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[Cancer Research 66, 4553-4557, May 1, 2006]
=A9 = 2006 American = Association=20 for Cancer Research

Reviews

Normal Stem Cells and Cancer Stem Cells: The Niche Matters=20

Linheng Li1,3 and = William B. Neaves1,2

1 Stowers Institute for Medical Research = and=20 2 University of Missouri-Kansas City School of Medicine, = Kansas City,=20 Missouri and 3 University of Kansas Medical Center, Kansas = City,=20 Kansas

Requests for reprints: Linheng Li, Stowers = Institute for=20 Medical Research, Kansas City, MO. E-mail: lil{at}stowers-institute.org .


3D"   =20 Abstract
Top
3D"Abstract
Is Cancer a Disease...
Homeostatic Regulation of Stem...
Stem Cell Niche: Gatekeeper...
Link between Stem Cell...
Closing Remarks
References
 
S= cientists=20 have tried for decades to understand cancer development in = the=20 context of therapeutic strategies. The realization that = cancers may=20 rely on "cancer stem cells" that share the self-renewal = feature of=20 normal stem cells has changed the perspective with regard to = new=20 approaches for treating the disease. In this review, we = propose that=20 one of the differences between normal stem cells and cancer = stem=20 cells is their degree of dependence on the stem cell niche, a = specialized microenvironment in which stem cells reside. The = stem=20 cell niche in adult somatic tissues plays an essential role = in=20 maintaining stem cells or preventing tumorigenesis by = providing=20 primarily inhibitory signals for both proliferation and=20 differentiation. However, the niche also provides transient = signals=20 for stem cell division to support ongoing tissue regeneration. = The=20 balance between proliferation-inhibiting and = proliferation-promoting=20 signals is the key to homeostatic regulation of stem cell = maintenance=20 versus tissue regeneration. Loss of the niche can lead to = loss=20 of stem cells, indicating the reliance of stem cells on niche = signals. Therefore, cancer stem cells may arise from an = intrinsic=20 mutation, leading to self-sufficient cell proliferation, = and/or=20 may also involve deregulation or alteration of the niche by=20 dominant proliferation-promoting signals. Furthermore, the = molecular=20 machinery used by normal stem cells for homing to or = mobilizing=20 from the niche may be "hijacked" by cancer stem cells for = invasion=20 and metastasis. We hope this examination of the interaction=20 between stem cells and their niche will enhance understanding = of the process of cancer development, invasiveness, and = metastasis=20 and reveal possible targets for cancer treatment. (Cancer Res = 2006; 66(9): 4553-7)


3D"    Is=20 Cancer a Disease of Stem Cells?
Top
Abstract
3D"Is Cancer a = Disease...
Homeostatic Regulation of Stem...
Stem Cell Niche: Gatekeeper...
Link between Stem Cell...
Closing Remarks
References
 
I= n recent=20 decades, biomedical research has revealed extraordinary = diversity=20 within the broad category of diseases known as cancers. This=20 astounding variety confounds attempts to find common features = among=20 the many forms of cancer. However, all clinically significant = cancers=20 share at least one common characteristic: excessive = proliferation of=20 affected cells. As highly differentiated cells rarely divide, = and=20 rapidly proliferating cells have poorly differentiated = phenotypes,=20 two basic therapeutic approaches for combating cancers have=20 developed: "differentiation therapy" (= 1) to=20 induce differentiation and "destruction therapy" (= 2) to=20 thwart malignant proliferation. Apart from limited success in = some=20 cases, neither of these approaches completely cures = cancer.=20

In the early 1990s, clinical observations and genetic studies = of a=20 variety of cancers led to the hypothesis that six genetic = mutations=20 were required to convert a normal somatic cell into a cancer = cell (= 3, = 4).=20 These six mutations included (a) self-sufficiency for = growth=20 signals, (b) insensitivity to antigrowth signals, = (c)=20 evasion of apoptosis, (d) limitless ability to replicate,=20 (e) sustained angiogenesis, and (f) tissue invasion = and=20 metastasis.

However, not all cells in a given tissue are created equally = in=20 terms of their stage of development and their potential for=20 proliferation and/or differentiation. Stem cells sit at the = top=20 of the developmental hierarchy, having the ability to self-renew = and=20 give rise to all the cell lineages in corresponding tissues. = Stem=20 cells divide to produce two daughter cells. One daughter = remains a=20 stem cell (self-renewal). The other daughter becomes a = progenitor=20 cell that undergoes expansion and further differentiation = into mature=20 cells. Stem cells have the highest potential for = proliferation and a=20 much longer life span compared with their progeny and = therefore have=20 a greater opportunity to accumulate genetic mutations (= 5).=20 The realization that the adult body harbors small numbers of = stem=20 cells offered an alternative possibility for the origin of = cancer.=20 Perhaps only one or two mutations, such as self-sufficiency = in growth=20 or insensitivity to antigrowth signals, are needed for stem = cells to=20 initiate tumorigenesis rather than six mutations, a rare = event in any=20 type of cell.

