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application/octet-stream Content-Transfer-Encoding: quoted-printable Content-Location: http://download.interscience.wiley.com/freeflow/js/genlink.js function get_link(a, b) {=0A= document.write("" + b = + "");=0A= }=0A= =0A= function get_pdf_link(a, b, c) {=0A= document.writeln('' + b + = ' (Size: ' + c + 'K)');=0A= }=0A= =0A= function get_button_link(cgi, params, imgbutton) {=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_0076_01C82911.C76EF660 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('
3D"provided
');=0A= document.writeln('
    ');=0A= =0A= var i;=0A= //Change start for bug#2288=0A= if(typeof(maxBranding) =3D=3D "undefined" | maxBranding =3D=3D "" | = maxBranding =3D=3D 0){=0A= maxBranding =3D 3; // DEFAULT Value for No of Cobranding dispaly=0A= }=0A= var size =3D customerCoBranding.length;=0A= if(maxBranding !=3D -1 & size-1 > maxBranding){=0A= size =3D maxBranding;=0A= }=0A= //Change End for bug#2288=0A= =0A= // Add the co-branding images o the page.=0A= //for(i=3D0; i < customerCoBranding.length; i++ )=0A= for(i=3D0; i < size; i++ )=0A= {=0A= // ignore the terminating array element.=0A= if(customerCoBranding[i].image =3D=3D "none")=0A= {=0A= continue;=0A= }=0A= =0A= this.image =3D customerCoBranding[i].image;=0A= this.imageAltText =3D customerCoBranding[i].imageAltText;=0A= this.href =3D customerCoBranding[i].href;=0A= =0A= if (image =3D=3D "")=0A= {=0A= if(href =3D=3D "")=0A= {=0A= document.writeln('
  • ' + imageAltText + '
    • ');=0A= }=0A= else=0A= {=0A= document.writeln('
  • ' + imageAltText + = '
    • ');=0A= }=0A= }=0A= else=0A= {=0A= if(href =3D=3D "")=0A= {=0A= document.writeln('
  • 3D"'
    • ');=0A= }=0A= else=0A= {=0A= document.writeln('
  • 3D"'
    • ');=0A= }=0A= }=0A= }=0A= =0A= // If there are more co-branding images add in a link to them.=0A= // Changes made for Bug#2288=0A= //if(moreCustomerCoBranding =3D=3D "true")=0A= if(maxBranding !=3D -1 & customerCoBranding.length-1 > maxBranding)=0A= {=0A= document.writeln('
  • More Providers
    • ');=0A= }=0A= =0A= document.writeln('
');=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("");=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('
  • Login
    • ');=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 "
  • Log Out
    • ";=0A= }else=0A= {=0A= return "
  • Log = In
    • ";=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= document.getElementById("shcrt_id").style.display =3D "block";=0A= }=0A= else=0A= {=0A= document.getElementById("shcrt_id").style.display =3D "none";=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; i 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 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 (arguments.length >=3D 4 && arguments[3] =3D=3D 'cluster')=0A= {=0A= url +=3D '&type=3Dcluster';=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 "
  • more...
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    3D"Jump

    Developmental=20 Dynamics
    ISSN: 1097-0177 = (Online)
    ISSN:=20 1058-8388 (Print)

    Volume 236, Issue 12, 2007.
    Pages: = 3297-3308
    • Top of page
    • Abstract
    • INTRODUCTION
    • BRAIN TUMORS CONTAIN A DISTINCT STEM=20 CELL POPULATION
    • TGF/BMP PATHWAY
    • WNT PATHWAY
    • NOTCH PATHWAY
    • HEDGEHOG PATHWAY
    • PERSPECTIVES/CONCLUSION
    • Acknowledgements
    • References
    List of Images
    Abstract=20 Only

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    3D"About

    Online ISSN: 1097-0177    Print ISSN: = 1058-8388
    Developmental Dynamics
    Volume 236, Issue 12, 2007. Pages: 3297-3308
    (Special Issue: Special Focus on Stem = Cells. Issue Edited by John F. Fallon.)

    Copyright © 2007 Wiley-Liss, Inc.

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    Copyright © 2007 = Wiley-Liss, Inc.
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    '); } =0A= function display_fig001(size) { var i =3D new Array(); i[0] =3D = 'nfig001'; i[1] =3D 'mfig001'; var hwnd =3D newfigwin(); dochead(hwnd, = ''); copyright(hwnd); otherlinks(hwnd, 'fig001', size); imagelink(hwnd, = i[size]); gcaption_fig001(hwnd); caption_fig001(hwnd); doctail(hwnd); = hwnd.document.close(); hwnd.focus(); } =0A= function caption_fig002(hwnd) { hwnd.document.write('Figure 2. Pathways involved in neural development. A: The TGF/BMP = pathway. Inactivated transmembrane heterodimeric receptors exist = separately. Upon activation by TGF or BMP ligand, the receptors associate = and the type II receptor phosphorylates the serine residue of the type I = receptor. This in turn leads to phosphorylation of intracellular SMAD = proteins, association with a coSMAD, localization into the nucleus, = promoter binding by means of a CBP/p300 complex, and downstream gene = expression. B: Canonical WNT pathway. During inactivation, a = complex involving Axin, APC, and GSK3 acts = to phosphorylate -catenin, slating it for proteolysis. Upon binding = of WNT ligand to a Frizzled receptor and association with LRP, DSH is = activated and represses GSK3. This repression prevents = phosphorylation and allows cytosolic accumulation of -catenin, leading to nuclear localization and gene = expression by means of a TCF/LEF complex. C: Notch pathway. = Signaling is activated by ligand binding (Delta or Jagged) to the Notch = receptor. Cleavage of the Notch receptor results in both extracellular = and intracellular domains. The intracellular domain (NICD) localizes to = the nucleus, where it associates with MAML and induces gene expression = after promoter binding by means of a complex involving CSL. D: = Hedgehog signaling. During inactivation, Patched works to repress the = action of Smoothened and intracellular Gli proteins are repressed as = part of the Sufu complex. Sonic Hedgehog binding to Patched inhibits its = repression of Smoothened, which in turn inactivates the Sufu complex. = This repression frees Gli, allowing nuclear localization and gene = expression. Regulation of all pathways exists at multiple levels, = including inhibitory SMADs (iSMADs) for BMP signaling, DKK and sFRP for = WNT signaling, and HHIP for Hedgehog signaling, among others. TGF, = transforming growth factor ; BMP, bone morphogenetic protein; = SMAD, Sma/MAD protein; APC, adenomatosis polyposis coli; GSK3, = glycogen synthase kinase 3; -cat, -catenin; TCF/LEF, T-cell factor/lymphoid-enhancer = factor; MAML, Mastermind-like; Sufu, suppressor of fused homolog; DKK, = Dickkopf homolog 1; sFRP, secreted frizzled-related protein; HHIP, = hedgehog interacting protein.
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    '); caption_fig001(hwnd); = hwnd.document.write('
    [Normal View 55K | Magnified View = 224K]
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    [Normal View 61K | Magnified View = 180K]
    '); doctail(hwnd); = hwnd.document.close(); hwnd.focus(); } =0A= ------=_NextPart_000_0076_01C82911.C76EF660 Content-Type: application/octet-stream Content-Transfer-Encoding: quoted-printable Content-Location: http://www3.interscience.wiley.com/cgi-bin/fulltext/116843358/main.html,ftx_abs Wiley InterScience = :: Article Full Text HTML

    Developmental Dynamics

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    Volume 236, Issue 12, Pages 3297-3308

    Published Online: 14 Nov 2007

    Copyright =A9 2007 Wiley-Liss, Inc.

