: Jonathan Sugar, March 2003.=0A= * Updated: Ben Marvell, April 2006=0A= *=0A= * My profile link absolute as this file isnt only run from w3 anymore.=0A= */=0A= function insertMyArea(userdata)=0A= {=0A= // just in case the page assembler isn't running.=0A= =0A= =0A= if (userName !=3D null)=0A= {=0A= document.writeln("

" + = userName.substring(0,33) + "..., access your
" + userName + = ", access your

My Profile"); =0A= } =0A= document.writeln(getLoginOutLink());=0A= //CR 3652 getAthenStatus() as added=0A= document.writeln(getAthenStatus());=0A= document.writeln("

");=0A= } else {=0A= if(typeof(environment)!=3D'undefined' && = environment=3D=3D'PRODUCTION') {=0A= document.writeln("

Log Out");=0A= document.writeln("

"); =0A= }=0A= }=0A= if (menuloadedflag){=0A= wisMenu();=0A= }=0A= }=0A= =0A= /*=0A= * Insert the Customer Admin 'Login/Logout' link=0A= * -----------------------------=0A= *=0A= * Author: Bobby Jack, December 2004.=0A= *=0A= */=0A= function insertAdminLink(page)=0A= {=0A= val =3D getCookie("AID");=0A= =0A= if (val && val !=3D "-1")=0A= {=0A= document.writeln('

Logout');=0A= }=0A= else=0A= {=0A= document.writeln('

');=0A= }=0A= }=0A= =0A= /*=0A= * Insert the username section.=0A= * -----------------------------=0A= *=0A= * Author: Jonathan Sugar, March 2003.=0A= *=0A= * 1. Insert the username.=0A= */=0A= function insertUserName()=0A= {=0A= document.write(userName);=0A= }=0A= =0A= /*=0A= * Return the appropriate link to the login/logout cgi=0A= * ---------------------------------------------------=0A= *=0A= * Author: Jonathan Sugar, March 2003.=0A= * Updated: Ben Marvell, April 2006=0A= * Had to change the links absolute as this file isnt only run from w3 = anymore.=0A= */=0A= function getLoginOutLink()=0A= {=0A= if(userName !=3D "")=0A= {=0A= return "

";=0A= }else=0A= {=0A= return "

";=0A= }=0A= }=0A= =0A= /*=0A= * Return the appropriate link to the shopping cart content page=0A= * ---------------------------------------------------=0A= *=0A= * Author: Zhiming & Warrell June 2007=0A= */=0A= function getShCrtLink(logged)=0A= {=0A= if(logged =3D=3D true )=0A= return "

";=0A= else=0A= return "

";=0A= }=0A= =0A= function toggleShCrtLink()=0A= {=0A= shcrtCookie =3D readCookie("SHCRT");=0A= if(shcrtCookie !=3D null)=0A= {=0A= if(document.all)=0A= {=0A= return true;=0A= }=0A= else=0A= {=0A= document.getElementById("shcrt_id").style.display =3D "block";=0A= }=0A= }=0A= else=0A= {=0A= if(document.all)=0A= {=0A= return true;=0A= }=0A= else=0A= {=0A= document.getElementById("shcrt_id").style.display =3D "none";=0A= }=0A= }=0A= }=0A= =0A= =0A= =0A= function readCookie(name)=0A= {=0A= var nameEQ =3D name + "=3D";=0A= var ca =3D document.cookie.split(';');=0A= for(var i=3D0; iYou are logged in = to Athens';=0A= }=0A= else=0A= {=0A= return "

";=0A= }=0A= =0A= } ------=_NextPart_000_0000_01CA3DF9.47422A30 Content-Type: application/octet-stream Content-Transfer-Encoding: quoted-printable Content-Location: http://download.interscience.wiley.com/freeflow/js/site.js /************************************************************************= ***************************=0A= FILE: site.js=0A= AUTHOR: Jonathan Sugar, Chris Neatby-Smith and Digital Pulp. July = 2003.=0A= =0A= DESCRIPTION: Javascript relating to site wide functionality across =0A= InterScience.=0A= =0A= INCLUDES FUNCTIONS=0A= =3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=0A= =0A= Search Functions=0A= ----------------=0A= =0A= selectAndSubmit() - for deciding where to submit a query based on the = state of the form.=0A= processallContentSearch() - for validating form input for an all = content search.=0A= processTitleSearch() - for validating form input for a Title search.=0A= checkCitationSearch() - for validating the citation search form.=0A= selectAll() - check all the checkboxes in a form.=0A= do_popup() - stasa Acronym Finder window popup function.=0A= =0A= =0A= Other Functions=0A= ---------------=0A= =0A= fixInlineLists() - fix netscape 4.x bug where

tags with images = display both an image and=0A= the default bullet. =0A= =0A= = *************************************************************************= **************************/=0A= =0A= var http =3D false;=0A= if(navigator.appName =3D=3D "Microsoft Internet Explorer") {=0A= http =3D new ActiveXObject("Microsoft.XMLHTTP");=0A= } else {=0A= http =3D new XMLHttpRequest();=0A= } =0A= =0A= // Global Variables=0A= var debug =3D false;=0A= var first =3D true;=0A= =0A= // Browser detect globals:=0A= var uaStr =3D navigator.userAgent.toLowerCase();=0A= var uaVer =3D parseInt(navigator.appVersion);=0A= // for detecting netscape 4=0A= var netscape =3D (uaStr.indexOf("mozilla") > -1);=0A= var netscape4 =3D (netscape && uaVer < 5);=0A= =0A= /*=0A= * Used to switch search mode between APS and TitleFinder on quicksearch = boxes=0A= * = -------------------------------------------------------------------------= --=0A= *=0A= * 1. Decides which search is required based on the value of the radio = buttons=0A= * in 'document.formSelector.whichForm'.=0A= *=0A= * 2. Calls individual functions to process the forms and submit them.=0A= *=0A= */=0A= function selectAndSubmit()=0A= {=0A= var formSelection;=0A= =0A= // find out which form we need to process.=0A= var selector =3D document.formSelector.whichForm;=0A= for (var i =3D 0; i < selector.length; i++){=0A= if (selector[i].checked){=0A= formSelection =3D selector[i].value;=0A= }=0A= }=0A= =0A= // Call the relevent function to process the required form.=0A= if(formSelection =3D=3D "allContentSearch"){=0A= processallContentSearch(document.allContentSearchForm, = document.formSelector)=0A= }=0A= else if(formSelection =3D=3D "searchTitles"){=0A= processTitleSearch(document.searchTitles, document.formSelector)=0A= }=0A= else{=0A= return false;=0A= }=0A= =0A= //@@@DM It was anoying me this error =0A= return false;=0A= }=0A= =0A= /*=0A= *Process the ADS search form=0A= *=0A= */=0A= function trim(str)=0A= {=0A= return str.replace(/(^\s*)|(\s*$)/g,"");=0A= }=0A= =0A= function ADSquery(t) {=0A= var keyword =3D trim(t.getElementsByTagName("input")[0].value);=0A= if (keyword!=3D"") {=0A= = window.open("","popup","toolbar=3Dyes,location=3Dyes,status=3Dyes,menubar= =3Dno,scrollbars=3Dyes,resizable=3Dyes,width=3D800,height=3D500");=0A= t.target=3D"popup";=0A= t.qsearch.value=3Dkeyword;=0A= return true;=0A= = //processADSSearch(document.ADSSearchForm,document.ADSQueryForm,keyword);=0A= } else {=0A= alert("Please input a keyword for ADS searching before clicking go");=0A= return false;=0A= }=0A= }=0A= /*=0A= function processADSSearch(hiddenForm ,queryForm , str) {=0A= var terms =3D str;=0A= var formToSubmit =3D hiddenForm;=0A= var formToProcess =3D queryForm;=0A= formToSubmit.qsearch.value =3D terms;=0A= = window.open("","popup","toolbar=3Dyes,location=3Dyes,status=3Dyes,menubar= =3Dno,scrollbars=3Dyes,resizable=3Dyes,width=3D800,height=3D500");=0A= formToSubmit.action =3D = "http://adsabs.harvard.edu/cgi-bin/nph-basic_connect"=0A= formToSubmit.target =3D "popup";=0A= formToSubmit.submit();=0A= }=0A= */=0A= =0A= /*=0A= * Process the allContentSearch form=0A= * ---------------------------------=0A= * 1. Perform form validation, checking for empty fields.=0A= * Give the user a relevent message if required.=0A= *=0A= * 2. Process/Assign the appropriate form elements and submit the form.=0A= */=0A= function processallContentSearch(hiddenForm, queryForm)=0A= {=0A= var formToSubmit =3D hiddenForm;=0A= var formToProcess =3D queryForm;=0A= =0A= // Do some basic form validation=0A= if(formToProcess.terms.value !=3D "")=0A= {=0A= formToSubmit.WISsearch1.value =3D formToProcess.terms.value;=0A= formToSubmit.submit(); =0A= }=0A= else=0A= {=0A= alert("You must enter a search term in the text box before you click = go.");=0A= }=0A= }=0A= =0A= /*=0A= * Process the Title Search form=0A= * -----------------------------=0A= * 1. Perform form validation, checking for empty fields.=0A= * Give the user a relevent message if required.=0A= *=0A= * 2. Process/Assign the appropriate form elements and submit the form.=0A= */=0A= =0A= function processTitleSearch(hiddenForm, queryForm)=0A= {=0A= var formToSubmit =3D hiddenForm;=0A= var formToProcess =3D queryForm;=0A= =0A= // Do some basic form validation=0A= if(formToProcess.terms.value !=3D "")=0A= {=0A= formToSubmit.query.value =3D formToProcess.terms.value;=0A= formToSubmit.submit();=0A= }=0A= else=0A= {=0A= alert("You must enter a search term in the text box before you click = go.");=0A= }=0A= }=0A= =0A= function doCitationSearch()=0A= {=0A= var form =3D document.citsearchform;=0A= if(checkCitationSearch())=0A= {=0A= form.action =3D "/search/allsearch";=0A= form.submit();=0A= }=0A= }=0A= =0A= // Preprocesses the arguments sent to CitationSearch and checks validity = of user inputs.=0A= function checkCitationSearch()=0A= {=0A= var supplementFound =3D 0; //increment if found;=0A= var hyphenFound =3D 0; //increment if found;=0A= var fm =3D document.citsearchform;=0A= var errmsg =3D "Please use the valid digits '0' to '9'";=0A= // remove all spaces=0A= fm.volume.value =3D fm.volume.value.replace(/ /g, "");=0A= fm.issue.value =3D fm.issue.value.replace(/ /g, "");=0A= fm.pages.value =3D fm.pages.value.replace(/ /g, "");=0A= =0A= if (fm.issn.value.length > 0 && fm.volume.value.length > 0 && = fm.pages.value.length > 0)=0A= {=0A= // check page range=0A= var pageRange =3D fm.pages.value;=0A= var volume =3D fm.volume.value;=0A= var issue =3D fm.issue.value;=0A= var continueFlag =3D 0;=0A= //check the volume=0A= // if (isNaN(volume))=0A= // {=0A= // // volume failed checking=0A= // alert("Volume is invalid. "+errmsg+".");=0A= // return false;=0A= // }=0A= //check the issue=0A= if ((issue.length !=3D 0) && isNaN(issue))=0A= {=0A= // issue failed checking=0A= alert("Issue is invalid. "+errmsg+" or leave blank.");=0A= return false;=0A= }=0A= //check the page range=0A= if (isNaN(pageRange))=0A= {=0A= var isValid =3D false;=0A= // check for hyphen=0A= var hyphenIndex =3D pageRange.indexOf("-");=0A= if ((hyphenIndex !=3D -1) && (hyphenIndex =3D=3D = pageRange.lastIndexOf("-")))=0A= {=0A= // we have only one hyphen, so extract each number=0A= var firstNum =3D pageRange.substring(0, hyphenIndex);=0A= var secondNum =3D pageRange.substring(hyphenIndex + 1);=0A= // check for S=0A= var firstS =3D firstNum.indexOf("S");=0A= var secondS =3D secondNum.indexOf("S");=0A= if (firstS =3D=3D secondS)=0A= {=0A= if ((firstS =3D=3D -1) && isNum(firstNum) && isNum(secondNum) && = (firstNum.length > 0) && (secondNum.length > 0))=0A= isValid =3D true; // both inputs are digits=0A= else if (firstS =3D=3D 0)=0A= {=0A= var firstNumNoS =3D firstNum.substring(1);=0A= var secondNumNoS =3D secondNum.substring(1);=0A= if (isNum(firstNumNoS) && isNum(secondNumNoS) && = (firstNumNoS.length > 0) && (secondNumNoS.length > 0))=0A= isValid =3D true; // both inputs are Sdigits=0A= }=0A= =0A= }=0A= }=0A= if (isValid)=0A= {=0A= return true;=0A= }=0A= else=0A= {=0A= alert("The page range is invalid. "+errmsg+" and a hyphen '-' if = required.");=0A= return false;=0A= }=0A= }=0A= return true;=0A= }=0A= else=0A= {=0A= alert("Volume and pages are required fields. Please make sure data has = been entered for both fields.");=0A= return false;=0A= }=0A= }=0A= =0A= // returns true if a is an Integer.=0A= function isNum(a)=0A= { return !(isNaN(a)); }=0A= =0A= function fixInlineLists() {=0A= if (!document.getElementById) return;=0A= var allLIs =3D document.getElementsByTagName('li');=0A= var bulletNode =3D document.createElement('img');=0A= bulletNode.src = =3D"http://download.interscience.wiley.com/images/icon.bullet.gif";=0A= =0A= for (var i=3D0; iAbstract | References';=0A= }=0A= //alert("URL: " + loc + "\nStart Index: " + startIndex + "\nEnd Index: = " + endIndex + "\nPage: " + page + "\nLink Text: " + links);=0A= return links;=0A= }=0A= =0A= =0A= function selectAll(fm)=0A= {=0A= //var fm =3D document.viewSelectedForm;=0A= =0A= for (var i =3D 0; i < fm.elements.length; i++)=0A= {=0A= if (fm.elements[i].type =3D=3D 'checkbox' /*&& fm.elements[i].name = =3D=3D 'ID'*/)=0A= {=0A= fm.elements[i].checked =3D true;=0A= }=0A= }=0A= }=0A= =0A= =0A= function do_popup(file)=0A= {=0A= var w =3D window.open(file, 'popWin', = 'width=3D350,height=3D500,scrollbars=3Dyes');=0A= =0A= }=0A= =0A= =0A= function mailTool(itemID, useurl, skin)=0A= {=0A= //var url =3D "/cgi-bin/mailform?item=3D"+itemID;=0A= var url =3D "/cgi-bin/mailform?item=3D" + itemID + "&skin=3D" + skin;=0A= var parameters =3D = 'status=3Dno,scrollbars=3Dno,resizable=3Dyes,width=3D400,height=3D475';=0A= =0A= if (useurl !=3D "")=0A= {=0A= url +=3D "&useurl=3D"+useurl;=0A= }=0A= =0A= if ((isNaN(parseInt(itemID))=3D=3Dtrue)||(arguments.length >=3D 4 && = arguments[3] =3D=3D 'cluster'))=0A= {=0A= url +=3D '&type=3Dcluster';=0A= }=0A= =0A= //check whether the last 2 arguments is used for urllink.=0A= // urllink is needed to open up mail form for mrw pages on tomcat = port=0A= if (arguments.length>=3D5 && = arguments[arguments.length-2]=3D=3D'urllink' && = arguments[arguments.length-1]!=3D'')=0A= {=0A= url =3D arguments[arguments.length-1] + url;=0A= }=0A= =0A= if (arguments.length>=3D5 && arguments[3]=3D=3D'currentlink' && = arguments[4]!=3D'')=0A= {=0A= url =3D url + '¤tLink=3D' + arguments[4];=0A= =0A= //processing specific cases=0A= if (arguments[4]=3D=3D'jcatalogjsphdr')=0A= {=0A= //get the issn and pass it the next stage for processing=0A= var currloc =3D location.href;=0A= var issnloc =3D currloc.indexOf("&issn=3D");=0A= if (issnloc !=3D -1)=0A= {=0A= url =3D url + '¤tISSN=3D' + = currloc.substring(issnloc+6);=0A= }=0A= }=0A= // issn is needed for cocoon rendered mrw to form the final url.=0A= else if ( (arguments[4]=3D=3D'cocoonmrwhome') || = (arguments[4]=3D=3D'cocoonmrwarticle') )=0A= {=0A= if (arguments.length>=3D7 && arguments[5]=3D=3D'issn' && = arguments[6]!=3D'')=0A= {=0A= url =3D url + '¤tISSN=3D' + arguments[6];=0A= }=0A= //getting the parameters of the currently shown mrw from the = url=0A= //the method used here is a little crude, it extracts the = values from the current url of the page the user is in =0A= //to pass it to the background program to reconstruct the = requred url=0A= if (arguments[4]=3D=3D'cocoonmrwhome')=0A= {=0A= var currloc =3D location.href;=0A= var mrwParamArr =3D currloc.split("/");=0A= if (mrwParamArr.length >=3D 7)=0A= {=0A= url =3D url + '&mrwPath=3D' + mrwParamArr[5];=0A= var mrwFileParam =3D mrwParamArr[6];=0A= var seploc =3D mrwFileParam.indexOf("#");=0A= if (seploc !=3D -1)=0A= {=0A= url =3D url + '&mrwSection=3D' + = mrwFileParam.substring(seploc+1);=0A= mrwFileParam =3D = mrwFileParam.substring(0,seploc);=0A= }=0A= seploc =3D mrwFileParam.indexOf("?");=0A= if (seploc !=3D -1)=0A= {=0A= url =3D url + '&mrwUrlParam=3D' + = mrwFileParam.substring(seploc+1);=0A= url =3D url + '&mrwDocType=3D' + = mrwFileParam.substring(0,seploc);=0A= }=0A= else=0A= {=0A= url =3D url + '&mrwDocType=3D' + mrwFileParam;=0A= }=0A= }=0A= =0A= }=0A= else if (arguments[4]=3D=3D'cocoonmrwarticle')=0A= {=0A= var currloc =3D location.href;=0A= var mrwParamArr =3D currloc.split("/");=0A= if (mrwParamArr.length >=3D 7)=0A= {=0A= url =3D url + '&mrwPath=3D' + mrwParamArr[5];=0A= url =3D url + '&mrwAid=3D' + mrwParamArr[7];=0A= url =3D url + '&mrwVersion=3D' + mrwParamArr[8];=0A= var mrwFileParam =3D mrwParamArr[9];=0A= var seploc =3D mrwFileParam.indexOf("#");=0A= if (seploc !=3D -1)=0A= {=0A= url =3D url + '&mrwSection=3D' + = mrwFileParam.substring(seploc+1);=0A= url =3D url + '&mrwDocType=3D' + = mrwFileParam.substring(0,seploc);=0A= }=0A= else=0A= {=0A= url =3D url + '&mrwDocType=3D' + mrwFileParam;=0A= }=0A= }=0A= }=0A= }=0A= }=0A= =0A= //checking if a html file exists in the url=0A= var tmpfname =3D location.href;=0A= var loc =3D tmpfname.indexOf("?");=0A= if (loc !=3D -1)=0A= {=0A= tmpfname =3D tmpfname.substring(0,loc);=0A= }=0A= loc =3D tmpfname.indexOf(".html");=0A= if (loc !=3D -1)=0A= {=0A= loc =3D tmpfname.lastIndexOf("/");=0A= if (loc !=3D -1)=0A= {=0A= tmpfname =3D tmpfname.substring(loc+1);=0A= url =3D url + '¤tFile=3D' + tmpfname;=0A= }=0A= }=0A= =0A= if (arguments.length>=3D7 && arguments[5]=3D=3D'currentyear' && = arguments[6]!=3D'')=0A= {=0A= url =3D url + '¤tYear=3D' + arguments[6];=0A= }=0A= =0A= eval("wileyMailTool =3D = window.open('"+url+"','MailTool','"+parameters+"')");=0A= =0A= // If object exists ensure has focus=0A= if (eval("wileyMailTool") && window.focus)=0A= eval("wileyMailTool").focus();=0A= }=0A= =0A= =0A= /*=0A= * 1. Find the links we need to alter.=0A= * 2. For each link apply the new styles we need.=0A= */=0A= function fixAbsRefRendering()=0A= { =0A= var table =3D document.getElementById('prerendered');=0A= var anchors =3D table.getElementsByTagName('a');=0A= for (var i =3D 1; i < anchors.length; i++)=0A= {=0A= if(anchors[i].href !=3D"") =0A= { =0A= applyAbsRefStyleCorrection(anchors[i]);=0A= =0A= }=0A= }=0A= }=0A= =0A= function applyAbsRefStyleCorrection(currentLink)=0A= {=0A= currentLink.style["color"] =3D "#369";=0A= currentLink.style["fontWeight"] =3D "normal";=0A= currentLink.style["marginLeft"] =3D "3px";=0A= currentLink.style["marginRight"] =3D "5px";=0A= }=0A= =0A= function populatePage(formName)=0A= {=0A= if (formName.Page.value =3D=3D '')=0A= {=0A= formName.Page.value =3D document.location;=0A= }=0A= }=0A= =0A= function equalizeColumnWidth(numFeatures)=0A= {=0A= var numberOfFeatures =3D numFeatures; =0A= // Percentage width of table to use for each column.=0A= var percentPerFeature =3D Math.floor(100 / numberOfFeatures); =0A= // Number of columns in total. Content cols + seperators. =0A= =0A= document.writeln("");=0A= for(var i =3D 0; i < numberOfFeatures; i++)=0A= { =0A= document.writeln(' 3D"blank"