The thought that cancer might originate in stem cells harkens = back=20 to the 19th century concept of "embryonal rest" (= 6, = 7).=20 Over a century later, one recognizes the similarity between = the=20 old belief that cancer arises from embryonal rests and the=20 contemporary view that some forms of cancer originate in = adult=20 stem cells. In 1994, John Dick's lab showed that = leukemia-initiating=20 stem cells present in the peripheral blood of acute = myelogenous=20 leukemia (AML) patients (1 of 250,000 cells) could induce AML = when transplanted into severe combined immunodeficient (SCID) = mice (= 8).=20 Demonstration of tumorigenesis in SCID mice became convincing = proof=20 of the role of stem cells in perpetuating cancer in various = organs.=20 In 2003, Michael Clarke's lab conclusively showed the = presence of=20 stem cells in breast cancer (= 9).=20 The following year, Peter Dirks' lab unequivocally proved = stem=20 cell involvement in brain cancer (10).=20

Within established tumors, the great majority of the cancer = cells=20 cannot sustain the lesion nor establish it elsewhere in the = body.=20 Only a few cells within the tumor, the cancer stem cells, are = tumorigenic and possess the metastatic phenotype (= 5).=20 This circumstance has implications for both therapy and = research (11).=20 It explains why treatments that substantially reduce the = tumor mass=20 by removing proliferating cells fail to cure patients with = some types=20 of cancer, because cancer stem cells are usually slowly = cycling cells=20 and thus insensitive to these treatments. It also introduces = a note=20 of caution among researchers seeking insight from analysis of = a=20 cross-section of the tumor cell population. Gene expression = profiles=20 obtained from samples of heterogeneous tumor tissue probably = bear=20 limited resemblance to those of the tumor stem cell = population,=20 which forms only a tiny fraction of the whole tumor (12).=20

Anyone tempted to embrace the stem cell genesis of cancer too=20 warmly should remember the accumulated frustrations of the=20 two-century-long quest to find a unifying theory of how = malignant=20 tumors arise. Stem cell biology clearly holds critical = insight for=20 understanding and defeating many kinds of cancer, but not all = cancers=20 come from populations of self-renewing stem cells. Some forms = of=20 leukemia clearly come from true stem cells (13),=20 but cancer can also arise from progenitor cells downstream of = stem=20 cells. For example, Weissman's lab recently found that a = mutation=20 that enhances nuclear =DF-catenin in = granulocyte-macrophage=20 progenitor cells causes a blast crisis in some patients with=20 chronic myeloid leukemia (14).=20 It seems these mutated progenitor cells have acquired the = ability to=20 self-renew, a feature thought to be specific to stem cells, = and to=20 undergo unlimited growth as cancer cells. In this sense, = cancer may=20 prove to be more of a stem cell disease than previously = suspected (13,=20 15).=20 This concept has immediately changed the perspective of the=20 cancer field and shed light on new strategies for therapeutic = treatment of cancers.


3D"   =20 Homeostatic Regulation of Stem Cells by the Niche: a Balance = between=20 Self-renewal and Differentiation
Top
Abstract
Is Cancer a Disease...
3D"Homeostatic Regulation of=20 Stem...
Stem Cell Niche: Gatekeeper...
Link between Stem Cell...
Closing Remarks
References
 
I= n adults,=20 stem cells reside in a physiologically limited and = specialized=20 microenvironment, or niche, that supports stem cells but = varies in=20 nature and location depending on the tissue type (16,=20 17).=20 Remarkable progress has been made in studies regarding the=20 interaction between stem cells and their surrounding = microenvironment=20 in flies, Caenorhabditis elegans, and mammals. By = comparing=20 the stem cell niches in these systems, features and functions = common to all stem cell niches have emerged as follows (17=9619):

  • The stem cell niche is composed of a group of cells in = a=20 special location that functions to maintain stem = cells.=20
  • The niche is a physical anchoring site for stem cells, = and=20 adhesion molecules are involved in the = interaction=20 between stem cells and the niche and between = stem cells=20 and the extracellular matrix.
  • The niche generates extrinsic factors that control stem = cell number, proliferation, and fate = determination. Many=20 developmental regulatory signal molecules, = including hh,=20 Wnts, bone morphogenetic proteins (BMP), = fibroblast=20 growth factors, and Notch, have been shown to play = roles=20 in controlling stem cell self-renewal and in = regulating=20 lineage fate in different systems.
  • The niche controls normal asymmetrical division of stem = cells. This has been shown in invertebrates; = whether it=20 is conserved in the mammalian system is still an = open=20 question.

Normally, at least in the hematopoietic, intestinal, and hair=20 follicle systems, the niche maintains stem cells primarily in = a=20 quiescent state by providing signals that inhibit cell = proliferation=20 and growth as evidenced by the ability of stem cells to = retain=20 bromodeoxyuridine labeling for a relatively long period of = time=20 (20=9624).=20 Only upon receipt of a stimulating signal does the stem cell = become=20 activated to divide and proliferate (Fig.=20 1 ). Therefore, stem cell proliferation depends on = dynamic=20 niche signaling. Maintaining a balance between the = proliferation=20 signal and antiproliferation signal is the key to homeostatic = regulation of stem cells, allowing stem cells to undergo = self-renewal=20 while supporting ongoing tissue regeneration (25).=20 Any genetic mutation that leads stem cells to become = independent of=20 growth signals, or to resist antigrowth signals, will cause = the stem=20 cells to undergo uncontrolled proliferation and possible=20 tumorigenesis (Fig.=20 1). In this review, we will use recent studies of signaling=20 regulation of stem cells in bone marrow, intestine, and skin = to=20 show the importance of this balanced control of stem cells by = both=20 growth-promoting and growth-inhibiting signals.