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     Special Issue Reviews-A Peer Reviewed = Forum
    Developmental signaling pathways = in brain=20 tumor-derived stem-like cells
    Paul A. Clark, Daniel M. Treisman, Johnathan Ebben, John = S.=20 Kuo *
    Brain Tumor Research Lab, Department of Neurological = Surgery,=20 University of Wisconsin School of Medicine and Public = Health,=20 Madison, Wisconsin
    email: John S. Kuo (j.kuo@neurosurg.wisc.edu)

    *Correspondence to John S. = Kuo,=20 Department of Neurological Surgery, University of Wisconsin School = of=20 Medicine and Public Health, 600 Highland Avenue, CSC K3/803, = Madison, WI=20 53792-8660

    Keywords
    brain tumor =95 stem cell =95 WNT =95 BMP =95 TGF =95 Hedgehog =95 = Notch

    Abstract
    3DAbstract=20 3D""=20
    Recently, a subpopulation of cells highly efficient in = tumor=20 initiation and growth has been isolated from brain tumors. = Of=20 interest, these brain tumor initiating cells exhibit many = stem-like=20 properties, including self-renewal, extended proliferation, = and=20 multipotency, and are both phenotypically and genetically = similar to=20 normal neural stem cells (NSCs). Aberrant expression of=20 developmental pathways, such as WNT, Hedgehog, Notch, and=20 transforming growth factor-/bone morphogenetic protein, = have been=20 demonstrated in brain tumors, and extrinsic regulation of = these=20 pathways may be used to target brain tumor stem-like cells = (BTSCs)=20 and form the basis of novel biological therapies. Because of = regulatory redundancy during normal development, future = therapeutic=20 strategies to inhibit BTSC-mediated tumor growth and = minimize=20 NSC-related deleterious effects may require detailed = understanding=20 and regulation of multiple cellular mechanisms. This review = analyzes=20 the role developmental pathways play in brain tumors, = focusing on=20 the potential effects of pathway regulation on BTSC-driven=20 tumorigenesis. Developmental Dynamics 236:3297-3308, 2007. = =A9 2007=20 Wiley-Liss, Inc.

    Accepted: 10 October 2007

    Digital Object = Identifier=20 = (DOI)

    10.1002/dvdy.21381  About=20 DOI

    Article=20 Text

    INTRODUCTION
    3DINTRODUCTION=20 3D""=20

    For many malignant brain tumors such as grade IV astrocytoma=20 (glioblastoma multiforme, GBM) and medulloblastoma, clinical = prognosis is=20 dismal despite aggressive therapy. Recently, tumor cells with = stem-like=20 properties were isolated from hematological and solid tumors = (Bonnet and=20 Dick,[1997];=20 Al-Hajj et al.,[2003];=20 Collins et al.,[2005];=20 Fang et al.,[2005];=20 Gibbs et al.,[2005];=20 Dalerba et al.,[2007];=20 Li et al.,[2007a];=20 Ma et al.,[2007];=20 O'Brien et al.,[2007];=20 Ricci-Vitiani et al.,[2007]),=20 including brain tumors (Hemmati et al.,[2003];=20 Singh et al.,[2003];=20 Galli et al.,[2004];=20 Yuan et al.,[2004]).=20 It was observed that these cells initiate and propagate neoplasms = with=20 high efficiency, and when tumor stem-like cells were removed from = the bulk=20 tumor mass, growth is rarely observed (Al-Hajj et al.,[2003];=20 Singh et al.,[2004b]).=20 These findings challenge the classic model of cancer, in which = every tumor=20 cell has initiation potential, and suggest a hierarchal model for=20 tumorigenesis (Hope et al.,[2004]),=20 similar to the cellular hierarchy arising from fetal and adult = stem cells=20 in tissue development and maintenance. Additional characterization = of the=20 cancer stem cells demonstrated expression of many stem cell = markers and=20 differentiation=20 to postmitotic cells of the appropriate tissue (Bonnet and = Dick,[1997];=20 Singh et al.,[2003];=20 Galli et al.,[2004]),=20 suggesting that cancer arises from a transformed stem cell and = possibly=20 partially propagates through mechanisms similar to a developmental = process=20 gone awry (Wechsler-Reya and Scott,[2001]).=20 The cellular origin of these tumor initiating cells is unclear, = and,=20 therefore, they have been labeled various names including brain = tumor=20 initiating cells, CD133+ cells, and brain tumor = stem-like cells=20 (BTSCs). To provide clarity and consistency throughout this review = and to=20 emphasize their relationship to normal neural stem cells (NSCs), = we=20 hereafter refer to these cells as BTSCs.

    Neural development is a complex process involving multiple = signaling=20 pathways, many of which are closely conserved across species. = Rapid=20 proliferation and high motility are hallmarks of both development = and=20 tumorigenesis; therefore, pathways important for development are = probable=20 targets for oncogenic transformations (Wechsler-Reya and Scott,[2001];=20 Vogelstein and Kinzler,[2004];=20 Kelleher et al.,[2006];=20 Read et al.,[2006]).=20 The persistence of neural stem cells into adulthood in the = subventricular=20 zone and subgranular zone of the hippocampus (Gage et al.,[1995];=20 Eriksson et al.,[1998];=20 Morshead and van der Kooy,[2001])=20 also provide a pool of candidate cells for oncogenic = transformation=20 because of their extended lifespan and cellular machinery for = unlimited=20 growth. If aberrant control of developmental pathways is = responsible for=20 propagation and/or maintenance of cancer stem cells, it is = conceivable=20 that exogenous pathway regulators may have novel therapeutic roles = for=20 brain cancer. This review will discuss some of the major neural=20 developmental pathways (WNT, Notch, Hedgehog, transforming growth=20 factor- [TGF]/bone morphogenetic protein [BMP]) = that have=20 been implicated in brain tumors, focusing on the potential for=20 developmental cues to regulate BTSC-mediated tumor initiation and=20 growth.