');=0A= }=0A= document.writeln("");=0A= }=0A= =0A= function old_equalizeColumnWidth(numFeatures)=0A= {=0A= var numberOfFeatures =3D numFeatures; =0A= // Percentage width of table to use for each column.=0A= var percentPerFeature =3D Math.floor(100 / numberOfFeatures); =0A= // Number of columns in total. Content cols + seperators. =0A= =0A= if(debug)=0A= {=0A= alert("Number of feature boxes: " + numberOfFeatures + "\nPercent per = feature: " + percentPerFeature);=0A= }=0A= =0A= document.writeln("");=0A= for(var i =3D 0; i < numberOfFeatures; i++)=0A= { =0A= if (netscape4 =3D=3D false)=0A= {=0A= document.writeln(' 3D"blank"

'); =0A= }=0A= }=0A= document.writeln("");=0A= }=0A= =0A= function writeFBoxCell()=0A= {=0A= if(first)=0A= {=0A= document.write('');=0A= }else=0A= {=0A= document.write('');=0A= }=0A= numFeatures ++;=0A= }=0A= =0A= =0A= //=0A= // escape apostrophe characters within a string=0A= //=0A= function encode(str)=0A= {=0A= out =3D '';=0A= =0A= for (a =3D 0; a < str.length; a++)=0A= {=0A= c =3D str.charAt(a);=0A= =0A= if (c =3D=3D "'")=0A= {=0A= out +=3D '\\';=0A= }=0A= =0A= out +=3D c;=0A= }=0A= =0A= return out;=0A= }=0A= =0A= =0A= //=0A= //=0A= //=0A= function escapeEntities(str)=0A= {=0A= while (str.indexOf("'") > -1)=0A= {=0A= pos =3D str.indexOf("'");=0A= str =3D str.substr(0, pos) + '\\\'' + str.substr(pos + 6);=0A= }=0A= =0A= return str;=0A= }=0A= =0A= =0A= // new popup function less intrusive just uses the DOM to pickup links = with an exwin class.=0A= // currently implemented for Figure popups on D&T homepage.=0A= =0A= function exLinks()=0A= {=0A= if (document.getElementById)=0A= {=0A= var aObject =3D document.getElementsByTagName("a");=0A= for (var x=3D0; x" + = liels[j].innerHTML + "

You do not have = anything saved in this menu.

";=0A= else=0A= tmpinnerhtml +=3D "

" = + liels[j].innerHTML + "

"; =0A= } =0A= } else {=0A= //setup var to see if more is required=0A= var more =3D (subnodeslength < lilength) ? true : = false; =0A= var flag =3D true;=0A= for (var j=3D0; j" + liels[j].innerHTML + = "";=0A= } else if (j > lilength-3){=0A= if (j =3D=3D lilength-2){=0A= var url =3D liels[j].innerHTML.split('"')[1];=0A= tmpinnerhtml +=3D "

" + liels[j].innerHTML + "

";=0A= } else {=0A= tmpinnerhtml +=3D "

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Brain Pathology

ISSN: 1750-3639 (Online)

ISSN: 1015-6305 (Print)

Volume 19, Issue 4, 2009.

Pages: 674=96693

Top of Page
Abstract
INTRODUCTION
CENTRAL ROLE OF DENDRITIC CELLS (DCs) IN THE ACTIVATION = OF THE=20 IMMUNE SYSTEM
THE CNS=97AN IMMUNOLOGICALLY SPECIALIZED SITE
INTERACTION OF MALIGNANT GLIOMA AND THE IMMUNE = SYSTEM
GLIOMA-ASSOCIATED TARGET STRUCTURES FOR = IMMUNOTHERAPY
GLIOMA IMMUNOTHERAPY
ENHANCEMENT OF VACCINE IMMUNOGENICITY
BREAKING THE LOCAL IMMUNOSUPPRESSIVE ENVIRONMENT OF = GLIOMAS
COMBINATION OF IMMUNOTHERAPY AND RADIOCHEMOTHERAPY
CONCLUSION
ACKNOWLEDGMENTS
References

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Abstract=20 Only

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***************************=0A= FILE: site.js=0A= AUTHOR: Jonathan Sugar, Chris Neatby-Smith and Digital Pulp. July = 2003.=0A= =0A= DESCRIPTION: Javascript relating to site wide functionality across =0A= InterScience.=0A= =0A= INCLUDES FUNCTIONS=0A= =3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=0A= =0A= Search Functions=0A= ----------------=0A= =0A= selectAndSubmit() - for deciding where to submit a query based on the = state of the form.=0A= processallContentSearch() - for validating form input for an all = content search.=0A= processTitleSearch() - for validating form input for a Title search.=0A= checkCitationSearch() - for validating the citation search form.=0A= selectAll() - check all the checkboxes in a form.=0A= do_popup() - stasa Acronym Finder window popup function.=0A= =0A= =0A= Other Functions=0A= ---------------=0A= =0A= fixInlineLists() - fix netscape 4.x bug where