View = larger=20 version (48K):
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  		Figure 1. Comparison of = the niches=20 under normal and cancerous conditions. The stem cell niche = under=20 normal physiological conditions provides an environment that = predominantly inhibits both proliferation and = differentiation.=20 However, a transient proliferating signal is required to = support=20 ongoing tissue regeneration. In cancer or tumors, owing to = internal=20 mutations, cancer stem cells become self-sufficient to = undergo=20 uncontrolled proliferation or, due to changes in the per se = or a=20 change in the niche signals, the niche is converted into an=20 environment with dominant signals favoring cell = proliferation and=20 growth. In some cases, a combination of these scenarios may = be=20 required. In addition, uncontrolled proliferation of = stem/progenitor=20 cells leads to expansion of the progenitor pool, which is = poised to=20 accumulate a secondary genetic mutation. =

 = ;
In=20 adults, hematopoiesis occurs in bone marrow in which hematopoietic=20 stem cells (HSC) are primarily located in the osteoblastic = niche=20 on the bone surface (21,=20 22,=20 26,=20 27).=20 Upon mobilization, HSCs and their progenitor cells are found = adjacent=20 to the sinusoid endothelial cells (vascular niche; refs. 28,=20 29).=20 It has been proposed that a gradient of osteoblastic niche to = vascular niche exists in bone marrow, with the osteoblastic = niche=20 providing a quiescent microenvironment, and the vascular = niche=20 favoring for proliferation and further differentiation (30).=20

In skin, stem cells are located in the bulge area of the hair=20 follicle (24).=20 Wnt signaling has been reported to play a role in promoting = stem cell=20 activation and expansion in skin (31,=20 32).=20 However, Wnt inhibitors, including Dkk, sFRP, and Wif, have = been=20 found to be dominantly present in the stem cell niche in the = hair=20 follicle bulge, providing an environment of cell growth = inhibition=20 (20).=20 The Wnt molecules are primarily expressed in dermal papilla, = separate=20 from the bulge region, and only when the bulge area is close = to the=20 dermal papilla during the early anagen phase can stem cells = be=20 activated in response to Wnt signals emanating from the = dermal=20 papilla (33).=20 Likewise, Wnt signaling can also promote HSC proliferation = (34),=20 but which Wnt signal, if any, is expressed in the = osteoblastic or=20 vascular niche is thus far unknown.

In intestine, intestinal stem cells (ISC) are located between=20 differentiated Paneth cells and proliferating progenitor = cells=20 (35=9637).=20 Wnt signaling is known to promote crypt cell proliferation = (38);=20 however, sFRP5, a Wnt inhibitor, has also been shown to be=20 predominantly expressed in ISCs (39).=20 In contrast, active Wnt signaling is widely seen in the = proliferating=20 crypt cells (37,=20 38).=20 Overall, Wnt signaling is most likely only transiently active = in the=20 ISC niche (25).=20

On the other hand, signals, including transforming growth = factor-=DF=20 (TGF-=DF) and BMP, provide proliferation-inhibition = signals to=20 inhibit stem cell activation and proliferation (37,=20 40,=20 41),=20 but whether they are expressed in each or all of the niches = described=20 above is not clear, apart from BMP4, which has been shown to = be=20 expressed in the intestinal stem cell niche (37).=20

Wnt signaling, known to promote cell growth (42),=20 is activated when Wnt binds its receptor Frizzled and sends a = signal=20 to inhibit a negative complex formed by adenomatous polyposis = coli=20 (APC) and glycogen synthase kinase-3=DF, which controls = the=20 phosphorylation and subsequent degradation of =DF-catenin.=20 Abnormal activation of the Wnt signaling pathway causes cells = to receive a continuous signal for proliferation due to = accumulation=20 of =DF-catenin in the nuclei, thereby leading to the = development=20 of APC in intestine, hair follicle tumors in skin, and = leukemia in=20 bone marrow (14,=20 43=9645).=20

BMPs belong to the TGF-=DF super family, which in general = inhibits=20 cell growth with exceptions in some systems (40,=20 46,=20 47).=20 BMP2/BMP4 signaling is mediated by Bmpr1A or Bmpr1B (46)=20 and through Smad transcriptional factors 1, 5, or 8 together=20 with Smad4 and regulates targeted gene expression (48).=20 BMP activity can be regulated by its antagonists, such as = Noggin=20 (49).=20 In a mouse model in which BMPR1a was conditionally inactivated, = the=20 stem cell populations were expanded in hair follicle, intestine, = and=20 bone marrow, resulting in hair follicle tumors (50),=20 intestinal polyposis (37),=20 and abnormal bone growth and expansion of the HSC population, = respectively (21).=20 These observations have shown that BMP signaling mediated by = Bmpr1a=20 directly inhibits stem cell proliferation in the niches of = intestine=20 and skin and indirectly regulates hematopoietic stem cells = through=20 control of its niche. Although BMP4 is constantly expressed = in the=20 ISC niche, its antagonist Noggin is transiently expressed in = stem=20 cells of the intestines and the hair follicle bulge area (37).4=20 It has been proposed that coordination between Wnt and the=20 transiently expressed Noggin, which overrides BMP inhibition=20 signaling, is required to activate stem cells, at least in = skin and=20 intestine (25,=20 51).=20 The fact that overexpression of Noggin leads to intestinal = polyposis=20 supports this model (52).=20