    BRAIN TUMORS = CONTAIN A=20 DISTINCT STEM CELL=20 POPULATION
    3D"BRAIN 3D""=20

    Tumors were long noted to contain heterogeneous populations of = cells=20 with differing physical appearance and cellular functions. The = idea that=20 only a subset of these cells has the ability to initiate tumors = arose from=20 histological observations and colony-forming assays designed to = isolate=20 and study tumor stem cells=20 (Hamburger and Salmon,[1977]).=20 Isolation and identification of human tumor initiating cells was = first=20 accomplished in hematological cancer by serial dilution of = leukemic cells=20 that demonstrated only a small fraction of the cells could = initiate the=20 cancer (Blair et al.,[1997];=20 Bonnet and Dick,[1997]).=20 Surprisingly, these leukemia initiating cells (LICs) exhibited=20 characteristics of normal hematopoietic stem cells, including=20 multipotency, self-renewal, and expression of stem cell surface = markers,=20 suggesting that LICs may arise from transformation of primitive = stem cells=20 and not from committed progenitors (Bonnet and Dick,[1997];=20 Hope et al.,[2004]).=20 The identification of similar tumor initiating cells with stem = cell=20 properties also emerged for solid tumors such as breast cancer = (Al-Hajj et=20 al.,[2003]).=20 For breast cancer, a small fraction of tumor initiating cells = selected by=20 expression of stem cell surface markers were highly efficient at = inducing=20 xenograft tumors in immunodeficient mice (with as few as 100 = cells).=20 Importantly, tumor cells negative for stem cell surface markers = did not=20 efficiently form tumors even when injected in much higher numbers = (Al-Hajj=20 et al.,[2003]),=20 indicating a hierarchy of cells within tumors - only a = small=20 fraction is highly capable and efficient at tumor initiation and=20 propagation.

    Identification of tumor initiating cells in human brain tumors = was also=20 reported. By sorting for tumor cells expressing the NSC marker = CD133,=20 Singh et al. (2004b) demonstrated that as few as 100 cells = isolated from=20 high-grade astrocytomas (GBM) or medulloblastomas could initiate = and=20 propagate a tumor when re-injected orthotopically in brains of=20 immunodeficient mice. Similar to breast cancer, injection of = exponentially=20 more CD133- cells was required to initiate tumors = (Singh et=20 al.,[2004b]).=20 Similar techniques were used to isolate tumor initiating cells = from=20 pediatric brain tumors (Hemmati et al.,[2003])=20 and ependymomas (Poppleton and Gilbertson,[2007]).=20 These tumor initiating cells were observed to bear striking = similarities=20 to normal NSCs on further analyses. The BTSCs propagated in vitro = as=20 free-floating neurospheres when cultured in serum-free medium = supplemented=20 with epidermal growth factor (EGF) and basic fibroblast growth = factor=20 (bFGF), an assay system classically used to isolate NSC as = neurospheres=20 from developing and adult brain (Reynolds and Weiss,[1992],[1996];=20 Svendsen et al.,[1998];=20 Uchida et al.,[2000]).=20 Three criteria of stem cells were also satisfied by these isolated = BTSCs:=20 extended proliferation, self-renewal, and multipotency. = Self-renewal was=20 demonstrated in vitro by limiting dilution and clonal analyses to = show=20 BTSC's ability to form primary, secondary, and tertiary = neurospheres=20 (Ignatova et al.,[2002];=20 Singh et al.,[2003];=20 Galli et al.,[2004]),=20 and in vivo by serial transplantation and tumor formation in=20 immunodeficient mice (Singh et al.,[2004b]).=20 These BTSCs also expressed stem cell-associated markers exhibited = by fetal=20 and adult NSCs, including CD133 and nestin (Uchida et al.,[2000];=20 Singh et al.,[2003];=20 Yuan et al.,[2004];=20 Fig. 1).=20 Upon exposure to differentiation conditions, BTSCs displayed = markers of=20 multiple different neural fates, including glial (glial fibrillary = acidic=20 protein, GFAP) and neuronal (III-tubulin, a.k.a. Tuj1; Fig. 1)=20 cell lineages, although sometimes in aberrant patterns (Ignatova = et=20 al.,[2002];=20 Singh et al.,[2003];=20 Galli et al.,[2004]).=20

    Figure 1. Isolation of = human=20 brain tumor stem-like cells (BTSCs) and parallels to normal = fetal=20 neural stem cells (NSCs). When cultured in conditions = encouraging=20 stem cell growth, BTSCs proliferate as neurospheres (A1) = similar to=20 NSCs (A2). BTSCs also express specific stem cell markers = such as=20 CD133 (A3) and nestin (A5), with staining patterns = equivalent to=20 NSCs (A4, A6). Under differentiation conditions, BTSCs = exhibit=20 multipotency to neural and glial lineages, displaying = extending=20 processes when plated (B1) and expression of = lineage-specific=20 proteins, including III-tubulin (neurons; B3) and = glial=20 fibrillary acidic protein (GFAP, astrocytes; B5). This=20 differentiation resembles that of normal NSCs (B2, B4, = B6).
    [Normal View 55K | = Magnified View=20 224K]

    Although cancer stem cells have been isolated from multipe = types of=20 both solid and liquid cancers, it should be noted that much of = their cell=20 biology and relationship to normal stem cells remains unknown, and = they=20 are now functionally isolated and defined as cells with stem-like=20 properties (Clarke et al.,[2006]).=20 Self-renewal and multipotency are critical defining properties of = cancer=20 stem cells and are currently assayed by molecular markers and = serial=20 transplantation of putative cancer stem cells and subsequent tumor = formation in an orthotopic animal model (Singh et al.,[2004b];=20 Clarke et al.,[2006]).=20 A current paucity of stem cell markers for many tissue lineages = prevents=20 geneology tracing to determine the cellular origin of cancer stem = cells,=20 making the functional in vivo self-renewal assay the most reliable = currently available (Clarke et al.,[2006]).=20 Tumor sphere formation, such as neurospheres for BTSCs, provides a = powerful tool for the study of cancer stem cell self-renewal in = culture,=20 but care must be taken in the interpretation of these results = because the=20 in vitro assay may or may not be selecting the cancer stem cells = (Clarke=20 et al.,[2006])=20 and is a phenomenon that does not occur in vivo (Chaichana et = al.,[2006]).=20 Even the term tumor initiating cell can lead to confusion, as = cancer stem=20 cells may not actually initiate tumors but be stimulated to = neoplastic=20 transformation by environmental insults (Clarke et al.,[2006]).=20 While mindful of these current limitations in studying cancer stem = cells=20 and BTSC, many intriguing similarities are observed between BTSCs = and=20 NSCs.

    During development or after xenograft injection, normal NSCs = exhibit a=20 high degree of motility throughout the brain (Dirks,[2001];=20 Watson et al.,[2006]).=20 This property is especially demonstrated when NSCs are injected=20 immediately after injury (Hayashi et al.,[2005];=20 Belmadani et al.,[2006];=20 Chang et al.,[2007])=20 or during tumorigenesis (Lee et al.,[2003];=20 Ehtesham et al.,[2005];=20 Li et al.,[2007b]).=20 Normal NSCs exhibit an uncanny ability to home to cytokine signals = and=20 engraft to repair injured areas. A hallmark of certain brain = tumors such=20 as GBM is their infiltrative nature, including invasion into the = brain=20 along white matter tracts such as the corpus callosum (Galli et = al.,[2004];=20 Singh et al.,[2004b];=20 Lee et al.,[2006]).=20 With the identification of BTSCs, it was postulated that these may = be the=20 main cells involved in infiltration (Dirks,[2001]).=20 It was observed that orthotopically injected BTSCs display high = motility=20 and easily migrate throughout the brain (Galli et al.,[2004];=20 Lee et al.,[2006]).=20 After injection and tumor formation in the striatum of = immunodeficient=20 mice, BTSCs can even be found in the olfactory bulb (Lee et = al.,[2006]),=20 a site distant from the injection but similar to the rostral = migratory=20 stream of normal NSCs from the lateral ventricle to the olfactory = bulb.=20 Such observations provide evidence that NSCs and BTSCs may respond = to=20 migratory cues in similar fashions, leading to the proposed use of = NSCs to=20 inhibit glioma growth (Staflin et al.,[2004])=20 or as delivery vehicles for antitumor therapeutics (Ehtesham et = al.,[2005]).