tags with images = display both an image and=0A= the default bullet. =0A= =0A= = *************************************************************************= **************************/=0A= =0A= var http =3D false;=0A= if(navigator.appName =3D=3D "Microsoft Internet Explorer") {=0A= http =3D new ActiveXObject("Microsoft.XMLHTTP");=0A= } else {=0A= http =3D new XMLHttpRequest();=0A= } =0A= =0A= // Global Variables=0A= var debug =3D false;=0A= var first =3D true;=0A= =0A= // Browser detect globals:=0A= var uaStr =3D navigator.userAgent.toLowerCase();=0A= var uaVer =3D parseInt(navigator.appVersion);=0A= // for detecting netscape 4=0A= var netscape =3D (uaStr.indexOf("mozilla") > -1);=0A= var netscape4 =3D (netscape && uaVer < 5);=0A= =0A= /*=0A= * Used to switch search mode between APS and TitleFinder on quicksearch = boxes=0A= * = -------------------------------------------------------------------------= --=0A= *=0A= * 1. Decides which search is required based on the value of the radio = buttons=0A= * in 'document.formSelector.whichForm'.=0A= *=0A= * 2. Calls individual functions to process the forms and submit them.=0A= *=0A= */=0A= function selectAndSubmit()=0A= {=0A= var formSelection;=0A= =0A= // find out which form we need to process.=0A= var selector =3D document.formSelector.whichForm;=0A= for (var i =3D 0; i < selector.length; i++){=0A= if (selector[i].checked){=0A= formSelection =3D selector[i].value;=0A= }=0A= }=0A= =0A= // Call the relevent function to process the required form.=0A= if(formSelection =3D=3D "allContentSearch"){=0A= processallContentSearch(document.allContentSearchForm, = document.formSelector)=0A= }=0A= else if(formSelection =3D=3D "searchTitles"){=0A= processTitleSearch(document.searchTitles, document.formSelector)=0A= }=0A= else{=0A= return false;=0A= }=0A= =0A= //@@@DM It was anoying me this error =0A= return false;=0A= }=0A= =0A= /*=0A= *Process the ADS search form=0A= *=0A= */=0A= function trim(str)=0A= {=0A= return str.replace(/(^\s*)|(\s*$)/g,"");=0A= }=0A= =0A= function ADSquery(t) {=0A= var keyword =3D trim(t.getElementsByTagName("input")[0].value);=0A= if (keyword!=3D"") {=0A= = window.open("","popup","toolbar=3Dyes,location=3Dyes,status=3Dyes,menubar= =3Dno,scrollbars=3Dyes,resizable=3Dyes,width=3D800,height=3D500");=0A= t.target=3D"popup";=0A= t.qsearch.value=3Dkeyword;=0A= return true;=0A= = //processADSSearch(document.ADSSearchForm,document.ADSQueryForm,keyword);=0A= } else {=0A= alert("Please input a keyword for ADS searching before clicking go");=0A= return false;=0A= }=0A= }=0A= /*=0A= function processADSSearch(hiddenForm ,queryForm , str) {=0A= var terms =3D str;=0A= var formToSubmit =3D hiddenForm;=0A= var formToProcess =3D queryForm;=0A= formToSubmit.qsearch.value =3D terms;=0A= = window.open("","popup","toolbar=3Dyes,location=3Dyes,status=3Dyes,menubar= =3Dno,scrollbars=3Dyes,resizable=3Dyes,width=3D800,height=3D500");=0A= formToSubmit.action =3D = "http://adsabs.harvard.edu/cgi-bin/nph-basic_connect"=0A= formToSubmit.target =3D "popup";=0A= formToSubmit.submit();=0A= }=0A= */=0A= =0A= /*=0A= * Process the allContentSearch form=0A= * ---------------------------------=0A= * 1. Perform form validation, checking for empty fields.=0A= * Give the user a relevent message if required.=0A= *=0A= * 2. Process/Assign the appropriate form elements and submit the form.=0A= */=0A= function processallContentSearch(hiddenForm, queryForm)=0A= {=0A= var formToSubmit =3D hiddenForm;=0A= var formToProcess =3D queryForm;=0A= =0A= // Do some basic form validation=0A= if(formToProcess.terms.value !=3D "")=0A= {=0A= formToSubmit.WISsearch1.value =3D formToProcess.terms.value;=0A= formToSubmit.submit(); =0A= }=0A= else=0A= {=0A= alert("You must enter a search term in the text box before you click = go.");=0A= }=0A= }=0A= =0A= /*=0A= * Process the Title Search form=0A= * -----------------------------=0A= * 1. Perform form validation, checking for empty fields.=0A= * Give the user a relevent message if required.=0A= *=0A= * 2. Process/Assign the appropriate form elements and submit the form.=0A= */=0A= =0A= function processTitleSearch(hiddenForm, queryForm)=0A= {=0A= var formToSubmit =3D hiddenForm;=0A= var formToProcess =3D queryForm;=0A= =0A= // Do some basic form validation=0A= if(formToProcess.terms.value !=3D "")=0A= {=0A= formToSubmit.query.value =3D formToProcess.terms.value;=0A= formToSubmit.submit();=0A= }=0A= else=0A= {=0A= alert("You must enter a search term in the text box before you click = go.");=0A= }=0A= }=0A= =0A= function doCitationSearch()=0A= {=0A= var form =3D document.citsearchform;=0A= if(checkCitationSearch())=0A= {=0A= form.action =3D "/search/allsearch";=0A= form.submit();=0A= }=0A= }=0A= =0A= // Preprocesses the arguments sent to CitationSearch and checks validity = of user inputs.=0A= function checkCitationSearch()=0A= {=0A= var supplementFound =3D 0; //increment if found;=0A= var hyphenFound =3D 0; //increment if found;=0A= var fm =3D document.citsearchform;=0A= var errmsg =3D "Please use the valid digits '0' to '9'";=0A= // remove all spaces=0A= fm.volume.value =3D fm.volume.value.replace(/ /g, "");=0A= fm.issue.value =3D fm.issue.value.replace(/ /g, "");=0A= fm.pages.value =3D fm.pages.value.replace(/ /g, "");=0A= =0A= if (fm.issn.value.length > 0 && fm.volume.value.length > 0 && = fm.pages.value.length > 0)=0A= {=0A= // check page range=0A= var pageRange =3D fm.pages.value;=0A= var volume =3D fm.volume.value;=0A= var issue =3D fm.issue.value;=0A= var continueFlag =3D 0;=0A= //check the volume=0A= // if (isNaN(volume))=0A= // {=0A= // // volume failed checking=0A= // alert("Volume is invalid. "+errmsg+".");=0A= // return false;=0A= // }=0A= //check the issue=0A= if ((issue.length !=3D 0) && isNaN(issue))=0A= {=0A= // issue failed checking=0A= alert("Issue is invalid. "+errmsg+" or leave blank.");=0A= return false;=0A= }=0A= //check the page range=0A= if (isNaN(pageRange))=0A= {=0A= var isValid =3D false;=0A= // check for hyphen=0A= var hyphenIndex =3D pageRange.indexOf("-");=0A= if ((hyphenIndex !=3D -1) && (hyphenIndex =3D=3D = pageRange.lastIndexOf("-")))=0A= {=0A= // we have only one hyphen, so extract each number=0A= var firstNum =3D pageRange.substring(0, hyphenIndex);=0A= var secondNum =3D pageRange.substring(hyphenIndex + 1);=0A= // check for S=0A= var firstS =3D firstNum.indexOf("S");=0A= var secondS =3D secondNum.indexOf("S");=0A= if (firstS =3D=3D secondS)=0A= {=0A= if ((firstS =3D=3D -1) && isNum(firstNum) && isNum(secondNum) && = (firstNum.length > 0) && (secondNum.length > 0))=0A= isValid =3D true; // both inputs are digits=0A= else if (firstS =3D=3D 0)=0A= {=0A= var firstNumNoS =3D firstNum.substring(1);=0A= var secondNumNoS =3D secondNum.substring(1);=0A= if (isNum(firstNumNoS) && isNum(secondNumNoS) && = (firstNumNoS.length > 0) && (secondNumNoS.length > 0))=0A= isValid =3D true; // both inputs are Sdigits=0A= }=0A= =0A= }=0A= }=0A= if (isValid)=0A= {=0A= return true;=0A= }=0A= else=0A= {=0A= alert("The page range is invalid. "+errmsg+" and a hyphen '-' if = required.");=0A= return false;=0A= }=0A= }=0A= return true;=0A= }=0A= else=0A= {=0A= alert("Volume and pages are required fields. Please make sure data has = been entered for both fields.");=0A= return false;=0A= }=0A= }=0A= =0A= // returns true if a is an Integer.=0A= function isNum(a)=0A= { return !(isNaN(a)); }=0A= =0A= function fixInlineLists() {=0A= if (!document.getElementById) return;=0A= var allLIs =3D document.getElementsByTagName('li');=0A= var bulletNode =3D document.createElement('img');=0A= bulletNode.src = =3D"http://download.interscience.wiley.com/images/icon.bullet.gif";=0A= =0A= for (var i=3D0; iAbstract | References';=0A= }=0A= //alert("URL: " + loc + "\nStart Index: " + startIndex + "\nEnd Index: = " + endIndex + "\nPage: " + page + "\nLink Text: " + links);=0A= return links;=0A= }=0A= =0A= =0A= function selectAll(fm)=0A= {=0A= //var fm =3D document.viewSelectedForm;=0A= =0A= for (var i =3D 0; i < fm.elements.length; i++)=0A= {=0A= if (fm.elements[i].type =3D=3D 'checkbox' /*&& fm.elements[i].name = =3D=3D 'ID'*/)=0A= {=0A= fm.elements[i].checked =3D true;=0A= }=0A= }=0A= }=0A= =0A= =0A= function do_popup(file)=0A= {=0A= var w =3D window.open(file, 'popWin', = 'width=3D350,height=3D500,scrollbars=3Dyes');=0A= =0A= }=0A= =0A= =0A= function mailTool(itemID, useurl, skin)=0A= {=0A= //var url =3D "/cgi-bin/mailform?item=3D"+itemID;=0A= var url =3D "/cgi-bin/mailform?item=3D" + itemID + "&skin=3D" + skin;=0A= var parameters =3D = 'status=3Dno,scrollbars=3Dno,resizable=3Dyes,width=3D400,height=3D475';=0A= =0A= if (useurl !=3D "")=0A= {=0A= url +=3D "&useurl=3D"+useurl;=0A= }=0A= =0A= if ((isNaN(parseInt(itemID))=3D=3Dtrue)||(arguments.length >=3D 4 && = arguments[3] =3D=3D 'cluster'))=0A= {=0A= url +=3D '&type=3Dcluster';=0A= }=0A= =0A= //check whether the last 2 arguments is used for urllink.=0A= // urllink is needed to open up mail form for mrw pages on tomcat = port=0A= if (arguments.length>=3D5 && = arguments[arguments.length-2]=3D=3D'urllink' && = arguments[arguments.length-1]!=3D'')=0A= {=0A= url =3D arguments[arguments.length-1] + url;=0A= }=0A= =0A= if (arguments.length>=3D5 && arguments[3]=3D=3D'currentlink' && = arguments[4]!=3D'')=0A= {=0A= url =3D url + '¤tLink=3D' + arguments[4];=0A= =0A= //processing specific cases=0A= if (arguments[4]=3D=3D'jcatalogjsphdr')=0A= {=0A= //get the issn and pass it the next stage for processing=0A= var currloc =3D location.href;=0A= var issnloc =3D currloc.indexOf("&issn=3D");=0A= if (issnloc !=3D -1)=0A= {=0A= url =3D url + '¤tISSN=3D' + = currloc.substring(issnloc+6);=0A= }=0A= }=0A= // issn is needed for cocoon rendered mrw to form the final url.=0A= else if ( (arguments[4]=3D=3D'cocoonmrwhome') || = (arguments[4]=3D=3D'cocoonmrwarticle') )=0A= {=0A= if (arguments.length>=3D7 && arguments[5]=3D=3D'issn' && = arguments[6]!=3D'')=0A= {=0A= url =3D url + '¤tISSN=3D' + arguments[6];=0A= }=0A= //getting the parameters of the currently shown mrw from the = url=0A= //the method used here is a little crude, it extracts the = values from the current url of the page the user is in =0A= //to pass it to the background program to reconstruct the = requred url=0A= if (arguments[4]=3D=3D'cocoonmrwhome')=0A= {=0A= var currloc =3D location.href;=0A= var mrwParamArr =3D currloc.split("/");=0A= if (mrwParamArr.length >=3D 7)=0A= {=0A= url =3D url + '&mrwPath=3D' + mrwParamArr[5];=0A= var mrwFileParam =3D mrwParamArr[6];=0A= var seploc =3D mrwFileParam.indexOf("#");=0A= if (seploc !=3D -1)=0A= {=0A= url =3D url + '&mrwSection=3D' + = mrwFileParam.substring(seploc+1);=0A= mrwFileParam =3D = mrwFileParam.substring(0,seploc);=0A= }=0A= seploc =3D mrwFileParam.indexOf("?");=0A= if (seploc !=3D -1)=0A= {=0A= url =3D url + '&mrwUrlParam=3D' + = mrwFileParam.substring(seploc+1);=0A= url =3D url + '&mrwDocType=3D' + = mrwFileParam.substring(0,seploc);=0A= }=0A= else=0A= {=0A= url =3D url + '&mrwDocType=3D' + mrwFileParam;=0A= }=0A= }=0A= =0A= }=0A= else if (arguments[4]=3D=3D'cocoonmrwarticle')=0A= {=0A= var currloc =3D location.href;=0A= var mrwParamArr =3D currloc.split("/");=0A= if (mrwParamArr.length >=3D 7)=0A= {=0A= url =3D url + '&mrwPath=3D' + mrwParamArr[5];=0A= url =3D url + '&mrwAid=3D' + mrwParamArr[7];=0A= url =3D url + '&mrwVersion=3D' + mrwParamArr[8];=0A= var mrwFileParam =3D mrwParamArr[9];=0A= var seploc =3D mrwFileParam.indexOf("#");=0A= if (seploc !=3D -1)=0A= {=0A= url =3D url + '&mrwSection=3D' + = mrwFileParam.substring(seploc+1);=0A= url =3D url + '&mrwDocType=3D' + = mrwFileParam.substring(0,seploc);=0A= }=0A= else=0A= {=0A= url =3D url + '&mrwDocType=3D' + mrwFileParam;=0A= }=0A= }=0A= }=0A= }=0A= }=0A= =0A= //checking if a html file exists in the url=0A= var tmpfname =3D location.href;=0A= var loc =3D tmpfname.indexOf("?");=0A= if (loc !=3D -1)=0A= {=0A= tmpfname =3D tmpfname.substring(0,loc);=0A= }=0A= loc =3D tmpfname.indexOf(".html");=0A= if (loc !=3D -1)=0A= {=0A= loc =3D tmpfname.lastIndexOf("/");=0A= if (loc !=3D -1)=0A= {=0A= tmpfname =3D tmpfname.substring(loc+1);=0A= url =3D url + '¤tFile=3D' + tmpfname;=0A= }=0A= }=0A= =0A= if (arguments.length>=3D7 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return hwnd; } =0A= function pagetitle() {return 'Brain Pathology Vol. 19, 4 Pages: = 674-693'; } =0A= function dochead(hwnd, spec) {var title =3D pagetitle(); = hwnd.document.open(); = hwnd.document.write(''+spec+title+''); } =0A= function doctail(hwnd) {hwnd.document.write(''); } =0A= function pagehead(hwnd) {hwnd.document.write('

3D"About

Online ISSN: = 1096-9896 Print ISSN: 0022-3417
The Journal of = Pathology
Volume 214, Issue 3, 2008. Pages: 328-336

Copyright =C2=A9 2007 Pathological Society of Great = Britain and Ireland. Published by John Wiley & Sons, Ltd.

'); } =0A= function copyright(hwnd) {var title =3D pagetitle(); = hwnd.document.write(title.bold() + '
Copyright Journal compilation = © 2009 International Society of Neuropathology

'); } =0A= function imagelink(hwnd, iname) {if (iname.indexOf(' ') > -1) {var = images =3D iname.split(' ');for (var i =3D 0; i < images.length; ++i) = {hwnd.document.write('

');}} = else {hwnd.document.write('

');}}=0A= function otherlinks(hwnd, iname, size) { hwnd.document.write('View List of Images = '); hwnd.document.write('