In summary, the interplay between the BMP antigrowth signal = and=20 the Wnt growth-promoting signal regulates the homeostatic = balance of=20 stem cell self-renewal and ongoing regeneration. If this = balance is=20 disrupted, stem cells may proliferate without restraint, such = as when=20 loss of BMP signaling or abnormal activation of Wnt signaling = leads=20 to tumorigenesis (14,=20 37,=20 45,=20 52,=20 53).=20


3D"    Stem=20 Cell Niche: Gatekeeper of Pandora's Box =
Top
Abstract
Is Cancer a Disease...
Homeostatic Regulation of Stem...
3D"Stem Cell Niche:=20 Gatekeeper...
Link between Stem Cell...
Closing Remarks
References
 
T= he role=20 of the niche in maintaining stem cells has been shown in = several=20 systems. For example, genetic ablation of the germ line stem = cell=20 niche in flies results in loss of stem cells (54).=20 Increasing the niche size in mice leads to an increased = number of=20 hematopoietic stem cells (21),=20 and in contrast, depleting the osteoblastic lining cells = leads to=20 depletion of hematopoietic tissue (55).=20 However, recent evidence has suggested that the stem cell = niche may=20 have another important function that has thus far been=20 underestimated. That function is to prevent tumorigenesis by=20 controlling stem cell proliferation. Here, we hypothesize = that=20 deregulation of the niche leading to uncontrolled proliferation = of=20 stem cells may result in tumorigenesis (Fig.=20 1), much like opening "Pandora's box." Recently, R. = Dickson's lab=20 reported that deregulation in the mammary gland stem cell = niche=20 leads to abnormal expression of TFF3D{alpha}=20, = resulting in=20 the development of breast cancer (56),=20 and this seems to support our hypothesis.


3D"    Link=20 between Stem Cell Homing/Mobilization and Cancer Cell = Invasion/Metastasis=20
Top
Abstract
Is Cancer a Disease...
Homeostatic Regulation of Stem...
Stem Cell Niche: Gatekeeper...
3D"Link between Stem=20 Cell...
Closing Remarks
References
 
A= basic=20 function of the niche is to anchor stem cells in the = appropriate=20 microenvironment. This function is mediated by adhesion = molecules,=20 including an adherent complex composed of cadherin and = =DF-catenin. It=20 has been reported that different forms of =DF-catenin = interact with=20 different protein complexes. That is, the heterodimeric form = of=20 =DF-catenin/3D{alpha}=20-catenin=20 interacts with membrane-bound cadherin, and the monomer form=20 interacts with Tcf in nuclei, and that the phosphorylation of = the COOH terminus of =DF-catenin (by non-Wnt signals) = regulates=20 the conversion between the two forms (57).=20 It is, therefore, reasonable to propose that =DF-catenin = is=20 a key molecule bridging two states of stem cells (58):=20 the arrested state when stem cells are attached to the niche = through=20 the cadherin-=DF-catenin adhesion interaction (21,=20 59)=20 and the activated state in which =DF-catenin is = nuclearly=20 localized (31,=20 37).=20 Defining the signals that regulate the conformational change = of=20 =DF-catenin through phosphorylation of its COOH terminus to = control the=20 conversion of =DF-catenin from its membrane-bound form to the = form=20 favoring Tcf binding will provide insight into understanding = stem=20 cell activation, as the =DF-catenin/Tcf complex will turn on=20 cycle-related genes, including cyclin D1 and = c-Myc (60,=20 61).=20 The signal responsible for regulation of the =DF-catenin COOH = terminus=20 may be required to coordinate with the Wnt signal, which=20 primarily prevents =DF-catenin from degradation, to fully = activate=20 stem cells. Indeed, the fact that a mutation in E-cadherin = leads=20 to nuclearly localized =DF-catenin has been observed in = breast=20 cancer seems to support this argument (62).=20

There is a certain degree of similarity in terms of the = molecules=20 and the underlying machinery used by both normal stem cells = for=20 homing or mobilization and cancer cells for invasion and = metastasis.=20 For example, during HSC activation and mobilization, matrix=20 metalloproteinase-9 (MMP-9) is required for proteolysis of = the=20 extracellular matrix components and converting stem cell = factor from=20 a membrane-bound form into a free form, which then promotes = HSC=20 proliferation and mobilization through c-Kit receptor (63).=20 Intriguingly, the molecules of the MMP family are key = molecules=20 involved in the process of cancer cell metastasis (64).=20 Likewise, integrin is required for stem cell migration as = evidenced=20 in both hematopoietic and neural systems (65,=20 66),=20 and integrin has been reported to be associated with tumor = cell=20 migration and metastasis (67).=20 Finally, cancer cell metastasis exhibits some properties = shared by=20 stem cells, such as homing and mobilization in which SDF1 and = CXCR4=20 play essential roles (68).=20 It was recently found that SDF1 is also involved in breast = cancer=20 cell migration (69).=20 In addition, recent data support the role of the vascular = niche in=20 initiating metastasis (70).=20 Thus, molecules involved in stem cell activation and = mobilization=20 from the niche and homing to the niche are possible targets = for=20 tumorigenesis, cancer development, and metastasis.