    BTSCs cultured in serum-free stem cell conditions also = genetically=20 resemble NSCs in the expression of stem cell-specific genes, = whereas=20 glioblastoma cells expanded using traditional serum culture = genetically=20 deviate over multiple in vitro passages from NSCs as well as the = parental=20 tumor source. After microarray analysis and unsupervised = hierarchical=20 cluster analysis of BTSCs isolated in serum and serum-free = conditions,=20 normal NSCs, and parental tumor, Lee et al. ([2006])=20 found two main clusters of genetic expression: one group involving = BTSCs,=20 NSCs, and parental GBM, and the other group involving serum = cultured cells=20 and their subsequent xenograft tumors. Additional functional = annotation of=20 genes enriched in BTSCs and primary GBM versus serum cultured = cells=20 predicted expression of genes that are involved in central nervous = system=20 (CNS) development, CNS function, and cell-to-cell signaling. = Finally, a=20 cluster of 200 genes compiled from the literature as unique to = NSCs was=20 compared with BTSCs and primary GBM and revealed similar = regulation of=20 these genes. Taken together, one conclusion was that BTSCs are = remarkably=20 genetically similar to normal NSCs (Lee et al.,[2006]).=20 Microarray analysis was also used to show up-regulation of = stem-like genes=20 in CD133+ BTSCs of GBM compared with the = CD133-=20 tumor cells that represent the differentiated cells of the tumor = mass=20 (Beier et al.,[2007]).

    Retrospective clinical observations also implicate BTSCs as the = main=20 drivers of tumor growth and recurrence. Pediatric brain tumors = such as=20 medulloblastoma are hypothesized to result from aberrant = developmental=20 processes (Maris and Denny,[2002]),=20 and histological evidence has pointed to hyperproliferation of = external=20 granule cells, implicating a primitive cerebellar stem cell in=20 medulloblastoma tumorigenesis (Kadin et al.,[1970];=20 Rubinstein,[1972];=20 Singh et al.,[2004a]).=20 GBM is thought to arise from a multipotent cell from observation = of both=20 neural and glial expression within tumors (Galderisi et al.,[2006]).=20 The NSC markers nestin and CD133 were also shown to be present in = multiple=20 brain tumors (Dahlstrand et al.,[1992];=20 Tohyama et al.,[1992];=20 Almqvist et al.,[2002];=20 Schrot et al.,[2007]),=20 and higher levels of nestin+ cells, presumably the = BTSCs,=20 correlate with increased tumor grade in astrocytomas (Mao et = al.,[2007]).=20 Comparative microarray analyses reached a similar conclusion that = higher=20 grade tumors express higher levels of neural stem cell markers, = whereas=20 lower grade express markers of neuroblasts or neurons (Phillips et = al.,[2006]).

    Brain tumors and their tumor initiating cells share many = properties=20 with NSCs that may be exploited for increased understanding of = tumor=20 biology, possibly leading to improved clinical therapies. Recent = findings=20 in brain tumors and BTSCs demonstrate the expression and = involvement of=20 pathways classically associated with neural development, including = the=20 WNT, Notch, Hedgehog, and TGF/BMP pathways. Modulation of these = pathways may=20 represent novel therapeutic approaches for brain cancer.

    TGF/BMP PATHWAY
    3D"TGF/BMP 3D""=20

    The TGF/BMP signal transduction pathway is = crucial=20 during development. The BMP family, a subset of the TGF superfamily and originally = discovered in bone=20 and cartilage development, has been shown to play many roles = throughout=20 CNS cell determination and differentiation. In general, TGF proteins are involved in controlling = differentiation and proliferation of many cell types; therefore, = they are=20 intensively studied.

    The most common TGF signal transduction pathway involves = SMADs,=20 homologs to Ceanorhabditis elegans Sma and = Drosophila Mad,=20 and begins when TGF binds to a type II receptor. For = BMP-specific=20 signaling, this receptor is BMPR2. After TGF binding to a type II receptor, a = type I receptor=20 is recruited to form a hetero-tetrameric complex, thus inducing=20 serine/threonine kinase signaling. The recruited type I receptor = contains=20 a serine-rich domain, while the type II receptor, which is = recruited by=20 TGF, acts to phosphorylate and activate = serine=20 residues on the type I receptor. The activated serine domain then=20 phosphorylates a receptor-regulated SMAD (R-SMAD) protein. The = R-SMAD=20 binds with a coSMAD, and this complex then enters the nucleus to = bind=20 transcription promoters and cofactors leading to transcription of=20 downstream effectors (Padgett et al.,[1997];=20 Wrana,[1998]).=20 BMPs lead to transcription of genes involved in neurogenesis, as = well as=20 osteogenesis, while TGF proteins lead to transcription of = genes involved=20 in immunosuppression, as well as cellular apoptosis, among other=20 processes. Multiple extracellular regulators of TGF/BMP have been identified, including = noggin and=20 chordin (Fig. 2),=20 and inhibitory SMADs are described that block intracellular signal = transduction. TGF/BMP signaling is closely related to = and=20 interacts with many other significant developmental pathways, = including=20 the WNT signaling pathway (Attisano and Labbe,[2004]).=20

    Figure 2. Pathways = involved in=20 neural development. A: The TGF/BMP pathway. Inactivated = transmembrane=20 heterodimeric receptors exist separately. Upon activation by = TGF or BMP ligand, the receptors = associate and=20 the type II receptor phosphorylates the serine residue of = the type I=20 receptor. This in turn leads to phosphorylation of = intracellular=20 SMAD proteins, association with a coSMAD, localization into = the=20 nucleus, promoter binding by means of a CBP/p300 complex, = and=20 downstream gene expression. B: Canonical WNT pathway. = During=20 inactivation, a complex involving Axin, APC, and GSK3 acts to phosphorylate -catenin, slating it for = proteolysis. Upon=20 binding of WNT ligand to a Frizzled receptor and association = with=20 LRP, DSH is activated and represses GSK3. This repression prevents = phosphorylation=20 and allows cytosolic accumulation of -catenin, leading to nuclear = localization=20 and gene expression by means of a TCF/LEF complex. C: = Notch=20 pathway. Signaling is activated by ligand binding (Delta or = Jagged)=20 to the Notch receptor. Cleavage of the Notch receptor = results in=20 both extracellular and intracellular domains. The = intracellular=20 domain (NICD) localizes to the nucleus, where it associates = with=20 MAML and induces gene expression after promoter binding by = means of=20 a complex involving CSL. D: Hedgehog signaling. = During=20 inactivation, Patched works to repress the action of = Smoothened and=20 intracellular Gli proteins are repressed as part of the Sufu = complex. Sonic Hedgehog binding to Patched inhibits its = repression=20 of Smoothened, which in turn inactivates the Sufu complex. = This=20 repression frees Gli, allowing nuclear localization and gene = expression. Regulation of all pathways exists at multiple = levels,=20 including inhibitory SMADs (iSMADs) for BMP signaling, DKK = and sFRP=20 for WNT signaling, and HHIP for Hedgehog signaling, among = others.=20 TGF, transforming growth factor = ; BMP, bone morphogenetic = protein; SMAD,=20 Sma/MAD protein; APC, adenomatosis polyposis coli; GSK3, glycogen synthase kinase = 3; -cat, -catenin; TCF/LEF, T-cell=20 factor/lymphoid-enhancer factor; MAML, Mastermind-like; = Sufu,=20 suppressor of fused homolog; DKK, Dickkopf homolog 1; sFRP, = secreted=20 frizzled-related protein; HHIP, hedgehog interacting = protein.
    [Normal View 61K | = Magnified View=20 180K]