'); } =0A= =0A= =0A= function caption_f1(hwnd) = {hwnd.document.write('Figure 1. Central role of = dendritic cells (DCs) in the initiation of an immune response. DCs are = present in virtually all tissues and organs including the brain and = continuously monitor their environment for the presence of danger, for = example, invading microorganisms and tissue damage. Immature DCs are = very efficient in antigen uptake, mediated by high endocytotic activity = and expression of an array of cell surface receptors. Upon recognition = of danger signals, DCs undergo maturation and migrate via lymph vessel = (LV) to the draining lymphoid organs. Here, mature DCs interact with and = activate naive lymphocytes specific for their cognate antigen and = initiate a primary immune response. After expansion, activated T = effector cells (Teffs) and natural killer/natural killer T cells (NK/NKT = cells) exit the lymphoid tissue and home back via the blood stream to = the site of antigen deposit to eliminate the threat in the endangered = tissue (eg, brain). Under steady state conditions immature, = non-activated DCs contribute to immune homeostasis by deleting = autoreactive T cells and inducing T-cell tolerance, or leading to the = generation of regulatory T cells (Tregs).'); }=0A= function display_f1(size) { var i =3D new Array(); i[0] =3D 'nf1'; i[1] = =3D 'nf1'; var hwnd =3D newfigwin(); dochead(hwnd, ''); copyright(hwnd); = otherlinks(hwnd, 'f1', size); imagelink(hwnd, i[size]); = caption_f1(hwnd); doctail(hwnd); hwnd.document.close(); hwnd.focus(); }=0A= function caption_f2(hwnd) = {hwnd.document.write('Figure 2. Toll-like receptor = (TLR)-mediated recognition of pathogen-associated molecular patterns = (PAMPs) and signaling pathways. TLR1, 2, 4, 5 and 6 are expressed on the = surface of dendritic cells, and are involved in detecting lipids, = carbohydrates and protein ligands from extracellular pathogens. In = contrast, TLR3, 7, 8 and 9 are mainly expressed in intracellular = vesicles and function within the acidified endosomes to detect nucleic = acids derived from viruses and bacteria. TLR2 recognizes bacterial = lipoproteins, peptidoglycan and lipoteichoic acid from Gram-positive = bacteria, and zymosam from fungi, and can associate with TLR1 and TLR6 = for functional responses to mycobacterial lipopeptides. TLR3 recognizes = viral double-stranded (ds) RNA and synthetic dsRNAs, such as = polyinosinic-polycytidylic acid (Poly I:C). TLR4 binds = lipopolysaccharides (LPS) from Gram-negative bacteria and viral envelope = proteins, whereas TLR5 recognizes flagellin. TLR7 and TLR8 recognize = viral single-stranded (ss) RNA and synthetic molecules like = imidazoquinoline or its derivates. TLR9 recognizes unmethylated CpG = motifs within bacterial and viral DNA. TLR3 uses Toll/Interleukin-1 = receptor (TIR) domain-containing adapter-inducing interferon (TRIF), = whereas all other TLRs use MyD88 as an adapter molecule. Both TRIF and = MyD88-dependent pathways lead to the activation of MAPK kinases such as = p38 and the activation of nuclear factor-κB (NF κB) and = interferon (IFN)-regulatory factors (IRFs) to induce type I IFN and = inflammatory cytokines, respectively.'); }=0A= function display_f2(size) { var i =3D new Array(); i[0] =3D 'nf2'; i[1] = =3D 'nf2'; var hwnd =3D newfigwin(); dochead(hwnd, ''); copyright(hwnd); = otherlinks(hwnd, 'f2', size); imagelink(hwnd, i[size]); = caption_f2(hwnd); doctail(hwnd); hwnd.document.close(); hwnd.focus(); }=0A= function caption_f3(hwnd) = {hwnd.document.write('Figure 3. Dendritic cell = (DC)-mediated T-cell polarization. After activation of Toll-like = receptors (TLRs) by pathogens (in green) DCs increase cell-surface = expression of MHC-peptide complexes, upregulate costimulatory molecules = (eg, CD86) and secrete immunomodulatory cytokines that direct T-cell = polarization. Ligation of distinct TLRs trigger differential cytokine = production in DCs. Production of interleukin-4 (IL-4) promotes the = development of T helper type 2 (Th2) cells, whereas the production of = IL-12 favors the development of Th1 cells. Th2 cells secrete IL-4, IL-5, = IL-10 and IL-13, whereas Th1 cells secrete IL-2 and IFN-γ. IL-4 = and IL-12 enhance the generation of their own Th-subset and = simultaneously inhibit the generation of the opposing subset. A = combination of IL-1 or IL-6 and TGF-s contributes to the development of = Th17 cells from naive precursors, whereas TGF-s alone promotes the = development of regulatory T cells (Tregs). Both IL-4 and IFN-γ = inhibit Th17 development. IL-6 inhibits the development of Tregs. Black = arrows indicate promoting activity, whereas red lines indicate = inhibitory activity.'); }=0A= function display_f3(size) { var i =3D new Array(); i[0] =3D 'nf3'; i[1] = =3D 'nf3'; var hwnd =3D newfigwin(); dochead(hwnd, ''); copyright(hwnd); = otherlinks(hwnd, 'f3', size); imagelink(hwnd, i[size]); = caption_f3(hwnd); doctail(hwnd); hwnd.document.close(); hwnd.focus(); }=0A= function caption_f4(hwnd) = {hwnd.document.write('Figure 4. Regulatory T cells = (Tregs) and immune cell suppression. Tregs are characterized by a set of = markers (in blue), suppress different types of immune cells (red lines) = and show their suppressive effects by a number of different mechanisms = (orange box). Tregs have cytolytic activity and can kill target cells = directly in a granzyme/perforin-dependent manner or induce cytokine = deprivation-mediated apoptosis. Two ectoenzymes, CD39 and CD73, = expressed on activated Tregs, induce the extracellular release of = adenosine nucleosides that suppress effector T-cell functions. Tregs = also promote the transfer of the potent inhibitory second messenger = cyclic adenosine monophosphate (cAMP) to effector T cells. In addition, = Tregs can condition DCs, via a CTLA-4:CD80/CD86-dependent mechanism, to = express indoleamine 2,3-dioxygenase (IDO). Expression of the lymphocyte = activation gene 3 (LAG3) on Tregs can further modulate the maturation = and immunostimulatory capacity of DCs. Finally, potent inhibitory = cytokines, produced by Tregs, such as membrane-bound or soluble TGF-s = (mTGF-s; sTGF-s), IL-10 or IL-35, contribute to their suppressive = function.'); }=0A= function display_f4(size) { var i =3D new Array(); i[0] =3D 'nf4'; i[1] = =3D 'nf4'; var hwnd =3D newfigwin(); dochead(hwnd, ''); copyright(hwnd); = otherlinks(hwnd, 'f4', size); imagelink(hwnd, i[size]); = caption_f4(hwnd); doctail(hwnd); hwnd.document.close(); hwnd.focus(); }=0A= function caption_f5(hwnd) = {hwnd.document.write('Figure 5. Immune escape = mechanisms of diffuse gliomas. Once antigen-specific effector T cells = (Teffs) reach the central nervous system (CNS) parenchyma through the = intact or disrupted blood–brain barrier (BBB) (1), they = may face regulation by CNS-residents cells such as astrocytes and = microglial cells that are able to inhibit T-cell proliferation and to = induce T-cell apoptosis by the secretion of immunosuppressive molecules = and the expression of death receptors ligands such as FasL (2). = Constitutive immunosuppressive factors in the brain parenchyma such as = TGF-s may also impede T-cell differentiation or T-cell effector = functions (3). Within the tumor, Teffs are confronted with = different subpopulations of immune suppressor cells that are attracted = to the tumor site, such as regulatory T cells (Tregs), myeloid-derived = suppressor cells (MDSCs) and mesenchymal stem cells (MSCs). Moreover, = tumor-infiltrating Teffs are exposed to high concentrations of = tumor-derived soluble immunosuppressive factors as well as = immunoinhibitory surface molecules expressed on the tumor cells = (4). Finally, efficient immune recognition of glial brain tumor = cells may be compromised by low MHC molecule expression and inefficient = processing and presentation of tumor-associated antigens (5). = Adapted from Walker et al (2002) (274).'); }=0A= function display_f5(size) { var i =3D new Array(); i[0] =3D 'nf5'; i[1] = =3D 'nf5'; var hwnd =3D newfigwin(); dochead(hwnd, ''); copyright(hwnd); = otherlinks(hwnd, 'f5', size); imagelink(hwnd, i[size]); = caption_f5(hwnd); doctail(hwnd); hwnd.document.close(); hwnd.focus(); }=0A= function caption_f6(hwnd) = {hwnd.document.write('Figure 6. Principles of dendritic = cell (DC) vaccination and further strategies to improve immunotherapy of = diffuse gliomas. The most common method used to generate ex vivo = DCs for vaccination is to culture autologous monocytes obtained from = leukapheresis in the presence of granulocyte monocyte colony-stimulating = factor (GM-CSF) and IL-4. Following 5–7 days in culture, the = monocytes differentiate into immature DCs. DC maturation is induced by = culturing immature DCs for an additional 24–48 hours in the = presence of a maturation cocktail, most commonly consisting of = TNF-α, IL-1β, IL-6 and PGE2, also known as = monocyte-conditioned medium. Tumor antigen loading with tumor lysate, = tumor RNA or synthetic tumor-specific peptides occurs at either the = immature or mature DC stage. Finally, mature tumor antigen-loaded DCs = are injected back into patients. Critical issues to enhance the = persistence of the vaccine-induced immune responses for future = immunotherapeutic approaches against diffuse gliomas are to improve the = immunogenicity of a DC vaccine and to break the local immunosuppressive = environment of diffuse gliomas. Toll-like receptor (TLR) agonists, = activation of costimulatory receptors, blockade of co-inhibitory = receptors and/or depletion or modulation of regulatory T cells (Treg) = could all be used to intensify antiglioma immune responses induced by = peripheral DC vaccinations. In addition, immunosuppressive molecules = could be targeted directly within the tumor microenvironment to enhance = treatment efficacy. Peri- or intratumoral administration of distinct TLR = agonists might serve as an additional option to activate local immune = cells and to potentiate antitumor immunity. Abbreviation: = BBB =3D blood–brain barrier; Teff =3D T = effector cells.'); }=0A= function display_f6(size) { var i =3D new Array(); i[0] =3D 'nf6'; i[1] = =3D 'nf6'; var hwnd =3D newfigwin(); dochead(hwnd, ''); copyright(hwnd); = otherlinks(hwnd, 'f6', size); imagelink(hwnd, i[size]); = caption_f6(hwnd); doctail(hwnd); hwnd.document.close(); hwnd.focus(); }=0A= =0A= =0A= function imagelist() {var hwnd =3D newfigwin(); dochead(hwnd, 'List of = Images - '); copyright(hwnd); =0A= hwnd.document.write('');=0A= =0A= =0A= hwnd.document.write('');=0A= hwnd.document.write('');=0A= hwnd.document.write('');=0A= hwnd.document.write('');=0A= hwnd.document.write('');=0A= hwnd.document.write('');hwnd.document.write('

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Brain Pathology

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Volume 19, Issue 4, Pages 674-693

Published Online: 4 Sep 2009

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MINI-SYMPOSIUM: Immunotherapy of = Gliomas

Immunotherapy of Diffuse Gliomas: = Biological=20 Background, Current Status and Future Developments

Oliver=20 M. Grauer, MD, PhD ^1,3 = ;=20 Pieter Wesseling, MD, = PhD=20 ^2,4 ; Gosse J. Adema, PhD ¹ =

¹ Departments = of Tumor=20 Immunology, ² Pathology,=20 Nijmegen Centre for Molecular Life Sciences, Radboud University = Nijmegen=20 Medical Centre;
⁴ Department of = Pathology, Canisius Wilhelmina Hospital, Nijmegen, the = Netherlands.=20
= ³ Department of = Neurology, University Medical Centre Regensburg, Regensburg,=20 Germany.

Correspondence to Gosse = J. Adema, PhD,=20 Tumor Immunology Laboratory, Radboud University Nijmegen Medical = Centre,=20 PO Box 9101, 6500 HB Nijmegen, the Netherlands (E-mail: G.Adema@ncmls.ru.nl)=20

Disclosure of potential conflicts of interest: Authors = have no=20 relevant conflicts of interest to disclose. =

Copyright Journal compilation =A9 2009 = International Society of Neuropathology

KEYWORDS

central nervous system =95 dendritic cell = =95 glioma =95=20 immune escape =95 immunotherapy =95 vaccine

ABSTRACT

3DAbstract=20

Despite aggressive multimodal treatment = approaches, the=20 prognosis for patients with diffuse gliomas remains disappointing. = Glioma=20 cells often extensively infiltrate in the surrounding brain = parenchyma, a=20 phenomenon that helps them to escape surgical removal, radiation = exposure=20 and chemotherapy. Moreover, conventional therapy is often = associated with=20 considerable local and systemic side effects. Therefore, the = development=20 of novel therapeutic approaches is essential to improve the = outcome of=20 these patients. Immunotherapy offers the opportunity to = specifically=20 target residual radio=97and chemoresistant tumor cells without = damaging=20 healthy neighboring brain tissue. Significant progress has been = made in=20 recent years both in understanding the mechanisms of immune = regulation in=20 the central nervous system (CNS) as well as tumor-induced and=20 host-mediated immunosuppression elicited by gliomas. In this = review, after=20 discussing the special requirements needed for the initiation and = control=20 of immune responses in the CNS, we focus on immunological = phenomena=20 observed in glioma patients, discuss different immunological = approaches to=20 attack glioma-associated target structures and touch on further = strategies=20 to improve the efficacy of immunotherapy of = gliomas.

Received 5 June 2009; accepted 9 June = 2009.

DIGITAL OBJECT IDENTIFIER (DOI)

10.1111/j.1750-3639.2009.00315.x About=20 DOI

=20

=20

=20

INTRODUCTION

Gliomas are the most common primary brain tumors = in adults.=20 They are categorized according to the World Health Organization = (WHO)=20 classification, most recently revised in 2007 (162).=20 Most gliomas, the "diffuse gliomas," are characterized by = extensive=20 infiltration of brain parenchyma. The diffuse gliomas can be = subtyped as=20 astrocytic, oligodendroglial and oligoastrocytic tumors, with a = malignancy=20 grade (low grade =3D WHO grade II; = malignant =3D WHO grade=20 III; highly malignant =3D WHO grade IV) assigned to each = tumor (162).=20 The most aggressive, that is WHO grade IV diffuse glioma, is = glioblastoma=20 (GBM). Although GBMs are generally considered purely astrocytic in = nature,=20 they in fact form a heterogeneous group of tumors, representing = 15%=9620% of=20 all intracranial neoplasms and approximately 50% of the malignant = gliomas.=20 As most studies on the immunobiology and immunotherapy of gliomas = were=20 carried out on diffuse gliomas, especially GBMs, the present = review=20 focuses on these tumors as well. Currently the standard of care = for=20 patients with GBM after maximal tumor resection is concomitant=20 chemoradiotherapy followed by adjuvant treatment with temozolomide = (TMZ).=20 The median overall survival for patients with GBM is 14.6 months = and the=20 overall survival rate is 27.2% at 2 years. After 3 years, nearly = all=20 patients have progressed, with mortality well over 90% after 5 = years (249,=20 250). Factors associated with an increased risk of death are = increased=20 age, lower Karnofsky performance score (KPS), corticosteroid use, = shorter=20 time from original diagnosis to recurrence, tumor outside the = frontal=20 lobe, unmethylated O6-methylguanine methyltransferase = (MGMT)-promotor=20 status and the presence of tumor-initiating glioma stem cells (40,=20 100, 196, 299). Overall, the prognosis for patients with GBM = remains=20 poor. It is thus essential to consider novel treatments in the = hope of=20 attacking residual radio- and chemoresistant tumor cells and to = improve=20 the survival of glioma patients. With increasing knowledge of = central=20 nervous system (CNS) immunity, immunotherapeutic approaches are = promising=20 options for the treatment of diffuse gliomas.

=20

=20

CENTRAL ROLE OF DENDRITIC CELLS = (DCs) IN THE=20 ACTIVATION OF THE IMMUNE SYSTEM

In general, the immune system is based on two = distinct types=20 of responses, the innate and the adaptive immune response. The = innate=20 immune system functions as a first line of defense against = invading=20 microorganisms. It discriminates between the different microbes by = recognizing a set of conserved molecular structures, so called=20 pathogen-associated molecular patterns (PAMPs), shared by large = groups of=20 microorganisms. Cells that orchestrate the innate immune response = are DCs,=20 macrophages, monocytes, granulocytes and natural killer (NK) = cells. The=20 specific, adaptive immune system forms the second line of defense, = which=20 depends on the activity of effector T and B cells. It uniquely=20 distinguishes distinct microorganisms and confers immunological = memory.=20 The specifity is mediated by membrane receptors bearing a great = diversity=20 of antigen binding sites.

=20

=20

DC subsets

DCs are the professional antigen-presenting cells = (APCs) of=20 the immune system that instruct and control primary immune = responses. Two=20 major subtypes of DCs have been defined, myeloid and plasmacytoid = DCs.=20 Both DC subsets differ in morphology, tissue distribution, = expression of=20 markers and function (270).=20 Plasmacytoid DCs are circulating cells with a plasmacytoid = morphology that=20 are capable of producing large amounts of type I interferons upon=20 activation by microbial stimuli (242).=20 In addition, they can differentiate into DCs that are capable of=20 activating naive T cells against allo-antigens (91)=20 and exogenous antigens (22).=20 Myeloid DCs can be further divided into migratory DCs, which serve = as=20 sentinels of the immune system in peripheral tissues and present = foreign=20 antigens to T cells after migration to the draining lymph nodes, = and=20 lymphoid-tissue-resident DCs that capture local (foreign and = self-)=20 antigens and present them to local T cells (238).

=20

=20

Migratory DCs

At an immature stage, myeloid DCs take up tissue = antigens,=20 both soluble and particulate antigens, very efficiently. After = challenge=20 with microbial or inflammatory ("danger"-associated) stimuli, DCs = undergo=20 a process of activation, also known as maturation. Several = environmental=20 stimuli, such as signals from pattern-recognition receptors (PPR), = inflammatory cytokines and members of the TNF superfamily (eg, = CD40L,=20 RANKL) have been shown to mediate DC activation (246).=20 During DC maturation, captured antigens are processed and bound to = both=20 classical major histocompatibility complex (MHC) class I and class = II=20 molecules that are translocated to the cell surface, accompanied = by an=20 increased expression of costimulatory molecules and the secretion = of=20 cytokines that influence T cell proliferation and differentiation. = In=20 response to the appropriate stimuli, DCs also upregulate CC = chemokine=20 receptor-7 (CCR7), a receptor that drives DC migration to the = lymphoid=20 vessels and T cell areas of secondary lymphoid organs (13).=20 There, DCs are mature and are well-equipped to attract and = activate naive=20 CD4+ and CD8+ T cells (3)=20 In addition, DCs are also able to directly activate innate = lymphocytes=20 such as NK cells or NKT cells via non-classical (CD1 family) MHC = molecules=20 presenting glycolipid structures (68,=20 72), thus providing a link between the adaptive and innate = immune=20 system (Figure 1).