3D"   =20 Closing Remarks
Top
Abstract
Is Cancer a Disease...
Homeostatic Regulation of Stem...
Stem Cell Niche: Gatekeeper...
Link between Stem Cell...
3D"Closing Remarks
References
 
N= ormal=20 stem cells in adult somatic tissues and cancer stem cells = share the=20 common features of self-renewal and slow cycling. Here, we = have=20 proposed another potential niche function in preventing = tumorigenesis=20 under normal physiologic conditions. The question arises as = to=20 whether or not cancer stem cells are dependent upon the = niche, as are=20 normal stem cells. This may vary with different types of = tumors or=20 cancers. In general, cancer stem cells resulting from = mutations in=20 stem/progenitor cells most likely undergo uncontrolled = proliferation.=20 We hypothesize that cancer stem cells may also arise from a=20 microenvironment with dominant growth-promoting signals = rather than=20 growth-inhibiting signals. This is supported by the fact that = certain=20 types of neuroblastoma require coordination of mutations in = both=20 Schwann cells and supportive cells (71) and, in general, = rapid=20 tumor growth requires de novo angiogenesis, in which = the=20 vascular niche provides growth-promoting signals with = enriched=20 oxygen and nutrition. In addition, stem cell mobilization = from or=20 homing to the niche uses molecular machinery similar to that=20 wrongly used by cancer cells for invasion and metastasis.=20 Exploring this process and the underlying molecular = mechanisms will=20 provide important insight into understanding cancer cell=20 metastasis and will benefit developing treatments aimed at = destroying=20 cancer stem cells without adversely affecting normal stem = cell=20 self-renewal.


3D"   =20 Acknowledgments
 
We = thank D. di Natale=20 for editorial assistance.


3D"   =20 Footnotes
 
Note: This review article is based on = our=20 presentations at the American Association for Cancer Research = 2005=20 Pathobiology of Cancer Workshop.

4 Zhang and Li, unpublished = data.

Received 11/ 4/05. Revised 1/20/05. Accepted 3/ 7/06.