    Because of the significant roles of TGF/BMP in development, dysregulation of = this=20 pathway has been investigated in cancer as a possible mechanism = leading to=20 uncontrolled proliferation. Normally, TGF acts as an inhibitor of cell = proliferation;=20 however, in various cancers, aberrant TGF signaling is markedly increased. = Cancerous cells=20 fail to respond to TGF protein, but may benefit=20 from other aspects of the signaling pathway, including its = angiogenic and=20 possible immunosuppressive roles, as TGF has been shown to minimize immune = surveillance=20 and potentially play a role in metastasis (Gold,[1999];=20 Sun,[2004]).=20 The action of TGF has also been observed in = immunoresistant human=20 glioma cells, where TGF proteins are significantly = up-regulated (Gomez=20 and Kruse,[2007]).=20 It appears that, in many cancer cells, elements of the TGF signaling pathway have been = interrupted or=20 suppressed, precluding TGF's check on cell proliferation = (Casanueva et=20 al.,[2006]).=20 Specifically, mutation of SMAD-4 has been linked to human = populations that=20 show a higher incidence of gastrointestinal polyps and cancer = (Miyaki and=20 Kuroki,[2003]).=20 In malignant gliomas, BMP receptors and ligands have been detected = and=20 increased expression correlates with tumor grade (Yamada et = al.,[1996]).=20 In medulloblastoma cells, BMP-2 induced apoptosis, whereas the BMP = antagonist noggin prevented apoptosis induced by BMP or retinoids=20 (Hallahan et al.,[2003]).=20 Addition of BMP2 to neuroblastoma cell lines induced growth arrest = and=20 differentiation (Nakamura et al.,[2003]).=20 The effects of TGF/BMP signaling have a clear influence = on tumor=20 growth.

    The role of TGF/BMP signaling and its effects on = BTSC growth and=20 tumor potential were recently demonstrated. Piccirillo et al. ([2006])=20 first tested the growth effects of BMP on CD133+ BTSC = and found=20 multiple ligand effects, with strongest growth inhibition induced = by BMP4.=20 BMP4 also increased differentiation while decreasing the overall=20 CD133+ BTSC population (Piccirillo et al.,[2006]).=20 SMAD signaling was also activated in BTSC, indicating normal = intracellular=20 transduction of the TGF/BMP signal. Co-engraftment of BTSC = and BMP4=20 successfully halted BTSC-driven tumor progression, whether BMP4 = was=20 injected at the same time or 10 days after BTSC injection. BMP4 = treatment=20 blocked tumor growth and mortality in 100% of the studied mice = (Piccirillo=20 et al.,[2006]).

    WNT = PATHWAY
    3D""=20 3D"WNT 3D""=20

    The WNT pathway, so named in humans because of homologs to the=20 Drosophila wingless (wg) and mouse int-1, is involved in = many key=20 developmental processes such as proliferation, stem cell = maintenance,=20 pattern formation, and differentiation (Ille and Sommer,[2005]).=20 Canonical, or WNT/-catenin, signaling is the most = thoroughly=20 studied WNT pathway, but the molecule has also been shown to = function=20 through two other pathways: the WNT/Ca2+ and planar = cell=20 polarity (PCP; Kuhl et al.,[2000];=20 Strutt,[2003];=20 Ille and Sommer,[2005]).

    In the canonical pathway, WNT acts as a secreted molecule and = begins=20 signaling by binding to a seven-transmembrane receptor called = Frizzled=20 (FZD) and a low-density lipoprotein receptor-related protein = (LRP).=20 Activation of this complex by WNT leads to phosphorylation of = Dishevelled=20 (Dsh). In the cytoplasm of the cell, -catenin usually exists as part of a = destruction=20 complex including Axin, adenoma polyposis coli (APC) and glycogen = synthase=20 kinase-3 (GSK3). Without WNT signaling, -catenin is phosphorylated by = GSK3, slating it for destruction by means = of the=20 ubiquitin-proteasome pathway. In the presence of WNT signaling, = Dsh=20 inhibits the activity of GSK3 leading to accumulation of -catenin and eventually its transport = into the=20 nucleus in a concentration-dependent manner. In the nucleus, -catenin associates with T-cell=20 factor/lymphoid-enhancer factor (TCF/LEF) transcription factors = leading to=20 transcription of downstream targets (Fig. 2;=20 Ille and Sommer,[2005];=20 Reya and Clevers,[2005]),=20 including proliferation genes such as cyclin D1 and MYC (He et = al.,[1998];=20 Chan et al.,[1999];=20 Shtutman et al.,[1999]).=20 Inhibitors of WNT signaling exist at multiple levels of the = pathway.=20 LRP-binding factors (Dickkopf, DKK) and secreted FZD-related = proteins=20 (sFRP) prevent formation of the WNT/receptor complex to block = signaling at=20 the receptor level (Glinka et al.,[1998];=20 Ille and Sommer,[2005]).=20 At the nuclear level, complex formation between TCF/LEF and -catenin can be inhibited by inhibitor of -catenin and TCF-4=20 (ICAT). DNA-binding affinity of the -catenin/TCF complex is modulated by = Nemo-like=20 kinase (NLK) and can indirectly regulate nuclear WNT signaling. = The=20 transcriptional repressor Pitx2 also works in the nucleus to = modulate WNT=20 signaling.

    WNT signaling has been shown to be involved in multiple cancer = types=20 (Reya and Clevers,[2005]).=20 Aberrant WNT signaling was first implicated in brain tumors = through study=20 of patients with Turcot's syndrome, which involves an APC mutation = linked=20 to a high incidence of colorectal cancers and brain tumors, = particularly=20 medulloblastoma (Hamilton et al.,[1995];=20 Wechsler-Reya and Scott,[2001]).=20 Mutations in Axin, -catenin, and APC were also found in = sporadic=20 medulloblastomas (Huang et al.,[2000];=20 Dahmen et al.,[2001];=20 Koch et al.,[2001];=20 Yokota et al.,[2002];=20 Baeza et al.,[2003]);=20 nuclear localization of -catenin suggesting constitutive WNT = signaling=20 has also been found (Eberhart et al.,[2000]).=20 Mutations of the WNT signaling pathway in medulloblastomas may = represent a=20 distinct molecular subgroup with its own set of genomic = aberrations=20 (Clifford et al.,[2006];=20 Thompson et al.,[2006]).=20 The WNT antagonist DKK-1 has been implicated as a medulloblastoma=20 suppressor that is epigenetically silenced during tumorigenesis, = and its=20 re-activation decreased tumor cell growth by 60% while increasing=20 apoptosis fourfold (Vibhakar et al.,[2007]).