=20

= Figure 1. Central=20 role of dendritic cells (DCs) in the initiation of an immune = response. DCs are present in virtually all tissues and = organs=20 including the brain and continuously monitor their = environment for=20 the presence of danger, for example, invading microorganisms = and=20 tissue damage. Immature DCs are very efficient in antigen = uptake,=20 mediated by high endocytotic activity and expression of an = array of=20 cell surface receptors. Upon recognition of danger signals, = DCs=20 undergo maturation and migrate via lymph vessel (LV) to the = draining=20 lymphoid organs. Here, mature DCs interact with and activate = naive=20 lymphocytes specific for their cognate antigen and initiate = a=20 primary immune response. After expansion, activated T = effector cells=20 (Teffs) and natural killer/natural killer T cells (NK/NKT = cells)=20 exit the lymphoid tissue and home back via the blood stream = to the=20 site of antigen deposit to eliminate the threat in the = endangered=20 tissue (eg, brain). Under steady state conditions immature,=20 non-activated DCs contribute to immune homeostasis by = deleting=20 autoreactive T cells and inducing T-cell tolerance, or = leading to=20 the generation of regulatory T cells (Tregs). =

[Normal=20 View ]

=20

=20

PPRs expressed by DCs

Four main PPRs expressed by DCs can be = distinguished. These=20 include Toll-like receptors (TLRs), C-type lectins, NOD-like = receptors and=20 cytoplasmic RNA helicases (149,=20 268).

So far, the best-characterized PPRs are the TLRs = (128,=20 154). The TLR family in humans consists of 11 transmembrane = members=20 that are located on the cell surface (TLR1, 2, 4, 5, 6, 10 and 11) = or=20 within the endosomal compartments (TLR3, 7, 8 and 9) (Figure 2).=20 Many specific ligands for TLRs have now been identified. TLR2 = recognizes=20 bacterial lipoproteins, peptidoglycan and lipoteichoic acid from=20 Gram-positive bacteria, and zymosam from fungi, and can associate = with=20 TLR1 and TLR6 for functional responses to mycobacterial = lipopeptides. TLR3=20 recognizes viral double-stranded (ds) RNA and synthetic dsRNAs, = such as=20 polyinosinic=96polycytidylic acid (Poly I:C). TLR4 binds = lipopolysaccharides=20 (LPS) from Gram-negative bacteria and viral envelope proteins, = whereas=20 TLR5 recognizes flagellin. TLR7 and TLR8 recognize viral single = stranded=20 RNA and synthetic molecules like imidazoquinoline or its = derivates. TLR9=20 recognizes unmethylated CpG motifs within bacterial and viral DNA. = The=20 specific ligand of TLR10 is currently unknown. The recently = discovered=20 TLR11 recognizes uropathogenic bacteria (117,=20 254). TLR expression by DCs is dependent on the cellular = subset and=20 differentiation state. Myeloid DCs express virtually all TLRs with = the=20 exception of TLR9, which is selectively expressed by plasmacytoid = DCs. In=20 contrast to humans, TLR9 is expressed both by plasmacytoid and = myeloid DCs=20 in mice (212).=20 Importantly, DC activation and cytokine production are strongly = dependent=20 on the type and combination of the TLRs that are triggered (121,=20 183). Consequently, the nature of specific T-cell responses = generated=20 also depends on the different stimuli that a DC encounters locally = (244).

=20

= Figure 2. Toll-like = receptor=20 (TLR)-mediated recognition of pathogen-associated molecular = patterns=20 (PAMPs) and signaling pathways. TLR1, 2, 4, 5 and 6 are = expressed on=20 the surface of dendritic cells, and are involved in = detecting=20 lipids, carbohydrates and protein ligands from extracellular = pathogens. In contrast, TLR3, 7, 8 and 9 are mainly = expressed in=20 intracellular vesicles and function within the acidified = endosomes=20 to detect nucleic acids derived from viruses and bacteria. = TLR2=20 recognizes bacterial lipoproteins, peptidoglycan and = lipoteichoic=20 acid from Gram-positive bacteria, and zymosam from fungi, = and can=20 associate with TLR1 and TLR6 for functional responses to=20 mycobacterial lipopeptides. TLR3 recognizes viral = double-stranded=20 (ds) RNA and synthetic dsRNAs, such as = polyinosinic-polycytidylic=20 acid (Poly I:C). TLR4 binds lipopolysaccharides (LPS) from=20 Gram-negative bacteria and viral envelope proteins, whereas = TLR5=20 recognizes flagellin. TLR7 and TLR8 recognize viral = single-stranded=20 (ss) RNA and synthetic molecules like imidazoquinoline or = its=20 derivates. TLR9 recognizes unmethylated CpG motifs within = bacterial=20 and viral DNA. TLR3 uses Toll/Interleukin-1 receptor (TIR)=20 domain-containing adapter-inducing interferon (TRIF), = whereas all=20 other TLRs use MyD88 as an adapter molecule. Both TRIF and=20 MyD88-dependent pathways lead to the activation of MAPK = kinases such=20 as p38 and the activation of nuclear factor-κB (NF = κB) and=20 interferon (IFN)-regulatory factors (IRFs) to induce type I = IFN and=20 inflammatory cytokines, respectively.

[Normal=20 View ]

=20

=20

T-cell polarization

Inside the lymph nodes, antigen-loaded activated = DCs=20 interact with naive T cells and induce their differentiation into = T=20 effector cells. It is a unique feature of DCs to efficiently = present=20 captured antigens on MHC class-II molecules to CD4+ T cells. Naive = CD4+ T=20 cells can be differentiated into either T-helper type 1 (Th1), = T-helper=20 type 2 (Th2) or TH17 cells. Th1 cells develop in the presence of=20 interleukin 12 (IL-12) and secrete IFN-γ, whereas Th2 cells = develop in the=20 presence of IL-4 and secrete IL-4, IL-5 and IL-13 (191,=20 256). For the development of TH17 cells from naive precursors = a=20 combination of IL-6 and TGF-β is required (23).=20 Moreover, IL-1 and IL-21 seem to play important roles in promoting = the=20 induction of TH17 cells, whereas IL-23 is vital for the expansion = and=20 survival of this population (24,=20 143, 148). In contrast to other APCs, DCs are also capable of=20 presenting captured antigens on MHC class-I molecules to CD8+ T = cells, a=20 process termed "cross-presentation"(5,=20 132). In vivo priming of CD8+ cytotoxic = T=20 lymphocytes (CTLs) generally requires the participation of CD4+ = T-helper=20 cells, CD40-CD40L interaction, innate lymphocytes or stimulation = via=20 certain TLRs (121,=20 160, 233). Besides effector T cells, DCs are also efficient at = activating naturally occurring CD4+ regulatory T cells (Tregs) (14,=20 130, 295). In addition, DCs are able to induce several subsets = of=20 Tregs capable of controlling effector T cells, including induced = Tregs,=20 type 1 regulatory T cells (Tr1 cells) and Th3 cells. The = regulatory=20 T-cell-polarizing factors are IL-10 and transforming growth = factor-β=20 (TGF-β) (44,=20 65, 273) (Figure 3).

=20

= Figure 3. Dendritic cell=20 (DC)-mediated T-cell polarization. After activation of = Toll-like=20 receptors (TLRs) by pathogens (in green) DCs increase = cell-surface=20 expression of MHC-peptide complexes, upregulate = costimulatory=20 molecules (eg, CD86) and secrete immunomodulatory cytokines = that=20 direct T-cell polarization. Ligation of distinct TLRs = trigger=20 differential cytokine production in DCs. Production of = interleukin-4=20 (IL-4) promotes the development of T helper type 2 (Th2) = cells,=20 whereas the production of IL-12 favors the development of = Th1 cells.=20 Th2 cells secrete IL-4, IL-5, IL-10 and IL-13, whereas Th1 = cells=20 secrete IL-2 and IFN-γ. IL-4 and IL-12 enhance the = generation of=20 their own Th-subset and simultaneously inhibit the = generation of the=20 opposing subset. A combination of IL-1 or IL-6 and TGF-s = contributes=20 to the development of Th17 cells from naive precursors, = whereas=20 TGF-s alone promotes the development of regulatory T cells = (Tregs).=20 Both IL-4 and IFN-γ inhibit Th17 development. IL-6 = inhibits the=20 development of Tregs. Black arrows indicate promoting = activity,=20 whereas red lines indicate inhibitory activity.=20

[Normal View=20 ]

=20

=20

Naturally occurring CD4+ regulatory = T=20 cells

Naturally occurring CD4+ Tregs represent 5%=9610% = of the=20 overall CD4+ T cell population and are generated in the thymus (223).=20 They constitutively express the IL-2 receptor α-chain (CD25), = cytotoxic=20 lymphocyte-associated antigen-4 (CTLA-4) and different members of = the=20 tumor necrosis factor (TNF) receptor superfamily such as the=20 glucocorticoid-induced TNF related protein (GITR) or Ox40 (237,=20 265). Other candidate markers of Tregs have been described and = currently include CD62L, CD103, CD122 and CD223 (178).=20 So far the most specific marker for naturally occurring CD4+ Tregs = is=20 FoxP3, a member of the forkhead family of DNA-binding = transcription=20 factors, which has been shown to be expressed specifically in = mouse CD4+=20 Tregs and acts as a master switch in the regulation of their = development=20 and function (71,=20 105). Per se, Tregs are hyporesponsive to T-cell receptor = (TCR)=20 stimulation in vitro, but high amounts of = IL-2 or=20 stimuli bypassing the TCR can overcome their anergic state (224).=20 After polyclonal or antigen-specific TCR stimulation, Tregs = potently=20 suppress the proliferation and cytokine production of effector = CD4+ and=20 CD8+ T cells by inhibiting IL-2 gene transcription. Once activated = in an=20 antigen-specific manner, Tregs also suppress effector T cells, = which are=20 specific for other antigens. Furthermore, Tregs have been shown to = inhibit=20 the proliferation and antibody production of B cells and to = profoundly=20 suppress NK-cell function (33,=20 77). Tregs show their suppressive effects by a complex and = overlapping=20 set of mechanisms (225)=20 (Figure 4).

=20

= Figure 4. Regulatory T = cells (Tregs)=20 and immune cell suppression. Tregs are characterized by a = set of=20 markers (in blue), suppress different types of immune cells = (red=20 lines) and show their suppressive effects by a number of = different=20 mechanisms (orange box). Tregs have cytolytic activity and = can kill=20 target cells directly in a granzyme/perforin-dependent = manner or=20 induce cytokine deprivation-mediated apoptosis. Two = ectoenzymes,=20 CD39 and CD73, expressed on activated Tregs, induce the=20 extracellular release of adenosine nucleosides that suppress = effector T-cell functions. Tregs also promote the transfer = of the=20 potent inhibitory second messenger cyclic adenosine = monophosphate=20 (cAMP) to effector T cells. In addition, Tregs can condition = DCs,=20 via a CTLA-4:CD80/CD86-dependent mechanism, to express = indoleamine=20 2,3-dioxygenase (IDO). Expression of the lymphocyte = activation gene=20 3 (LAG3) on Tregs can further modulate the maturation and=20 immunostimulatory capacity of DCs. Finally, potent = inhibitory=20 cytokines, produced by Tregs, such as membrane-bound or = soluble=20 TGF-s (mTGF-s; sTGF-s), IL-10 or IL-35, contribute to their=20 suppressive function.

[Normal View=20 ]

=20

=20

THE CNS=97AN IMMUNOLOGICALLY = SPECIALIZED=20 SITE

In the past, the CNS has been described as an=20 immunologically privileged site based on the presence of the = blood=96brain=20 barrier (BBB), graft acceptance, lack of conventional lymphatics, = low MHC=20 expression and low T cell trafficking (41,=20 50). However, with recent advances in understanding CNS = immunity it is=20 more accurate to regard the CNS as an immunologically specialized = site=20 that can be divided into three different compartments: the brain=20 parenchyma; the ventricles containing choroid plexus and = cerebrospinal=20 fluid; and the meninges. The immune reactivity of the ventricles = and=20 meninges is similar to that of the periphery, whereas immune = responses are=20 delayed or even abrogated within the brain parenchyma (17,=20 248, 280).

=20

=20

Initiation of an immune response = in the=20 CNS

Accumulating data suggest that DCs play a central = role in=20 the initiation of immune responses in the CNS (135,=20 198). DCs can be found in low numbers in the meninges, = perivascular=20 spaces, the choroid plexus and in the CSF where they reside in an = immature=20 state (169,=20 172, 197).

Under non-inflammatory conditions, DCs present = antigens=20 derived from tissue debris and apoptotic cells in the absence of=20 costimulatory molecules. Such antigen presentation by = non-activated DCs=20 induces T-cell anergy, T-cell tolerance or the induction of Tregs = (159,=20 236, 247). Moreover, it has been reported that non-stimulated, = brain-derived DCs preferentially target B-cell areas instead of = T-cell=20 areas, again skewing the immune system towards a humoral response = (96).=20 Similarly, drainage of brain-derived antigens was shown not to be=20 sufficient to induce a Th1-type and CTL response by itself, but = leads to=20 tolerance induction or skewing of the immune response towards a B = cell and=20 Th2-type response (94,=20 95, 283). However, under a variety of inflammatory conditions, = DCs are=20 quickly recruited to the site of the brain lesion and appear in = both the=20 brain parenchyma and the cerebrospinal fluid in high numbers (69,=20 157, 235). Importantly, it was recently demonstrated that = these DCs do=20 not differentiate from CNS-resident precursors like microglia = cells, but=20 are of peripheral origin (175).=20 At the site of the lesion, inflammatory mediators and danger = signals=20 promote maturation and rerouting of DCs to the secondary lymphoid = organs=20 where they prime antigen-specific immune responses.

Although conventional lymphatics are missing in = the CNS,=20 antigen-loaded DCs have access to secondary lymphoid organs = through=20 several pathways. The most prominent one is the drainage of = antigen-loaded=20 DCs along the subarachnoid space surrounding the olfactory bulbs = through=20 discrete channels in the cribriform plate into the lymphatics of = the nasal=20 submucosa and, subsequently, to the cervical lymph nodes. Regional = lymph=20 nodes that are associated with other cranial nerves might also be = involved=20 in the CNS drainage. With access to the cerebrospinal fluid and = the=20 perivascular spaces, antigen-loaded DCs can also migrate out = through the=20 arachnoid villi into the venous blood (103,=20 208, 282).

These data further support recent analyses = demonstrating=20 that brain-derived antigens can reach the cervical lymph nodes = very=20 quickly, but similar to the skin system, a second wave of incoming = brain-derived APCs, most likely DCs, is necessary for optimal = T-cell=20 activation (80,=20 119, 135). After clonal expansion, activated antigen-specific = T cells=20 preferentially home back to the site of antigen deposit in the = brain (34,=20 35).

=20

=20

T cell trafficking into the = CNS

In general, the traffic of leukocytes into the CNS = is a=20 highly regulated process. Resting T cells fail to enter the CNS, = whereas=20 activated T cells are able to penetrate the BBB under inflammatory = conditions (279,=20 281). For CD4+ T cells, the activation-stage rather than the=20 antigen-specificity determines BBB crossing (102).=20 CNS recruitment of CD8+ T cells is regulated differently than CD4+ = T=20 cells. Recent data show that antigen specificity is a factor that = governs=20 CD8+ T cell infiltration into the brain and that this process is = dependent=20 on luminal expression of MHC class I by cerebral endothelium, but=20 independent of antigen presentation by perivascular APCs (75).