3D"   =20 References
Top
Abstract
Is Cancer a Disease...
Homeostatic Regulation of Stem...
Stem Cell Niche: Gatekeeper...
Link between Stem Cell...
Closing Remarks
3D"References
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Opera = requires=0A= the Sun Java Runtime Environment .=0A= =0A= by Andrew Gregory=0A= http://www.scss.com.au/family/andrew/webdesign/xmlhttprequest/=0A= =0A= This work is licensed under the Creative Commons Attribution License. To = view a=0A= copy of this license, visit = http://creativecommons.org/licenses/by-sa/2.5/ or=0A= send a letter to Creative Commons, 559 Nathan Abbott Way, Stanford, = California=0A= 94305, USA.=0A= =0A= Attribution: Leave my name and web address in this script intact.=0A= =0A= Not Supported in Opera=0A= ----------------------=0A= * user/password authentication=0A= * responseXML data member=0A= =0A= Not Fully Supported in Opera=0A= ----------------------------=0A= * async requests=0A= * abort()=0A= * getAllResponseHeaders(), getAllResponseHeader(header)=0A= =0A= */=0A= // IE support=0A= if (window.ActiveXObject && !window.XMLHttpRequest) {=0A= window.XMLHttpRequest =3D function() {=0A= var msxmls =3D new Array(=0A= 'Msxml2.XMLHTTP.5.0',=0A= 'Msxml2.XMLHTTP.4.0',=0A= 'Msxml2.XMLHTTP.3.0',=0A= 'Msxml2.XMLHTTP',=0A= 'Microsoft.XMLHTTP');=0A= for (var i =3D 0; i < msxmls.length; i++) {=0A= try {=0A= return new ActiveXObject(msxmls[i]);=0A= } catch (e) {=0A= }=0A= }=0A= return null;=0A= };=0A= }=0A= // Gecko support=0A= /* ;-) */=0A= // Opera support=0A= if (window.opera && !window.XMLHttpRequest) {=0A= window.XMLHttpRequest =3D function() {=0A= this.readyState =3D 0; // = 0=3Duninitialized,1=3Dloading,2=3Dloaded,3=3Dinteractive,4=3Dcomplete=0A= this.status =3D 0; // HTTP status codes=0A= this.statusText =3D '';=0A= this._headers =3D [];=0A= this._aborted =3D false;=0A= this._async =3D true;=0A= this._defaultCharset =3D 'ISO-8859-1';=0A= this._getCharset =3D function() {=0A= var charset =3D _defaultCharset;=0A= var contentType =3D = this.getResponseHeader('Content-type').toUpperCase();=0A= val =3D contentType.indexOf('CHARSET=3D');=0A= if (val !=3D -1) {=0A= charset =3D contentType.substring(val);=0A= }=0A= val =3D charset.indexOf(';');=0A= if (val !=3D -1) {=0A= charset =3D charset.substring(0, val);=0A= }=0A= val =3D charset.indexOf(',');=0A= if (val !=3D -1) {=0A= charset =3D charset.substring(0, val);=0A= }=0A= return charset;=0A= };=0A= this.abort =3D function() {=0A= this._aborted =3D true;=0A= };=0A= this.getAllResponseHeaders =3D function() {=0A= return this.getAllResponseHeader('*');=0A= };=0A= this.getAllResponseHeader =3D function(header) {=0A= var ret =3D '';=0A= for (var i =3D 0; i < this._headers.length; i++) {=0A= if (header =3D=3D '*' || this._headers[i].h =3D=3D header) {=0A= ret +=3D this._headers[i].h + ': ' + this._headers[i].v + '\n';=0A= }=0A= }=0A= return ret;=0A= };=0A= this.getResponseHeader =3D function(header) {=0A= var ret =3D getAllResponseHeader(header);=0A= var i =3D ret.indexOf('\n');=0A= if (i !=3D -1) {=0A= ret =3D ret.substring(0, i);=0A= }=0A= return ret;=0A= };=0A= this.setRequestHeader =3D function(header, value) {=0A= this._headers[this._headers.length] =3D {h:header, v:value};=0A= };=0A= this.open =3D function(method, url, async, user, password) {=0A= this.method =3D method;=0A= this.url =3D url;=0A= this._async =3D true;=0A= this._aborted =3D false;=0A= this._headers =3D [];=0A= if (arguments.length >=3D 3) {=0A= this._async =3D async;=0A= }=0A= if (arguments.length > 3) {=0A= opera.postError('XMLHttpRequest.open() - user/password not = supported');=0A= }=0A= this.readyState =3D 1;=0A= if (this.onreadystatechange) {=0A= this.onreadystatechange();=0A= }=0A= };=0A= this.send =3D function(data) {=0A= if (!navigator.javaEnabled()) {=0A= alert("XMLHttpRequest.send() - Java must be installed and = enabled.");=0A= return;=0A= }=0A= if (this._async) {=0A= setTimeout(this._sendasync, 0, this, data);=0A= // this is not really asynchronous and won't execute until the = current=0A= // execution context ends=0A= } else {=0A= this._sendsync(data);=0A= }=0A= }=0A= this._sendasync =3D function(req, data) {=0A= if (!req._aborted) {=0A= req._sendsync(data);=0A= }=0A= };=0A= this._sendsync =3D function(data) {=0A= this.readyState =3D 2;=0A= if (this.onreadystatechange) {=0A= this.onreadystatechange();=0A= }=0A= // open connection=0A= var url =3D new java.net.URL(new = java.net.URL(window.location.href), this.url);=0A= var conn =3D url.openConnection();=0A= for (var i =3D 0; i < this._headers.length; i++) {=0A= conn.setRequestProperty(this._headers[i].h, this._headers[i].v);=0A= }=0A= this._headers =3D [];=0A= if (this.method =3D=3D 'POST') {=0A= // POST data=0A= conn.setDoOutput(true);=0A= var wr =3D new = java.io.OutputStreamWriter(conn.getOutputStream(), this._getCharset());=0A= wr.write(data);=0A= wr.flush();=0A= wr.close();=0A= }=0A= // read response headers=0A= // NOTE: the getHeaderField() methods always return nulls for me :(=0A= var gotContentEncoding =3D false;=0A= var gotContentLength =3D false;=0A= var gotContentType =3D false;=0A= var gotDate =3D false;=0A= var gotExpiration =3D false;=0A= var gotLastModified =3D false;=0A= for (var i =3D 0; ; i++) {=0A= var hdrName =3D conn.getHeaderFieldKey(i);=0A= var hdrValue =3D conn.getHeaderField(i);=0A= if (hdrName =3D=3D null && hdrValue =3D=3D null) {=0A= break;=0A= }=0A= if (hdrName !