    Some evidence also exists for WNT signaling in astrocytomas. = The WNT=20 receptor FZD9 was immunohistochemically detected and up-regulated = in human=20 astrocytomas, with staining intensity correlated to histological = grade=20 (Zhang et al.,[2006b]).=20 The production of sFRPs by human malignant astrocytoma cell lines = has been=20 demonstrated and shown to modulate growth and inhibit motility = (Roth et=20 al.,[2000]).=20 Ectopic expression of DKK-1 in the U87MG astrocytoma cell line = sensitized=20 these cells to DNA damage and induced much higher levels of = apoptosis=20 after chemotherapy (Shou et al.,[2002]).

    NOTCH = PATHWAY
    3D""=20 3D"NOTCH 3D""=20

    The Notch signaling pathway plays several significant roles in = both the=20 development and maintenance of organisms. In development, Notch is = responsible for lateral inhibition of surrounding cells, a = significant=20 mechanism of cell fate determination and proliferation (Liu et = al.,[2003];=20 Ehebauer et al.,[2006]).=20 Notch expression may be used to locate neural precursors within = embryonic=20 tissues (Basak and Taylor,[2007])=20 and has been used to track the mechanism of division in neural = precursors=20 (Tsai,[2004]).=20 Notch signaling is vital to organogenesis during embryonic = development=20 (Zhu et al.,[2006]),=20 this pathway is involved in determining cell fate by amplifying = variation=20 in nearly homogenous cell populations. Notch also participates in = cell=20 fate determination during creation and repair of differential = tissue=20 layers, as seen in epidermal and gut epithelia (Thelu et al.,[2002];=20 Ehebauer et al.,[2006];=20 Red-Horse et al.,[2007]).=20 The Notch pathway is expressed both in vitro and in vivo in adult = stem=20 cells (Campos,[2004];=20 Campos et al.,[2006]).=20 It is required for the maintenance of general stem cell = populations, which=20 undergo terminal differentiation without Notch expression=20 (Varnum-Finney et al.,[2003];=20 Molofsky et al.,[2004];=20 Ma et al.,[2005];=20 Alexson et al.,[2006]).=20 Notch also has a role during the renewal of existing cell = populations=20 through proliferation of progenitor cells, particularly during = epidermal=20 wound repair or in neuronal cell replacement (Morrison et al.,[2000];=20 Morrison,[2001];=20 Thelu et al.,[2002];=20 Liu et al.,[2003];=20 Miller,[2007]).

    The Notch signaling pathway (Fig. 2)=20 resembles other developmental signaling pathways, with some unique = differences. The Notch protein family consists of four = transmembrane=20 receptor proteins that share several key features, including a = repeating=20 EGF domain in the extracellular component (Liu et al.,[2003];=20 Bray,[2006];=20 Ehebauer et al.,[2006];=20 Kelleher et al.,[2006]).=20 The Notch protein is targeted by the ligands Delta (DLL) and = Jagged (JAG),=20 which are transmembrane proteins integrated into the membrane of=20 neighboring cells (Karanu et al.,[2000]).=20 When one of these ligands binds to Notch, two proteolytic cleavage = events=20 are promoted. The first of these cleavage events is linked to the = sheddase=20 tumor necrosis factor alpha converting enzyme (TACE), a member of = the ADAM=20 metalloprotein family (Brou et al.,[2000]).=20 TACE allows the cell to shed the extracellular domain of Notch, = which is=20 taken up by the ligand-expressing cell through endocytosis. = Following TACE=20 action, the -secretase complex, an integral membrane protein = associated with=20 a wide range of cellular actions, liberates the Notch = intracellular domain=20 (NICD) from the cell membrane through a second cleavage event = (Shih and=20 Wang,[2007]).=20 Once NICD has been released into the cytoplasm, it is transported = to the=20 nucleus where it forms a coactivator complex with Mastermind-like = (MAML)=20 and activates DNA binding protein CSL complex (CSL; Bray,[2006];=20 Kelleher et al.,[2006]).=20 This process causes expression of several of the target genes of = Notch,=20 including HES1 and HES5, and continues until NICD is = phosphorylated by=20 cyclin-dependent kinase 8 (CDK8). Phosphorylated NICD is then=20 ubiquitinated and undergoes proteolysis, allowing repressor = complexes to=20 halt further CSL function. Aside from the primary pathway, several = other=20 factors activate or suppress Notch function within the cell, = including=20 several major signaling pathways (Bray,[2006];=20 Campos et al.,[2006];=20 Niimi et al.,[2007]).

    In addition to participating in stem cell proliferation, the = Notch=20 pathway has also been associated with tumor development, = potentially as an=20 oncogene (Radtke and Raj,[2003];=20 Weng and Aster,[2004]).=20 However, the exact nature of oncogenic Notch signaling is unclear, = as it=20 has also been shown to act as a tumor suppressor. Notch and its = family=20 members have different effects on cell fate during development = (Fan et=20 al.,[2004]),=20 and Notch's involvement in tumorigenesis may also be dependent on = the=20 cellular and tissue context (Kunnimalaiyaan and Chen,[2007]).=20 The correlation between brain tumor growth and notch expression is = well=20 documented for several tumor types. In medulloblastomas grown in=20 transgenic mice, high levels of NOTCH1 signaling were detected in = the=20 tumor mass compared with unaffected tissue, whereas NOTCH2 was=20 down-regulated (Dakubo et al.,[2006]).=20 NOTCH1 and NOTCH2, as well as the notch ligand JAG1, have been = found=20 up-regulated in malignant meningiomas cultured from fresh tumor = specimens=20 (Cuevas et al.,[2005]).=20 Primary GBM tissue has been shown by reverse = transcriptase-polymerase=20 chain reaction to express high levels of NOTCH3 and increased HES1 = transcription compared with typical neural tissue (Kanamori et = al.,[2007]).=20 Expression of NOTCH1 and several of its ligands was shown to be = required=20 for continued survival and proliferation of astrocytoma cells = (Purow et=20 al.,[2005];=20 Kanamori et al.,[2007]).=20 By silencing the expression of any of these proteins, cell growth = was=20 inhibited both in culture and in xenograft. In the established = U373=20 astrocytoma line, a subpopulation of cells has been isolated that = exhibit=20 stem-like properties, increased rates of growth and high levels of = Notch=20 expression (Patrawala et al.,[2005]).

    Evidence is growing in support of notch signaling leading to = brain=20 tumor development driven by BTSC. In GBM tissue samples, high = nestin=20 levels have been associated with high levels of Notch expression,=20 suggesting correlation between BTSC and Notch expression (Shih and = Holland,[2006]).=20 After global gene microarray analysis, it was found that Notch = expression=20 in brain tumors correlated with good versus poor prognosis = (Phillips et=20 al.,[2006]).=20 Pharmacologically blocking the -secretase complex in medulloblastomas decreased the = quantity of=20 CD133+ BTSCs in culture and inhibited proliferation = (Fan et=20 al.,[2006]).=20 When implanted into nude mice, cells treated with a -secretase inhibitor demonstrated reduced ability to = form=20 tumors.