The current paradigm of blood leukocyte = transendothelial=20 migration involves a sequential, multistep adhesion cascade = between=20 leukocyte and endothelial cell adhesion molecules (19,=20 63). T-cell priming in CNS-draining lymph nodes is usually = associated=20 with a rapid upregulation of α4 and β1 integrin (35).=20 These α4β1 integrins have been shown to interact with = VCAM-1 on cerebral=20 vascular endothelium and this interaction has been reported to = facilitate=20 CNS entry of encephalitogenic or virus-specific T cells (39,=20 264). An important function for ALCAM in the recruitment of = CD4+ T=20 cells and monocytes across the BBB endothelium has recently been=20 demonstrated (43).=20 After CNS entry, antigen-specific reactivation of effector T cells = by=20 perivascular APCs is needed for T-cell persistence and = amplification of=20 T-cell-mediated immune responses in the CNS. In general, those T = cells=20 that have encountered their target antigen within the brain are = retained=20 for longer periods within the CNS (168).

After contact with perivascular APCs, effector T = cells=20 undergo rapid reactivation with renewed induction of activation = markers=20 such as CD25 and CD134 (OX-40) (49,=20 90, 136). Moreover, CD8+ T cells further differentiate in the = brain,=20 showing enhanced IFN-γ and granzyme B expression and = induction of αEβ7=20 integrin, mediating increased adhesion to the brain parenchyma (168).=20 Finally, effector T cells migrate to the site of the brain lesion = towards=20 a chemotactic gradient. Chemokines such as monocyte = chemoattractant=20 protein (MCP)-1 also induce the expression of matrix = metalloproteinases=20 and other ectoenzymes that enable penetration of effector T cells = into the=20 brain parenchyma (6,=20 11).

=20

=20

Perivascular macrophages and = parenchymal=20 microglial cells

Next to the DCs, two other major populations of = phagocytic=20 cells of myeloid origin function as APCs in the CNS: perivascular=20 macrophages and parenchymal microglia cells. Based on their = morphology and=20 immunophenotype, perivascular macrophages appear to be very = similar to=20 blood-derived macrophages (228).=20 Moreover, it has been shown that brain perivascular cells contain = a=20 population of replaceable, rather than resident phagocytic cells = (18).

Microglial cells are the primary immunocompetent = cells in=20 the brain. In addition to their phagocytic function, they may also = participate in the regulation of innate and adaptive immune = responses.=20 They show a very low turnover rate and remain in an = undifferentiated state=20 with little expression of MHC class II under steady-state = conditions. Upon=20 activation, microglial cells can quickly upregulate their antigen=20 presenting capabilities in response to inflammatory or microbial = stimuli=20 both in vitro and in = vivo; they=20 can also develop into more DC-like cells (70,=20 195, 227). However, even upon full activation, the expression = levels=20 of MHC and costimulatory molecules on DC-like microglial cells are = much=20 lower than generally found on DCs. Furthermore, CNS-resident = microglial=20 cells purified from the inflamed CNS were found to be largely = incapable of=20 activating either naive or effector T cells (CD4+ T helper cells), = in=20 contrast to peripherally derived myeloid DCs (171,=20 175). In addition, there are currently no data available on = the=20 ability of microglial cells to migrate out of the CNS in = significant=20 numbers and present antigens in the draining lymph nodes. Instead = of=20 T-cell priming, both cell types might play a direct role in = reshaping the=20 function CD8+ effector T cells or a more indirect role in the = conditioning=20 of the DC precursors to differentiate into DCs (136,=20 168).

=20

=20

Control of immune responses in the = CNS

The time of onset, the intensity and duration of = immune=20 responses within the CNS have to be tightly controlled; otherwise=20 permanent tissue damage can occur. Immunosuppressive Tregs have = been shown=20 to be essential for the control of immune pathology. It has been = reported=20 that, similar to effector T cells, Tregs traffic to the inflamed = site=20 within the CNS, become reactivated, and further expand in=20 situ. Interestingly, it has been shown that Tregs are not=20 functional at the disease peak of experimental autoimmune=20 encephalomyelitis (EAE). However, in the recovery phase, Tregs = regain=20 suppressor activity and potently curb the autoimmune responses = locally (144,=20 190). Moreover, it was recently demonstrated that CNS DCs show = a dual=20 role during the disease course of an EAE: these cells promote CNS=20 inflammation at the onset of the disease, whereas by the peak of = the=20 disease, they lose their optimal T-cell stimulatory capacity and = support=20 Treg-mediated immunosuppression to limit the extent of CNS = inflammation (58).

=20

=20

INTERACTION OF MALIGNANT GLIOMA = AND THE IMMUNE=20 SYSTEM

=20

=20

Immune cell infiltrates

The immune recognition of glial tumors arising = within the=20 brain is usually prevented at the earliest stages of neoplastic=20 transformation where the tumor cells are totally contained within = the=20 normal brain parenchyma. As such, primary brain tumors present a = unique=20 challenge for CNS immunosurveillance. However, at later stages of = tumor=20 growth, when massive tissue damage with destruction of the BBB and = tumor=20 cell necrosis with antigen drainage to the periphery occurs, brain = tumors=20 become accessible to the peripheral immune system. In this case, = albeit at=20 varying degrees, immune cell infiltrates can regularly be found = within=20 malignant gliomas. The vast proportion of immune cells, mainly=20 macrophages, microglial cells, DCs and T cells, is found at = perivascular=20 regions, but can also be observed throughout the tumor bed and = within=20 necrotic tissue regions (110,=20 199, 216, 272). Attraction of these immune cells is directed = by a=20 number of molecules, which are mainly produced by oxygen-deprived = tumor=20 cells surrounding necrosis. Hypoxia inducible factor-1α = (HIF-1α) has been=20 identified as a key factor in gliomas promoting the release of=20 chemoattractants, such as CXCL5, CXCL8/IL-8 and CXCL12/SDF-1 (57,=20 253). Other chemoattractants, such as CCL2/MCP-1, = CCL3/MIP1-α,=20 CCL4/MIP1-β, CCL22/MDC also contribute to the recruitment of = immune cells=20 to gliomas (56,=20 118, 252). However, early studies have already determined that = the=20 presence of immune cell infiltrates usually does not correlate = with the=20 clinical course of glioma patients or may even be a negative = prognostic=20 factor (217,=20 220, 221).

=20

=20

Immunosuppression elicited by = malignant=20 gliomas

Compelling evidence exists that immune activation = within=20 malignant gliomas is suppressed by the local tumor = microenvironment (61,=20 274, 275) (Figure 5).=20 Malignant gliomas are characterized by the presence of a large = number of=20 immunosuppressive soluble factors, such as vascular endothelial = growth=20 factor (VEGF), IL-10, TGF-β, whereas immunostimulatory = molecules, such as=20 IL-12, IL-18, INF-γ, are lacking. In addition, = immunosuppressive enzymes=20 such as indoleamin 2,3-dioxygenase (IDO), cyclooxygenase-2 = (COX-2),=20 arginase and nitric-oxide synthase-2 (NOS-2) are overexpressed in = glioma=20 cells (28,=20 32, 42, 48, 83, 185). Moreover, many immunoinhibitory = molecules are=20 abundantly expressed on the surface of glioma cells. Non-classical = MHC=20 ligands such as HLA-G and HLA-E (286,=20 290), co-inhibitory molecules such as PD-L1 (B7-H1) (288,=20 289), minor brain gangliosides such as GM2 and GM3 (88),=20 and galectin-1 and galectin-3, mammalian lectins with specificity = to=20 beta-galactosides have been detected (74,=20 218). Furthermore, inhibitory cytokine signaling molecules = such as=20 signal transducers and activators of transcription 3 (Stat3) are = known to=20 be constitutively activated in several human glioma cell lines, = promoting=20 tumor cell growth and survival (2,=20 142, 207).

=

= Figure 5. Immune=20 escape mechanisms of diffuse gliomas. Once antigen-specific = effector=20 T cells (Teffs) reach the central nervous system (CNS) = parenchyma=20 through the intact or disrupted blood=96brain barrier (BBB) = (1), they may face regulation by = CNS-residents cells=20 such as astrocytes and microglial cells that are able to = inhibit=20 T-cell proliferation and to induce T-cell apoptosis by the = secretion=20 of immunosuppressive molecules and the expression of death = receptors=20 ligands such as FasL (2). = Constitutive=20 immunosuppressive factors in the brain parenchyma such as = TGF-s may=20 also impede T-cell differentiation or T-cell effector = functions=20 (3). Within the tumor, Teffs are = confronted=20 with different subpopulations of immune suppressor cells = that are=20 attracted to the tumor site, such as regulatory T cells = (Tregs),=20 myeloid-derived suppressor cells (MDSCs) and mesenchymal = stem cells=20 (MSCs). Moreover, tumor-infiltrating Teffs are exposed to = high=20 concentrations of tumor-derived soluble immunosuppressive = factors as=20 well as immunoinhibitory surface molecules expressed on the = tumor=20 cells (4). Finally, efficient immune=20 recognition of glial brain tumor cells may be compromised by = low MHC=20 molecule expression and inefficient processing and = presentation of=20 tumor-associated antigens (5). = Adapted from=20 Walker et al (2002) (274).=20

[Normal View=20 ]

As a consequence, differentiation, maturation and = function=20 of tumor-infiltrating DCs and other APCs, as well as the = generation and=20 activation of immune effector cells are all profoundly suppressed = in the=20 tumor microenvironment. In addition, the cytolytic activity of=20 macrophages, NK cells and cytotoxic T cells is deeply disturbed (81,=20 111, 179, 239, 241), and other players in tumor-induced=20 immunosuppression are recruited to the tumor, preventing = tumor-specific=20 immunity. Among those are myeloid-derived suppressor cells, = representing a=20 phenotypically heterogeneous cell population that includes = immature=20 myelomonocytic cells, terminally differentiated monocytes and = granulocytes=20 (82,=20 203, 263), but also mesenchymal stem cells with = immunosuppressive=20 functions (26,=20 260). Recent studies clearly show that CD4+ Tregs infiltrate = and=20 fbaccumulate within gliomas (62,=20 125) and profoundly suppress antiglioma immune responses. = Also,=20 patients with malignant glioma show an elevated proportion of = Tregs in=20 peripheral blood in the setting of an overall diminished CD4+ = T-cell pool=20 (66).=20 This predominance of Tregs was shown to be responsible for the = multiple=20 immunological defects that have been previously described in = glioma=20 patients, including abnormal delayed hypersensitivity responses, = depressed=20 mitogen responsiveness of T and B cells, decreased antibody = responses, and=20 impaired T-cell cytotoxicity (60).

=20

=20

GLIOMA-ASSOCIATED TARGET = STRUCTURES FOR=20 IMMUNOTHERAPY

The ultimate goal of glioma immunotherapy is to = induce=20 prominent antitumor immune response leading to the complete = eradication of=20 malignant cells without eliciting serious negative side effects. = An=20 essential step in the development of immunotherapeutic strategies = against=20 malignant gliomas is the identification of suitable target = structures. An=20 ideal target for immunotherapy is an antigen that is specifically = and=20 stably expressed by the tumor, absent from normal tissues, and = crucial for=20 the survival of the cancer cell. Cancer/testis (CT) antigens have = the=20 potential to match such requirements. CT antigens are encoded by = genes=20 that are normally expressed only in the human germ line, but are=20 aberrantly expressed in various tumor types. So far, more than 40 = CT=20 antigen family members have been identified, most of them in = melanomas. Of=20 note, these antigens are frequently found in only a relatively = small=20 proportion of tumor cells. Interestingly, cancer germline genes = (CGGs) are=20 frequently co-expressed, and tumors that express them tend to = express=20 several CT antigens (93,=20 124).

=20

=20

CT antigens

The knowledge of tumor-specific target structures = for glioma=20 immunotherapy is not far advanced. The fact that glial cells and=20 melanocytes ontogenetically have a common neuroectodermal origin = may=20 explain the finding that melanoma-associated CGGs such as the = melanoma=20 antigen-encoding (MAGE) genes MAGE-1 and MAGE-3, MAGE-E1 or GAGE-1 = (151,=20 229, 230) can also be detected in malignant gliomas. Other = CGGs, such=20 as the expression of homo sapiens testis (HOM-TES)-14 [also known = as=20 stromal cell-derived protein (SCP)-1], synovial sarcoma X = breakpoint=20 (SSX)-1, SSX-2, SSX-4, HOM-TES-85 and Sry-related high-mobility = group=20 (HMG) box-containing gene (SOX)-6 have also been described in = malignant=20 gliomas, although their antigenic determinants are not yet known = (222,=20 261). Most studies have analyzed antigen expression at the = mRNA level=20 by reverse transcription polymerase chain reaction (RT=96PCR). = Protein=20 expression or immunogenicity of CT antigens have only rarely been=20 investigated in malignant gliomas (158).=20 Efficient immune recognition of CT antigens on glioma cells may be = compromised by low or absent expression of classical MHC molecules = and=20 inefficient processing and presentation of such antigens (64,=20 173).

=20

=20

Overexpressed self-antigens

Further potential target structures with = restricted protein=20 expression include overexpressed self-antigens, such as mutated = versions=20 of the epidermal growth factor receptor (EGFR), especially of = variant III=20 (EGFRvIII), the IL-13 receptor α chain 2 (IL-13Rα2) or = the apoptosis=20 inhibitor protein, survivin (109,=20 133, 287). Other tumor-associated targets can be detected in = malignant=20 gliomas, such as the squamous cell carcinoma antigen recognized by = T=20 cells, SART1 and SART3 (114,=20 180). Furthermore, transferrin receptors that are = overexpressed on=20 rapidly dividing cells, most notably on hematopoietic cells and = various=20 tumor cells, including GBM cells, are identified as target = structures (210).=20 Currently, much attention is drawn to viral antigens unique to = human=20 cytomegalovirus, which are expressed within the vast majority of=20 high-grade gliomas, but not within surrounding normal brain (176).

=20

=20

Differentiation antigens

Additional potential targets include = differentiation=20 antigens that are normally only seen at particular phases of cell=20 differentiation, such as tyrosinase related protein (TRP)-1 and = TRP-2 or=20 gp100, but also antigen isolated from immunoselected melanoma = (AIM)-2, ADP=20 ribosylation factor 4-like protein ARF4L, and betaGlcNAc beta1,=20 3-galactosyltransferase, polypeptide 3 (GALT3). However, as these = antigens=20 often demonstrate a broader tissue expression, their value as = targets for=20 antiglioma therapy might be limited (45,=20 158, 187, 230, 257).

=20

=20

Stromal antigens

Target structures within the tumor stroma have = also been=20 identified. One of the best examples is tenascin, a polymorphic=20 glycoprotein of the extracellular matrix, which is expressed in = about 80%=20 of malignant gliomas, especially in GBM (20).

=20

=20

GLIOMA IMMUNOTHERAPY

For treatment strategies of gliomas, passive, = adoptive and=20 active immunotherapeutic approaches have been evaluated.

=20

=20

Passive immunotherapy

To target glioma-specific structures, different = monoclonal=20 antibodies (mAbs) have been designed that are coupled to = radionucleotides=20 (radioimmunoconjugates) or exotoxins (immunotoxins) and are = administrated=20 locally. In some studies, a survival benefit in glioma patients = has been=20 documented. However, a disadvantage of this approach is that the=20 penetration of these molecules into the tumor tissue is quite = limited,=20 because of high interstitial pressures in the tumor and = surrounding=20 tissue. High-flow convention enhanced methods are needed to = efficiently=20 deliver these molecules to the more peripheral, diffusely = infiltrative=20 portions. Moreover, the effectiveness of the therapy seems to be=20 restricted to those patients with a low tumor burden (29,=20 150, 277).