=3D null) {=0A= this._headers[this._headers.length] =3D {h:hdrName, = v:hdrValue};=0A= switch (hdrName.toLowerCase()) {=0A= case 'content-encoding': gotContentEncoding =3D true; break;=0A= case 'content-length' : gotContentLength =3D true; break;=0A= case 'content-type' : gotContentType =3D true; break;=0A= case 'date' : gotDate =3D true; break;=0A= case 'expires' : gotExpiration =3D true; break;=0A= case 'last-modified' : gotLastModified =3D true; break;=0A= }=0A= }=0A= }=0A= // try to fill in any missing header information=0A= var val;=0A= val =3D conn.getContentEncoding();=0A= if (val !=3D null && !gotContentEncoding) = this._headers[this._headers.length] =3D {h:'Content-encoding', v:val};=0A= val =3D conn.getContentLength();=0A= if (val !=3D -1 && !gotContentLength) = this._headers[this._headers.length] =3D {h:'Content-length', v:val};=0A= val =3D conn.getContentType();=0A= if (val !=3D null && !gotContentType) = this._headers[this._headers.length] =3D {h:'Content-type', v:val};=0A= val =3D conn.getDate();=0A= if (val !=3D 0 && !gotDate) this._headers[this._headers.length] = =3D {h:'Date', v:(new Date(val)).toUTCString()};=0A= val =3D conn.getExpiration();=0A= if (val !=3D 0 && !gotExpiration) = this._headers[this._headers.length] =3D {h:'Expires', v:(new = Date(val)).toUTCString()};=0A= val =3D conn.getLastModified();=0A= if (val !=3D 0 && !gotLastModified) = this._headers[this._headers.length] =3D {h:'Last-modified', v:(new = Date(val)).toUTCString()};=0A= // read response data=0A= var reqdata =3D '';=0A= var stream =3D conn.getInputStream();=0A= if (stream) {=0A= var reader =3D new java.io.BufferedReader(new = java.io.InputStreamReader(stream, this._getCharset()));=0A= var line;=0A= while ((line =3D reader.readLine()) !=3D null) {=0A= if (this.readyState =3D=3D 2) {=0A= this.readyState =3D 3;=0A= if (this.onreadystatechange) {=0A= this.onreadystatechange();=0A= }=0A= }=0A= reqdata +=3D line + '\n';=0A= }=0A= reader.close();=0A= this.status =3D 200;=0A= this.statusText =3D 'OK';=0A= this.responseText =3D reqdata;=0A= this.readyState =3D 4;=0A= if (this.onreadystatechange) {=0A= this.onreadystatechange();=0A= }=0A= if (this.onload) {=0A= this.onload();=0A= }=0A= } else {=0A= // error=0A= this.status =3D 404;=0A= this.statusText =3D 'Not Found';=0A= this.responseText =3D '';=0A= this.readyState =3D 4;=0A= if (this.onreadystatechange) {=0A= this.onreadystatechange();=0A= }=0A= if (this.onerror) {=0A= this.onerror();=0A= }=0A= }=0A= };=0A= };=0A= }=0A= // ActiveXObject emulation=0A= if (!window.ActiveXObject && window.XMLHttpRequest) {=0A= window.ActiveXObject =3D function(type) {=0A= switch (type.toLowerCase()) {=0A= case 'microsoft.xmlhttp':=0A= case 'msxml2.xmlhttp':=0A= case 'msxml2.xmlhttp.3.0':=0A= case 'msxml2.xmlhttp.4.0':=0A= case 'msxml2.xmlhttp.5.0':=0A= return new XMLHttpRequest();=0A= }=0A= return null;=0A= };=0A= }=0A= ------=_NextPart_000_005B_01C89190.9A597050 Content-Type: application/octet-stream Content-Transfer-Encoding: quoted-printable Content-Location: http://cancerres.aacrjournals.org/javascript/ajax/utility.js /************************************************************************= *****=0A= * javascript/ajax/utility.js=0A= *=0A= * Utility functions for working with XMLHttpRequest data.=0A= *=0A= * Copyright 2006 Board of Trustees of the Leland Stanford Junior = University.=0A= = *************************************************************************= ***/=0A= =0A= /*=0A= * Copy XML nodes into an HTMLElement. This effectively=0A= * clones XML markup which uses XHTML naming conventions=0A= * into an HTML DOM.=0A= */=0A= function copy_xml_to_html(src, dst) {=0A= if (src.nodeType =3D=3D 1) { /* Node.ELEMENT_NODE */=0A= var e =3D document.createElement(src.nodeName);=0A= for (var i =3D 0; i < src.childNodes.length; i++) {=0A= copy_xml_to_html(src.childNodes[i], e);=0A= }=0A= for (var i =3D 0; i < src.attributes.length; i++) {=0A= var n =3D src.attributes[i].name;=0A= var v =3D unescape_xml_string(src.attributes[i].value); =0A= e.setAttribute(n, v);=0A= if (n =3D=3D "class") {=0A= e.className =3D v;=0A= }=0A= else if (n =3D=3D "style") {=0A= set_css_style(v, e, "");=0A= }=0A= }=0A= dst.appendChild(e);=0A= }=0A= else if (src.nodeType =3D=3D 3) { /* Node.TEXT_NODE */=0A= dst.appendChild(document.createTextNode(src.nodeValue));=0A= }=0A= }=0A= =0A= /* =0A= * It is unclear that this is the right thing to be calling=0A= * from copy_xml_to_html, but it appears that Safari decides=0A= * to convert & to the NCR #, and then encodes that=0A= * NCR to &%26%2338;. So, I'm going to treat the DOM Attr=0A= * value as a plain string, and run our XML string input=0A= * through the decoding routine below.