    HEDGEHOG = PATHWAY
    3D""=20 3D"HEDGEHOG

    The Hedgehog (HH) pathway includes signaling mediated through = three=20 different polypeptide ligands: Sonic, Indian, and Desert Hedgehog. = Sonic=20 Hedgehog (SHH) is one of the best studied in CNS development and=20 participates in many key developmental processes, including = controlling=20 cell differentiation and proliferation as well as morphogenesis = (Dahmane=20 et al.,[2001]).=20 Recently, HH signaling was also shown to be active in self-renewal = and=20 maintenance of NSCs (Lai et al.,[2003];=20 Machold et al.,[2003];=20 Ahn and Joyner,[2005];=20 Palma et al.,[2005];=20 Liu et al.,[2006]).

    The HH signaling cascade is initiated by HH binding to the cell = surface=20 receptor Patched (PTCH). In the absence of HH, PTCH inhibits the = activity=20 of a seven membrane spanning G-protein-coupled receptor-like = receptor=20 called Smoothened (SMO). HH binding relieves PTCH inhibition, and = SMO is=20 allowed to signal downstream. Smoothened activates the family of = GLI=20 transcription factors, which then translocate to the nucleus and = initiate=20 transcription (Ingham and McMahon,[2001];=20 Lum and Beachy,[2004];=20 Rubin and de Sauvage,[2006];=20 Fig. 2).=20 Regulation of HH signaling occurs at multiple levels, much like = the other=20 developmental pathways. Binding of HH to PTCH leads to = internalization and=20 sequestration of the complex, forming a negative feedback system = for HH=20 signaling (Incardona et al.,[2000]).=20 Regulation also occurs by means of HH-interacting protein (HHIP), = which=20 sequesters HH proteins and prevents their binding to PTCH (Jeong = and=20 McMahon,[2005]).=20 Intracellularly, GLI proteins are regulated by suppressor of fused = homolog=20 (SUFU) complex (Rubin and de Sauvage,[2006]).=20 Although their involvement in normal signaling is unknown, many = small=20 molecule inhibitors of SMO exist that inhibit HH signaling (Cooper = et=20 al.,[1998];=20 Incardona et al.,[1998];=20 Taipale et al.,[2000];=20 Chen et al.,[2002];=20 Rubin and de Sauvage,[2006]).

    The involvement of HH signaling in brain tumorigenesis is best=20 characterized in medulloblastoma. A subset of medulloblastomas = harbor=20 mutations of the PTCH gene (Vorechovsky et al.,[1997];=20 Zurawel et al.,[2000]).=20 A small percentage of transgenic heterozygous PTCH+/- = mice=20 sporadically develop medulloblastomas (Goodrich et al.,[1997]),=20 and altered expression of other HH signaling components such as = SMO or SHH=20 itself also lead to medulloblastoma-like growths (Weiner et = al.,[2002];=20 Hallahan et al.,[2004];=20 Rao et al.,[2004];=20 Fults,[2005];=20 Piedimonte et al.,[2005]).=20 These mouse models are powerful tools for characterizing the = development=20 of medulloblastoma and for screening anti-HH therapeutics. The = progression=20 of medulloblastoma in these mouse models supports tumor initiation = from=20 hyperactive stem-like or progenitor cells. Mice engineered to = overexpress=20 SMO from the NeuroD2 promoter (specific to early cerebellar = granule=20 neuronal precursors) that were euthanized before onset of = neurological=20 symptoms displayed hyperproliferation of the progenitor cells in = 80% of=20 cases (Hallahan et al.,[2004]).=20 Conditional viral transfection of mice to overexpress SHH leads to = medulloblastoma formation from nestin-expressing neural = progenitors, and=20 can be modulated with co-overexpression with insulin-like growth = factor=20 (IGF) or Akt (Rao et al.,[2004]).=20 Targeting the overexpressed SHH pathway in medulloblastoma = tumorigenesis=20 has thus been researched in depth and shows great promise. Use of=20 cyclopamine, a steroidal alkaloid inhibitor of SMO, was shown to = decrease=20 medulloblastoma cell growth in vitro and in vivo (Dahmane et = al.,[2001];=20 Berman et al.,[2002]).=20 In vitro, cyclopamine also drives medulloblastoma cells from a = stem cell=20 phenotype into a more differentiated state (Berman et al.,[2002]).=20 Cyclopamine was shown to reverse the effects of oncogenic = mutations in SMO=20 and PTCH (Taipale et al.,[2000]),=20 demonstrating potential as a therapeutic agent that may target = many types=20 of tumors exhibiting dysregulated SHH signaling. Other small = molecules=20 that inhibit SMO or downstream effectors such as the GLI proteins = have=20 shown similar success (Chen et al.,[2002];=20 Gabay et al.,[2003];=20 Williams et al.,[2003];=20 Lauth et al.,[2007]).=20 Importantly, treatment with SHH signaling inhibitors has been = shown to=20 inhibit medulloblastoma initiation in allograft mouse tumors = (Berman et=20 al.,[2002]),=20 and surprisingly can prevent medulloblastoma growth in = PTCH+/-=20 mice, even with concurrent knockout of p53 (p53-/-; = Romer and=20 Curran,[2005]).=20 As a small molecule, cyclopamine also has the ability to cross the = blood-brain barrier to systemically inhibit medulloblastoma in=20 PTCH+/- p53-/- mice, with no observed side = effects=20 (Sanchez and Ruiz i Altaba,[2005]).

    In glioblastomas, SHH has also shown involvement in tumor = initiation=20 and propagation. In both tumor cell lines and primary = astrocytomas, mRNA=20 expression for both PTCH and SMO was shown to inversely correlate = with=20 histological grade, highest in grade II astrocytomas and lowest in = grade=20 IV astrocytomas (Katayama et al.,[2002]).=20 Similar results found that grade II and III astrocytomas express = and=20 respond to extrinsic regulation of SHH pathway components, whereas = grade=20 IV astrocytoma do not (Ehtesham et al.,[2007]).=20 Of interest, PTCH expression indicating SHH pathway activity = colocalized=20 with stem-like cells expressing Ki67 (mitosis marker) and Bmi-1 = but not=20 with the differentiation marker GFAP. SHH induced = hyperproliferation of=20 precursor cells in both embryonic and postnatal mouse brain cells. = Pathway=20 components including PTCH and GLI were identified in high- and = low-grade=20 astrocytomas, and cyclopamine blockade decreased the growth of = brain tumor=20 cell lines and primary grade IV astrocytoma cells (Dahmane et = al.,[2001]).=20 In ependymomas, genome-wide analysis using microarray and other = techniques=20 has implicated aberrant SHH activity, among other developmental = pathways,=20 in a subset of these tumors (Modena et al.,[2006]).=20 The potential for targeting the SHH pathway to prevent BTSC-driven = gliomas=20 has also been shown. Blocking SMO signaling with pharmaceutical or = lentiviral techniques drastically inhibited cell proliferation and = self-renewal of BTSC in culture and halted BTSC-driven = tumorigenesis in=20 xenograft model (Bar et al.,[2007];=20 Clement et al.,[2007]).=20 Therefore, developmental pathways such as SHH are required for = BTSC and=20 glioma growth and may serve as effective targets for developing = novel=20 therapies.