=20

=20

Adoptive immunotherapy

Alternatively, the adoptive transfer of ex=20 vivo generated and activated effector cells into the = resection=20 cavity of patients with malignant gliomas has been extensively = evaluated.=20 Treatment approaches have differed in the types of cells = administered, the=20 route of administration, and the activation status of the cells. = These=20 approaches offer the advantage of circumventing deficits of = antitumor=20 effector cell populations in the host by providing optimal = conditions for=20 the culture and amplification of these cells in=20 vitro, in the absence of tumor-derived immunosuppressive = factors.=20 However, despite good tolerability, clinical efficacy has rarely = been seen=20 with the local administration of lymphokine-activated killer cells = (LAK-cells) (27,=20 59, 126), mitogen-activated killer cells (MAKs) (115,=20 129), NK cells, tumor-infiltrating lymphocytes (TILs) and = allogeneic=20 or autologous, tumor-specific cytototoxic T cells (139,=20 147, 200, 206, 291). Proinflammatory cytokines, such as IL-2 = have been=20 coadministered locally to enhance antitumor responses, but has = induced=20 significant toxicity, particularly in patients with large tumor = loads (16,=20 98).

=20

=20

Active immunotherapy

Active immunization of patients with malignant = gliomas is=20 regarded as a powerful strategy to induce potent antitumor = response in vivo. As a vaccine, autologous inactivated = tumor cells=20 have been used, either gene-modified or applied together with=20 cytokine-secreting fibroblasts (193,=20 245). Alternatively, tumor-specific peptide vaccines targeting = EGFRvIII have been administrated intradermally along with = granulocyte=20 macrophage colony-stimulating factor (GM-CSF) as an adjuvans (226).=20 One of the most promising immunotherapeutic approaches to amplify=20 tumor-specific T-cell responses is to use ex = vivo=20 generated, autologous tumor antigen-loaded DCs as a vaccine (79).=20 Several phase I/II studies have been carried out with this = approach, and=20 although these clinical trials differed in terms of DC generation, = loading=20 of tumor antigens and the route of application, robust = intratumoral=20 cytotoxic and memory T-cell infiltration could be detected in = patients who=20 underwent resurgery after vaccination. DC vaccinations appeared to = be=20 mainly beneficial for patients with younger age, minimal residual = tumor=20 burden and expression of low levels of TGF-β2 (54,=20 156, 219, 292, 294, 296, 297). The principles and results of = both=20 peptide-based vaccination and DC therapy against malignant gliomas = are=20 discussed in more detail in the companion articles of van Gool = et al(267)=20 and Choi et al(46).

=20

=20

ENHANCEMENT OF VACCINE = IMMUNOGENICITY

Data from phase I/II studies support the view that = strong=20 glioma-specific immune responses can be induced by a DC vaccine, = but that=20 therapy efficacy is still impeded by rapid tumor progression and a = strong=20 local immunosuppressive environment. To improve glioma = immunotherapy,=20 higher numbers and more potent glioma-specific effector cells = should be=20 induced that home in to the CNS glioma site, including the = peripheral,=20 diffusely infiltrative areas (Figure 6).

=20

= Figure 6. Principles of = dendritic=20 cell (DC) vaccination and further strategies to improve=20 immunotherapy of diffuse gliomas. The most common method = used to=20 generate ex vivo DCs for vaccination = is to=20 culture autologous monocytes obtained from leukapheresis in = the=20 presence of granulocyte monocyte colony-stimulating factor = (GM-CSF)=20 and IL-4. Following 5=967 days in culture, the monocytes = differentiate=20 into immature DCs. DC maturation is induced by culturing = immature=20 DCs for an additional 24=9648 hours in the presence of a = maturation=20 cocktail, most commonly consisting of TNF-α, = IL-1β, IL-6 and PGE2,=20 also known as monocyte-conditioned medium. Tumor antigen = loading=20 with tumor lysate, tumor RNA or synthetic tumor-specific = peptides=20 occurs at either the immature or mature DC stage. Finally, = mature=20 tumor antigen-loaded DCs are injected back into patients. = Critical=20 issues to enhance the persistence of the vaccine-induced = immune=20 responses for future immunotherapeutic approaches against = diffuse=20 gliomas are to improve the immunogenicity of a DC vaccine = and to=20 break the local immunosuppressive environment of diffuse = gliomas.=20 Toll-like receptor (TLR) agonists, activation of = costimulatory=20 receptors, blockade of co-inhibitory receptors and/or = depletion or=20 modulation of regulatory T cells (Treg) could all be used to = intensify antiglioma immune responses induced by peripheral = DC=20 vaccinations. In addition, immunosuppressive molecules could = be=20 targeted directly within the tumor microenvironment to = enhance=20 treatment efficacy. Peri- or intratumoral administration of = distinct=20 TLR agonists might serve as an additional option to activate = local=20 immune cells and to potentiate antitumor immunity. = Abbreviation:=20 BBB =3D blood=96brain barrier; = Teff =3D T effector=20 cells.

[Normal View=20 ]

=20

=20

DC maturation

When using ex vivo = generated DCs as a=20 vaccine, the induction of effective immune responses is dependent = upon=20 proper DC maturation. The most widely used maturation cocktail in = clinical=20 DC trials consists of four reagents: TNF-α; IL-1β; IL-6; = and PGE2, also=20 known as monocyte-conditioned medium. A major disadvantage of this = maturation cocktail is that the resulting DCs secrete little = IL-12, most=20 likely as a result of the presence of PGE2 present during = maturation (134,=20 213). Moreover, cytokine cocktail-matured DCs were found to be = more=20 effective than immature DCs in expanding a population of = immunosuppressive=20 Tregs (55,=20 259).

An excellent method to enhance the immunogenicity = of DCs is=20 to include immune response modifiers, such as TLR agonists into = the=20 maturation cocktail for optimal DC activation. Several groups = reported=20 that DCs matured with more extensive maturation cocktails = containing=20 TLR-agonists such as Poly I:C (TLR3) or R848 (TLR7/8) and = cytokines such=20 as TNF-α, IL-1β and INF-γ show superior = immunogenicity to standard=20 cocktail matured DCs; this strategy enhanced T-cell and NK-cell = responses,=20 while decreasing the chance to induce Tregs. Addition of = TLR-agonists to=20 the maturation cocktail also enabled the use of sufficiently low=20 concentrations of PGE2 that the capacity of DCs to produce IL-12 = was not=20 disturbed. Supplementation with PGE2 was essential to improve DC = handling=20 by reducing cell adherence and enhancing migratory capacity via=20 upregulation of CCR7. Moreover, TLR triggered DCs retained a = stable=20 phenotype and IL-12 producing capacity, even when exposed to = TGF-β, Th2 or=20 Treg promoting environments (30,=20 73, 84, 166, 302). At present, a phase I/II-study = (NCT00766753) using=20 TLR-polarized DCs (type-1 αDCs) loaded with glioma-associated = tumor=20 antigens is being carried out in patients with recurrent malignant = gliomas.

The importance of IL-12 for an effective = immunotherapy=20 against gliomas has been demonstrated in several animal and human = studies.=20 Coadministration of IL-12 with a DC vaccine was reported to = enhance=20 antitumor responses resulting in prolonged survival (116,=20 137, 293). In addition, IL-12 was shown to directly inhibit = Treg=20 differentiation from naive T cells (278).=20 Collectively, these data imply that mature DCs with retained = capacity to=20 produce IL-12 are the most promising candidates for glioma = immunotherapy=20 and point towards an important role for TLR-agonists in inducing = potent=20 anti-glioma responses.

In addition, TLR-agonists can be used as immune = adjuvans.=20 Pretreatment of the injection site with proinflammatory compounds = or=20 TLR-agonists such as imiquimode (TLR7) have been shown to = significantly=20 enhance both the persistence and trafficking of DCs into the = draining=20 lymph nodes after vaccination, resulting in increased priming of=20 tumor-specific T cells (167,=20 181, 204).

=20

=20

Discovery of major glioma = rejection=20 antigens

To create a powerful DC vaccine, it is not only = important to=20 use proper maturation stimuli, but also to efficiently load DCs = with=20 relevant tumor antigens. A major challenge is to discover new,=20 glioma-specific tumor antigens that can be used for targeted = immunotherapy=20 without immunological side effects. Particular attention should be = paid to=20 detection of major glioma rejection antigens that are recognized = by=20 tumor-infiltrating lymphocytes during endogenous antitumor = responses,=20 especially those expressed on tumor-initiating glioma stem cells.=20 Moreover, immunodominant CD4 and CD8 epitopes of these antigens = should be=20 defined to be able to generate tumor peptides that are presented = both by=20 MHC class I and class II molecules. Such information could be = further used=20 to create potent antitumor vaccines consisting of synthetic long = peptides=20 in combination with TLR-agonists to elicit strong effector T-cell=20 responses (25,=20 243). In addition, large numbers of antigen-specific effector = T cells=20 could be generated ex vivo that are = adoptively=20 transferred into lymphopenic patients followed by peptide-pulsed = DC=20 vaccination. This approach has already resulted in effective = antitumor=20 responses against preestablished intracranial tumors in a = preclinical=20 model (205).

Irrespective of the detection of new = glioma-specific tumor=20 antigens, future work should focus on the potential of = tumor-initiating=20 glioma stem cells to provide tumor antigens for vaccination. The=20 possibility of generating cancer stem cell lines from primary GBM = patients=20 has been demonstrated by several groups (21,=20 92, 155). These cancer stem cell lines could be used to = specifically=20 target glioma stem cells, for example, by replacing whole tumor = lysate or=20 total tumor RNA with lysate or RNA from glioma stem cells for = loading=20 DCs.

Further improvement could be obtained by = immunizing not only=20 against tumor cells, but also against the tumor stroma, which is = important=20 for tumor cell growth and survival. Despite the presence of = tumor-specific=20 T cells, tumor cells can escape immune destruction as a result of=20 inappropriate expression of MHC molecules or the presence of = antigen-loss=20 variants. However, stromal cell subpopulations that can capture = and=20 present tumor-derived antigens appear to show less immune escape=20 mechanisms, and therefore might be a better target for immune = effector=20 cells (298).

=20

=20

Intensification of T-cell = costimulation

A powerful option to enhance the immunogenicity of = a vaccine=20 is to increase T-cell costimulation. This can be achieved by=20 coadministering agonistic antibodies specific for costimulatory = molecules=20 belonging to the TNF receptor superfamily, such as GITR, OX40 = (CD134),=20 4-1BB (CD137) and RANK (47,=20 89, 170, 237, 265). In murine glioma models some of these = antibodies=20 have exerted a promising effect (138,=20 140).

Alternatively, T-cell costimulation can be = increased by=20 coadministering antagonistic antibodies specific for co-inhibitory = molecules expressed on T cells. For instance, many inhibitory = pathways=20 within the B7=96CD28 family have been described that can attenuate = T-cell=20 responses and promote T-cell tolerance. CTLA-4 and the = programmed-death=20 (PD)-1 receptor are two of the key negative regulators of T cell=20 responses. Anti-CTLA-4 antibodies have been studied as potential=20 therapeutics for glioma. We and others have shown that systemic = CTLA-4=20 blockade prolongs survival in treated mice, without eliciting = signs of=20 autoimmunity. Anti-CTLA-4 treatment reestablished normal CD4 = counts and=20 abrogated increased Treg fractions in the CD4 compartment observed = in=20 tumor-bearing mice. Moreover, the CD4 T-cell proliferative = capacity could=20 be restored and glioma-specific antitumor immunity was enhanced (67,=20 85).

Recent data suggest that CTLA-4 blockade can = result in the=20 effective treatment of tumors arising in the CNS. It was = demonstrated that=20 the systemic administration of a human mAb directed against CTLA-4 = (Ipilimumab, MDX-010, Bristol-Myers Squibb, New York, NY, USA and = Medarex=20 Inc. Princeton, NJ, USA) induced a significant clinical benefit in = a=20 female patient with metastatic melanoma to the CNS. Pathological=20 examination of the brain metastasis following Ipilimumab treatment = revealed abundant infiltrates of CD8+ lymphocytes and extensive = tumor=20 necrosis (104).

=20

=20

Counteracting Treg-mediated=20 immunosuppression

The immunogenicity of a vaccine can be further = enhanced by=20 removing suppression of Tregs. Especially in preclinical murine = models,=20 different strategies have been successfully used to eliminate = Tregs such=20 as CD25-specific mAbs, immunotoxins or different chemotherapeutic=20 agents.

We recently showed in a murine glioma model that = depletion=20 of Tregs by systemic administration of CD25-specific mAbs can = elicit an=20 otherwise suppressed immune response against glioma-specific tumor = antigens, leading to the rejection of the tumors. Additional = experiments=20 revealed that combining Treg depletion with administration of = CTLA-4 mAbs=20 further boosted glioma-specific CD4 and CD8 effector T cells, as = well as=20 anti-glioma IgG2a antibody titers in this model without any signs = of=20 autoimmunity (85).=20 The potency of Tregs to suppress an effective anti-glioma immune = response=20 was further demonstrated by the fact that mice were not protected = from=20 tumor outgrowth when vaccinated with tumor-lysate pulsed DCs in a=20 "simultaneous setting" where tumor cells and DCs are given at the = same=20 day. In contrast, depletion of Tregs before vaccination = considerably=20 increased the ability of vaccinated mice to survive the tumor = challenge.=20 Moreover, DC vaccination with anti-CD25 treatment allowed the = development=20 of long-lasting tumor protective immunity (87,=20 164). These results confirm that counteracting Treg-mediated=20 immunosuppression is an essential component in the success of = anti-glioma=20 vaccines. However, a disadvantage of CD25 depletion is that = treatment of=20 mice with anti-CD25 mAbs is only beneficial within a limited time = window=20 and its efficacy is dependent on tumor burden. Treg depletion = after=20 immunotherapy inhibited clonal expansion of tumor antigen specific = T cells=20 and reduced the efficacy of the vaccine (51).

In humans, several anti-CD25 antibodies such as = daclizumab=20 have been developed and tested for their ability to deplete human = Tregs.=20 However, recent studies demonstrated that these antibodies failed = to=20 eliminate Tregs or did not affect their suppressive function (145,=20 271). Currently, two phase I/II randomized studies = (NCT00626483,=20 NCT00626015) are being carried out in patients with newly = diagnosed GBM to=20 determine if daclizumab inhibits the functional and numeric = recovery of=20 Tregs after therapeutic TMZ-induced lymphopenia.

Besides CD25 mAb, a recombinant IL-2 diphtheria = toxin=20 conjugate, DAB389IL-2 (also known as denileukin diftitox or ONTAK) = and a=20 CD25-specific immunotoxin (LMB-2), which is formed of the = single-chain Fv=20 fragment of the anti-CD25 mAb with a recombinant form of the = pseudomonas=20 exotoxin, have been investigated for the elimination of Tregs. A = few=20 studies have shown a reduction in the number of circulating and=20 tumor-infiltrating Tregs after a single dose of ONTAK, with a more = prominent effect after successive ONTAK treatments or = administrations of=20 LMB-2. Moreover, ONTAK significantly improved the stimulation of=20 tumor-specific T cell responses after vaccination with = tumor-antigen=20 loaded DCs (53,=20 165, 202). However, despite inducing a reduction in Treg cell = numbers=20 in vivo, ONTAK or LMB-2 treatment have only = resulted=20 in limited objective clinical responses so far (146,=20 202).

Alternate chemotherapeutics are currently being = investigated=20 for their potency to selectively deplete Tregs (10,=20 76, 78). In a rat glioma model, oral administration of = low-dose=20 metronomic TMZ has recently been shown to reduce circulating = Tregs,=20 associated with a suppression of their inhibitory functions on = effector T=20 cells in a rat glioma model. In contrast, high-dose TMZ failed to=20 significantly modulate Treg numbers or function (15).=20 Similarly, a significant reduction of CD4+CD25+ T cells could be=20 demonstrated with metronomic administration of TMZ in melanoma = patients (251).=20 Therefore, a low dose metronomic TMZ regime in association with a = cancer=20 vaccine could be an attractive strategy for the treatment of = malignant=20 glioma and might be superior in efficacy to conventional TMZ = chemotherapy=20 alone.