=0A= */=0A= function unescape_xml_string(s) {=0A= return s.replace(/'/g, "'")=0A= .replace(/'/g, "'")=0A= .replace(/"/g, "\"")=0A= .replace(/"/g, "\"")=0A= .replace(/>/g, ">")=0A= .replace(/>/g, ">")=0A= .replace(/</g, "<")=0A= .replace(/</g, "<")=0A= .replace(/&/g, "&")=0A= .replace(/&/g, "&");=0A= }=0A= =0A= /*=0A= * Parse set of CSS rules and apply them to an element.=0A= * This is quite horrifying, but I'm unable to determine=0A= * how else to handle this with IE 6. FireFox and other=0A= * sane browsers let you simply set the style attribute=0A= * or use e.style.setProperty(rule, value, priority),=0A= * IE 6 appears to have neither of these capabilities..=0A= */=0A= function set_css_style(css, e, priority) {=0A= var rules =3D css.split(";");=0A= for (var i =3D 0; i < rules.length; i++) {=0A= var nvpair =3D rules[i].split(":");=0A= if (nvpair.length =3D=3D 2) {=0A= try {=0A= var name =3D nvpair[0]; /* style attribute */=0A= var value =3D nvpair[1]; /* attribute value */=0A= =0A= /*=0A= * For each possible style attribute, set the=0A= * appropriate style property in the element.=0A= */=0A= if (name =3D=3D "background") {=0A= e.style.background =3D value;=0A= }=0A= else if (name =3D=3D "background-attachment") {=0A= e.style.backgroundAttachment =3D value;=0A= }=0A= else if (name =3D=3D "background-color") {=0A= e.style.backgroundColor =3D value;=0A= }=0A= else if (name =3D=3D "background-image") {=0A= e.style.backgroundImage =3D value;=0A= }=0A= else 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quoted-printable Content-Location: http://cancerres.aacrjournals.org/javascript/entrez/callback.js /************************************************************************= *****=0A= * javascript/entrez/callback.js=0A= *=0A= * Entrez Linking callback to populate content box.=0A= *=0A= * Copyright 2006 Board of Trustees of the Leland Stanford Junior = University.=0A= = *************************************************************************= ***/=0A= =0A= /*=0A= * Execute callback to fill content box with Entrez Linking information.=0A= */=0A= function entrez_callback(pmid, callback_url) {=0A= /*=0A= * MSIE 5.5 and below have issues with the JavaScript=0A= * used for Entrez Linking. 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path=3D"+_utcp+";"+nx+_udo;=0A= _ubd.cookie=3D"__utmb=3D"+_udh+"; path=3D"+_utcp+";"+x+_udo;=0A= _ubd.cookie=3D"__utmc=3D"+_udh+"; path=3D"+_utcp+";"+_udo;=0A= _ufns=3D1;=0A= } else if (a>=3D0 && b>=3D0 && c>=3D0) {=0A= _ubd.cookie=3D"__utmb=3D"+_udh+"; path=3D"+_utcp+";"+x+_udo;=0A= } else {=0A= if (a>=3D0) a=3D_uFixA(_ubd.cookie,";",_ust);=0A= else a=3D_udh+"."+_uu+"."+_ust+"."+_ust+"."+_ust+".1";=0A= _ubd.cookie=3D"__utma=3D"+a+"; path=3D"+_utcp+";"+nx+_udo;=0A= _ubd.cookie=3D"__utmb=3D"+_udh+"; path=3D"+_utcp+";"+x+_udo;=0A= _ubd.cookie=3D"__utmc=3D"+_udh+"; path=3D"+_utcp+";"+_udo;=0A= _ufns=3D1;=0A= }=0A= if (_ulink && xx && xx!=3D"" && xx!=3D"-") {=0A= xx=3D_uUES(xx);=0A= if (xx.indexOf(";")=3D=3D-1) _ubd.cookie=3D"__utmx=3D"+xx+"; = path=3D"+_utcp+";"+nx+_udo;=0A= }=0A= if (_ulink && v && v!=3D"" && v!=3D"-") {=0A= v=3D_uUES(v);=0A= if (v.indexOf(";")=3D=3D-1) _ubd.cookie=3D"__utmv=3D"+v+"; = path=3D"+_utcp+";"+nx+_udo;=0A= }=0A= _uInfo(page);=0A= _ufns=3D0;=0A= _ufno=3D0;=0A= if (!page || page=3D=3D"") _uff=3D1;=0A= }=0A= function _uInfo(page) {=0A= var p,s=3D"",dm=3D"",pg=3D_udl.pathname+_udl.search;=0A= if (page && page!=3D"") pg=3D_uES(page,1);=0A= _ur=3D_ubd.referrer;=0A= if (!_ur || _ur=3D=3D"") { _ur=3D"-"; }=0A= else {=0A= dm=3D_ubd.domain;=0A= if(_utcp && _utcp!=3D"/") dm+=3D_utcp;=0A= p=3D_ur.indexOf(dm);=0A= if ((p>=3D0) && (p<=3D8)) { _ur=3D"0"; }=0A= if (_ur.indexOf("[")=3D=3D0 && = _ur.lastIndexOf("]")=3D=3D(_ur.length-1)) { _ur=3D"-"; }=0A= }=0A= s+=3D"&utmn=3D"+_uu;=0A= if (_ufsc) s+=3D_uBInfo();=0A= if (_uctm) s+=3D_uCInfo();=0A= if (_utitle && _ubd.title && _ubd.title!=3D"") = s+=3D"&utmdt=3D"+_uES(_ubd.title);=0A= if (_udl.hostname && _udl.hostname!=3D"") = s+=3D"&utmhn=3D"+_uES(_udl.hostname);=0A= s+=3D"&utmr=3D"+_ur;=0A= s+=3D"&utmp=3D"+pg;=0A= if ((_userv=3D=3D0 || _userv=3D=3D2) && _uSP()) {=0A= var i=3Dnew Image(1,1);=0A= i.src=3D_ugifpath+"?"+"utmwv=3D"+_uwv+s;=0A= i.onload=3Dfunction() {_uVoid();}=0A= }=0A= if ((_userv=3D=3D1 || _userv=3D=3D2) && _uSP()) {=0A= var i2=3Dnew Image(1,1);=0A= = i2.src=3D_ugifpath2+"?"+"utmwv=3D"+_uwv+s+"&utmac=3D"+_uacct+"&utmcc=3D"+= _uGCS();=0A= i2.onload=3Dfunction() { _uVoid(); }=0A= }=0A= return;=0A= }=0A= function _uVoid() { return; }=0A= function _uCInfo() {=0A= if (!_ucto || _ucto=3D=3D"") { _ucto=3D"15768000"; 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