    PERSPECTIVES/CONCLUSION
    3D""=20 3DPERSPECTIVES/CONCLUSION=20

    The significant parallels between normal neural stem cells = (NSCs) and=20 brain tumor stem-like cells (BTSCs) support a hypothesis of = tumorigenesis=20 that co-opts mechanisms used in normal brain development. This = view is not=20 entirely new and has been hypothesized in the past (Globus and=20 Kuhlenbeck,[1944];=20 Hamburger and Salmon,[1977]),=20 but recent findings provided compelling evidence of a hierarchy of = stem=20 and progenitor cells in various cancers related to normal = development=20 (Bonnet and Dick,[1997];=20 Al-Hajj et al.,[2003];=20 Singh et al.,[2003]).=20 Expression and mutation of components of multiple developmental = signaling=20 pathways such as BMP/TGF, WNT, Notch, and SHH have been = demonstrated in=20 various brain tumors, although their exact role(s) in = tumorigenesis=20 remains unclear. The close similarity of BTSC and NSC may explain = how=20 aberrant expression of normal developmental mechanisms could = potentially=20 be involved in the cancer initiation and growth. Improved = understanding of=20 these pathways during normal development could aid in elucidating = the=20 underlying biology of their role in tumorigenesis (Wechsler-Reya = and=20 Scott,[2001]),=20 even if their current biological significance for cancer is = largely=20 unknown.

    Many unanswered questions still remain relating to the biology = and=20 neoplastic events giving rise to BTSCs. Due to limited = availability of=20 many adult tissue stem cell markers, the geneology of isolated = BTSCs is=20 yet to be determined, and the origin of the BTSCs in brain tumors = is a=20 subject of debate (Clarke et al.,[2006]).=20 Evidence exists for both neoplastic transformation of resident NSC = as well=20 as re-acquisition of stem cell properties by progenitor or = differentiated=20 cells (Holland et al.,[2000];=20 Dai et al.,[2001];=20 Jackson et al.,[2006];=20 Kang et al.,[2006];=20 Krivtsov et al.,[2006];=20 Read et al.,[2006];=20 Zhang et al.,[2006a];=20 Sharif et al.,[2007];=20 Shiras et al.,[2007]).=20 Aside from direct neoplastic transformation, BTSCs may also arise = from=20 disruptions in the stem cell niche or tumor stroma leading to = unregulated=20 proliferation and self-renewal (Clarke et al.,[2006]),=20 such as postulated after disruption of Notch-mediated lateral = inhibition.=20 The exact identity or surface marker signature of BTSCs themselves = remains=20 elusive as well. Currently, CD133 is the standard for identifying = BTSCs=20 within brain tumors and has been shown to enrich for cells with = tumor=20 initiation activity (Singh et al.,[2004b];=20 Bao et al.,[2006];=20 Piccirillo et al.,[2006]).=20 However, isolated CD133- cells have also demonstrated=20 tumorigenicity (Beier et al.,[2007]),=20 suggesting that a more stringent surface marker signature of BTSCs = is=20 required.

    Although discussed as a single group in this review, there are = many=20 histological types of brain tumors with probable heterogeneous = cellular=20 origins. It is likely that BTSCs isolated from each brain tumor = type will=20 exhibit distinct characteristics and behaviors. Even tumors = identified as=20 the same histological grade exhibit different properties (Modena = et=20 al.,[2006]),=20 and some evidence exist that these differences are reflected in = their=20 BTSCs (Beier et al.,[2007]).=20 It must also be noted that BTSCs within any single tumor may also = be a=20 dynamically evolving cell type (Lobo et al.,[2007]),=20 partially suggested by the sheer number of mutations in human = cancer=20 (Greenman et al.,[2007]),=20 and, therefore, tumors at different time points, such as primary = vs.=20 recurrent, may yield distinct BTSCs. These variances point to a = need for=20 molecularly characterizing an extensive number of BTSC subtypes.=20 Clinically, the extensive complexity of cancer phenotypes calls = for=20 improved diagnostics (Bild et al.,[2006];=20 Potti et al.,[2006];=20 Greenman et al.,[2007]),=20 possibly in the form of microarrays (Phillips et al.,[2006])=20 or molecular testing for specific pathway or stem cell markers = (Clement et=20 al.,[2007])=20 to augment traditional histological analyses. These improved = diagnostics=20 may result in improved, individualized patient treatments (Bild et = al.,[2006];=20 Potti et al.,[2006]).

    The expression of developmental signaling pathways may provide = insight=20 into the mechanisms used by BTSC to confer enhanced proliferative = and=20 self-renewal potential. In line with this hypothesis, regulators = of these=20 pathways have been shown to affect the growth of brain tumor cell = lines,=20 self-renewal of BTSCs, and most importantly tumor growth in = xenograft or=20 transgenic mice (Fan et al.,[2006];=20 Piccirillo et al.,[2006];=20 Clement et al.,[2007];=20 Vibhakar et al.,[2007]).=20 Much of this evidence exists for embryonal brain tumors (Fan et = al.,[2006];=20 Vibhakar et al.,[2007])=20 as these tumors are postulated to arise during early developmental = stages,=20 but evidence is also mounting that aberrant developmental = signaling could=20 be involved in adult brain tumors and BTSCs (Piccirillo et al.,[2006];=20 Clement et al.,[2007]).=20 Whether these pathways play a role in oncogenic transformation or = are=20 activated in BTSCs afterward to confer enhanced proliferative = abilities is=20 unknown. As these pathways become better understood in normal=20 developmental biology, they may shed light on their role in BTSCs = and=20 brain tumor biology.

    Manipulation of these developmental pathways in BTSC also = offers=20 promise in developing novel therapeutics for brain tumors that = often have=20 dismal prognoses. The tight regulation and high level of = redundancy seen=20 during normal neural development may provide multiple targets to=20 compensate for the great heterogeneity seen in brain tumors. = Initial=20 results in animal models have been encouraging. For example, = systemic=20 administration of a Hedgehog pathway inhibitor reduced = medulloblastoma=20 formation in transgenic mice, with no visible side effects = (Sanchez and=20 Ruiz i Altaba,[2005]).=20 However, rigorous testing of such therapeutics to determine = clinical=20 safety will be required to ensure that normal NSC or related = developmental=20 processes are minimally affected. Although much work must still be = done,=20 the prospect of using regulators of developmental pathways as = therapeutic=20 agents is an exciting one.

    In summary, intensive investigations on the roles of = developmental=20 signaling pathways in brain cancer present an opportunity for = fruitful=20 collaborations between the fields of developmental biology and = oncology.=20 Future research may lead to novel therapeutic strategies to target = BTSCs,=20 offering new approaches to halt tumor growth and recurrence in = cancers=20 with poor prognoses.

    Acknowledgements
    3D""=20 3DAcknowledgements=20

    We apologize to authors whose work could not be cited due to = space=20 constraints. We acknowledge support from the Department of = Neurological=20 Surgery, the School of Medicine and Public Health, and the = Graduate School=20 at University of Wisconsin-Madison.

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