Another interesting approach to reduce the number = of=20 tumor-infiltrating Tregs is to selectively block their trafficking = to the=20 tumor site. Treg subsets have been reported to differ in homing = receptor=20 expression and chemokine responsiveness (108,=20 189, 240). Recently, it was demonstrated that Tregs from GBM = patients=20 express significantly higher levels of CCR4 than those from = healthy=20 controls and they respond to both the recombinant human chemokines = CCL2/MCP-1 and CCL22/MDC in vitro. = Moreover,=20 chemotherapeutic agents such as TMZ and carmustine [3-bis=20 (2-chloroethyl)-1-nitrosourea] were shown to reduce the production = of CCL2=20 by glioma cells (131).=20 Other inflammatory chemokine receptors involved in the attraction = of Tregs=20 are CCR2, CCR5 and CCR8 (113).=20 Gliomas can synthesize and release CXCL12/SDF-1 in a TGF-β = dependent=20 manner (252).=20 Interestingly, we observed CXCR4 expression on glioma-infiltrating = Tregs=20 and its upregulation during tumor growth. Implementation of CXCR4=20 inhibitors may thus improve immunotherapeutic strategies against = malignant=20 gliomas (211).

=20

=20

BREAKING THE LOCAL = IMMUNOSUPPRESSIVE=20 ENVIRONMENT OF GLIOMAS

In order to enhance the persistence of the = vaccine-induced=20 immune responses and to achieve optimal clinical benefit, apart = from=20 optimizing antiglioma vaccines, additional treatments need to be = developed=20 to break the local immunosuppressive environment of gliomas.

=20

=20

Targeting TGF-β

A powerful approach to overcome glioma-induced = tolerance=20 mechanisms involves targeting immunosuppressive molecules directly = within=20 the tumor microenvironment. In malignant gliomas, the three = existing=20 isoforms of TGF-β in mammals, termed TGF-β1, 2 and 3, = are differentially=20 expressed. High-grade gliomas mostly overexpress the TGF-β2 = isoform, which=20 is processed and secreted in large amounts in its active form (141).=20 In recent years, different strategies have been developed for = inhibiting=20 TGF-β. The most advanced in the clinical application is the = use of a=20 phosphorothioate-modified antisense oligonucleotide (trabedersen, = AP=20 12009, ANTISENSE Pharma GmbH, Regensburg, Germany), which is = complementary=20 to the mRNA encoding TGF-β2 isoform (122,=20 123, 232). Several phase I/II-studies have been carried out = applying=20 TGFβ2-antisense oligonucleotides intratumorally through = continuous=20 high-flow microperfusion [(convection-enhanced delivery (CED)] in = patients=20 with high-grade gliomas; these studies confirmed the safety of = this=20 approach, as well as long-term clinical benefit in several = individuals (97).=20 A multinational phase III study (NCT00761280) comparing=20 TGFβ2-antisense-oligonucleotides with standard chemotherapy = (TMZ or BCNU)=20 in adult patients with confirmed recurrent or refractory = anaplastic=20 astrocytoma (WHO grade III) is currently recruiting patients.

An alternative to the treatment with antisense=20 oligonucleotides is to prevent downstream signaling by interfering = with=20 TGF-β receptor kinase activities. Such kinase inhibitors have = already been=20 successfully tested in preclinical models, resulting in increased = survival=20 of treated animals, associated with pronounced tumor infiltration = by=20 NK-cells, CD8+ T-cells and macrophages (255,=20 262).

Strategies combining active immunotherapy with = local TGF-β=20 blockade could thus further enhance therapy efficacy. In a = preclinical=20 study using a rat glioma model, the combination of intracranial = TGF-β2=20 antisense oligonucleotide administration and vaccination with = irradiated=20 glioma cells not only inhibited TGF-β protein production = in=20 vivo, but also significantly prolonged survival times when = compared=20 with either vaccine alone or no therapy (161).

=20

=20

Targeting Stat3 and = immunosuppressive=20 enzymes

There is accumulating evidence from preclinical = studies that=20 targeting immunosuppressive molecules other than TGF-β = improves antitumor=20 immunity against gliomas as well.

Considering the suppressive role of signal = transducers and=20 activators of transcription 3 (Stat3) in antitumor immunity, = selective=20 inhibitors of Stat3 have been evaluated in murine glioma models = and were=20 shown to activate intratumoral macrophages and microglia, induce = apoptosis=20 in glioma cells, and inhibit tumor growth (112,=20 120, 300).

With regard to immunosuppressive enzymes, specific = IDO=20 inhibitors such as 1-methyl-l-trypophan have been studied to break = immune=20 resistance of malignant gliomas through T-cell inactivation caused = by=20 tryptophan depletion and metabolite accumulation (106,=20 177). Moreover, COX-2 inhibitors have been shown to = significantly=20 reduce PGE2 levels in Cox2-overexpressing gliomas, thereby = abrogating the=20 induction of IL-10 and TGF-β-secreting Tr1 cells (4).=20 Selective COX-2 inhibitors also show antiproliferative and=20 apoptosis-inducing effects independent of their COX-2 inhibitory = activity,=20 resulting in the reduction or inhibition of glioma growth in=20 vivo(182,=20 234). Furthermore, antitumor responses could also be elicited = by=20 blocking arginase expression using COX-2 inhibitors (214,=20 215). To restore T-effector-cell functions, selective iNOS = inhibitors=20 such as SD-3651 might be attractive for the treatment of gliomas = (186).

=20

=20

Local treatment of gliomas with = TLR=20 agonists

Local administration of immune response modifiers, = such as=20 TLR-agonists are powerful tools to generate immune responses = against=20 antigens derived from the tumor in vivo. = Pioneering=20 experiments from Carpentier et al have = shown=20 that direct injections of synthetic phosphothioate-stabilized=20 CpG-oligonucleotides (CpG-ODNs) in neuroblastomas induced complete = tumor=20 rejection in the majority of mice and triggered long-term immunity = (37).=20 Further studies have confirmed the antitumor effects of CpG-ODN in = different intracranial models of syngeneic glioma (38,=20 174). Recently, we could show in a murine glioma model that = the=20 therapeutic efficacy of CpG-ODN is predominately mediated through = a=20 TLR9-dependent immune activation leading to intratumoral = accumulation of=20 IFN-γ producing CD4 and CD8 T cells, a marked increase in the = ratio of CD4=20 effector T cells to Tregs, and long-term protective immunity. = Moreover,=20 local administration of CpG-ODNs (TLR9 agonist) was most efficient = in=20 inducing antitumor immunity as compared with other TLR-agonists (86).

A phase I trial using convection-enhanced = intratumoral=20 delivery of CPG-ODN (CpG-28) has already been completed in the = setting of=20 recurrent GBM and showed minor responses in two patients without = showing=20 serious adverse events (36).=20 A randomized phase-II trial with CpG-ODN in GBM is still ongoing=20 (NCT00190424). However, a major drawback of this approach is that = TLR9=20 expression in humans is far more restricted and predominately = confined to=20 plasmacytoid DCs and B cells. Therefore, besides CpG-ODN, it will = also be=20 interesting to explore local delivery of functionally similar = agents, such=20 as TLR7/8-agonists to break local immunosuppression in glioma = patients.=20 Survival benefit was observed in therapeutic murine glioma models = after=20 intratumoral injection of synthetic TLR7/8-agonists, such as R848=20 (resiquimod) or protamine-protected mRNA (86,=20 231). Alternatively, recently identified = phosphorothioate-modified=20 immunostimulatory RNA oligonucleotides might be attractive in this = setting, as they proved to be potent inducers of INF-α and = TH1 cytokines=20 via TLR 7/8 (secreted by DCs) and triggered an antigen-specific = cytotoxic=20 T-cell and IgG2a response (31).

In the future, it might be worthwhile to apply = certain=20 combinations of TLR agonists to further enhance the treatment = efficacy.=20 Synergy between different TLR agonists is now well documented (183,=20 276). Recent findings further imply that TLR agonists not only = induce=20 beneficial activating, but also potentially suppressive effector=20 responses. Therefore, selective inhibition of immunosuppressive = molecules=20 induced during TLR immunotherapy might further enhance the = efficacy of=20 TLR-agonists as tumor immunotherapeutics. Inhibition of IL-10 with = an=20 anti-IL-10 receptor antibody combined with CpG-ODN activation was = shown to=20 reverse the tolerogenic state of tumor-infiltrating DCs and to = augment=20 their therapeutic efficacy in a mouse tumor model (269).=20 Moreover, vaccinations with TLR-matured DCs pulsed with tumor = antigen=20 combined with peri- or intratumoral injection of TLR-agonists can=20 potentiate antitumor immunity, as it was shown to eradicate large = murine=20 tumors resistant to chemotherapy (99).

It will be also interesting to evaluate = stimulation of other=20 innate immune receptors for glioma therapy. Recently, bifunctional = RNA=20 molecules that were designed to target key tumor survival factors = and to=20 activate cytosolic retinoic acid-inducible gene-I (RIG-I)-like = helicases=20 promoted strong antitumor effects in a mouse model of metastatic = melanoma=20 to the lung (201).

To move forward, however, additional studies are = needed to=20 define the protective mechanisms of action of distinct innate = immune=20 receptor agonists and their potential toxicity, because immune = response=20 modifiers that activate a wide range of innate and adaptive immune = cells=20 can have severe adverse effects, especially in the = CNS.

=20

=20

Local glioma treatment with = DCs

An alternative strategy to modify the tumor = microenvironment=20 is to inject DCs directly into the tumor bed. Intratumoral = injections of=20 DCs either transduced with INF-α DNA or TLR-polarized DC have = been shown=20 to enhance anti-CNS immunity by promoting cross-presentation of=20 tumor-associated antigens in draining lymph nodes and by enhancing = CNS=20 tumor homing of antigen-specific type 1 CTLs through the induction = of=20 CXCL10 (73,=20 258). Furthermore, intratumoral delivery of DCs enhances the = antitumor=20 efficacy of peripheral vaccines (73,=20 152, 194). Preliminary clinical results also confirm that = intratumoral=20 DC application in addition to intradermal DC injections are more=20 beneficial in the treatment of glioma patients than intradermal DC = injections alone (294).

=20

=20

COMBINATION OF IMMUNOTHERAPY AND=20 RADIOCHEMOTHERAPY

Recent studies indicate that the clinical = responsiveness of=20 patients with malignant gliomas to chemotherapy is increased after = DC=20 vaccinations. Vaccinated patients receiving subsequent = chemotherapy showed=20 significantly longer times to tumor recurrence/progression and = longer=20 overall survival after chemotherapy than those who were treated = only with=20 chemotherapy. It has been postulated that therapeutic vaccinations = increase the sensitivity to chemotherapy by eliminating = chemoresistant=20 tumor cells (284,=20 285).

There are a number of reasons to combine = immunotherapeutic=20 strategies with conventional therapeutic methods such as = radiotherapy and=20 chemotherapy (153,=20 266). Recent data show that tumor cell death triggered by = chemotherapy=20 or radiotherapy initiates an immunoadjuvant pathway that = contributes to=20 the success of cytotoxic treatments (301).=20 Numerous endogenous danger signals transferred by dying tumor = cells to=20 innate immune effectors may account for the immunogenicity of = tumor cell=20 death (8).=20 Both anthracyclines and alkylating chemotherapeutics such as TMZ = have been=20 shown to induce an immunogenic cell death by triggering innate = receptors=20 such as TLRs. As a consequence, the ability of DCs to present = tumor=20 antigens from dying tumor cells to T and B cells is enhanced (7,=20 52, 192). Moreover, activation of innate immune receptors = leads to the=20 upregulation of MHC molecules on tumor cells, thus increasing = their=20 sensitivity to T-cell-mediated killing (86,=20 184). In addition, radiotherapy and chemotherapy remove local=20 suppressor cells, such as tumor-specific Tregs or might affect = their=20 function, thus permitting a more effective T-cell stimulation (188,=20 251). Furthermore, chemotherapy has been shown to induce = lymphopenia,=20 thereby allowing thymic-independent antigen-driven T-cell = regeneration=20 within the context of T-cell homeostasis (127,=20 163). The concept of tumor-specific immunization at the time = of immune=20 reconstitution after chemotherapy has been successfully tested in=20 different animal models and phase I/II clinical studies, = demonstrating=20 that the availability of tumor antigens during homeostatic T-cell=20 proliferation leads to effective antitumor immunity and enhanced = memory=20 T-cell responses (9,=20 12, 107, 209).

Combination therapies integrating vaccination = strategies=20 into the standard chemoradiotherapy protocol are currently under=20 evaluation. There is preliminary evidence of successful = combination of=20 immunotherapy and TMZ (101).=20 However, administration of anti-immunosuppressive therapy together = with=20 radiochemotherapy must be carefully timed so as to optimize the = immune=20 response. It is of critical importance to establish reliable, = reproducible=20 and quantitative assays to evaluate vaccine-induced immune = responses (1,=20 259). Ideally, pre- and postvaccination samples should be = taken=20 throughout the course of vaccination concomitantly with the = evaluation of=20 clinical parameters. Vaccine-induced cellular and humoral immune = responses=20 should be monitored in different compartments, especially at the = tumor=20 site, in the circulation, and at the vaccination site = [delayed-type=20 hypersensitivity (DTH) test biopsies]. Overall, the combination of = radiotherapy, chemotherapy and immunotherapy has the potential for = strong=20 antitumoral activity against malignant glioma, when applied using = a=20 well-designed strategy.

=20

=20

CONCLUSION

Although our understanding of glioma immunobiology = is=20 rapidly growing, the knowledge about the complex pathological = interactions=20 within the local tumor microenvironment is still limited. Further=20 elucidation of the spatiotemporal organization of the different = players in=20 tumor-induced immunosuppression is of utmost importance for = improving=20 intervention strategies that boost potent antitumor responses. = Current=20 vaccination protocols are still of limited efficacy for = suppressing glioma=20 growth. To achieve optimal clinical benefit, additional treatments = need to=20 be developed and combined with a vaccine to break the local=20 immunosuppressive environment of gliomas without inducing = autoimmunity.=20 This will enhance the persistence of the vaccine-induced immune = responses=20 and will increase the chance to eliminate diffusely infiltrating = tumor=20 cells embedded within the normal brain parenchyma. Moreover, = understanding=20 the details of immune evasion in individual patients is critical, = because=20 it will ultimately enable the development of tailored therapies = that=20 specifically overcome these mechanisms of resistance. Keeping in = mind that=20 many of these immune evasion strategies used by gliomas are also = part of=20 the regular defense mechanism of the brain to prevent = autoimmunity, such=20 therapies have to be monitored carefully to detect and limit = immune=20 responses that are harmful to normal brain tissue. With further = unraveling=20 of glioma immunobiology, immunotherapeutic strategies have the = opportunity=20 to become a standard component in the multimodal treatment of = malignant=20 gliomas.

=20

=20

=20

ACKNOWLEDGMENTS

This work was supported by grants from the German = Research=20 Foundation and the Medical Faculty of the University of Regensburg = (GR2089/1-1 and ReForM program to O.M. Grauer), and by grants from = the=20 KWF/Dutch Cancer Society (KUN 2003-2893 to G.J. Adema and KUN = 2003-2975 to=20 P. Wesseling).

=20

=20

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