From: Subject: IQGAP1 Protein Specifies Amplifying Cancer Cells in Glioblastoma Multiforme -- Balenci et al. 66 (18): 9074 -- Cancer Research Date: Tue, 15 Jan 2008 14:50:14 +0100 MIME-Version: 1.0 Content-Type: multipart/related; type="text/html"; boundary="----=_NextPart_000_0000_01C85785.EFA3B790" X-MimeOLE: Produced By Microsoft MimeOLE V6.00.2900.3198 This is a multi-part message in MIME format. ------=_NextPart_000_0000_01C85785.EFA3B790 Content-Type: text/html; charset="Windows-1252" Content-Transfer-Encoding: quoted-printable Content-Location: http://cancerres.aacrjournals.org/cgi/content/full/66/18/9074 IQGAP1 Protein Specifies Amplifying Cancer Cells in = Glioblastoma Multiforme -- Balenci et al. 66 (18): 9074 -- Cancer = Research 3D"Cancer 3D"
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[Cancer Research 66, 9074-9082, September 15, = 2006]
=A9 2006=20 American=20 Association for Cancer Research

Cell, Tumor, and Stem Cell = Biology

IQGAP1 Protein Specifies Amplifying Cancer Cells in Glioblastoma = Multiforme=20

Laurent Balenci1, Ian = D.=20 Clarke2, Peter B. Dirks2, = Nicole=20 Assard1, Fran=E7ois Ducray3, = Anne=20 Jouvet3, Marie-Fran=E7oise = Belin3,=20 Jer=F4me Honnorat3 and Jacques=20 Baudier1

1 Institut National de la Sant=E9 et de la = Recherche=20 M=E9dicale EMI 0104, D=E9partement de R=E9ponse et Dynamique = Cellulaires, CEA=20 Grenoble, Grenoble, France; 2 The Arthur and Sonia Labatt = Brain Tumor=20 Research Center, The Hospital for Sick Children, Toronto, Ontario, = Canada; and=20 3 Institut National de la Sant=E9 et de la Recherche = M=E9dicale Unit=E9=20 433, Institut F=E9d=E9ratif des Neurosciences de Lyon, Facult=E9 = Laennec, Lyon, France=20

Requests for reprints: Jacques Baudier, = Institut=20 National de la Sant=E9 et de la Recherche M=E9dicale EMI 0104/TS-DRDC, = CEA Grenoble,=20 17 rue des Martyrs, 38054 Grenoble Cedex 9, France. Phone: = 33-4-38-78-43-28;=20 Fax: 33-4-38-78-50-58; E-mail: jbaudier{at}cea.fr .


3D"   =20 Abstract
Top
3D"Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
T= he=20 accurate identification and thorough characterization of = tumorigenic=20 cells in glioblastomas are essential to enhance our = understanding of=20 their malignant behavior and for the design of strategies = that target=20 this important cell population. We report here that, in rat = brain,=20 the scaffolding protein IQGAP1 is a marker of brain=20 nestin+ amplifying neural progenitor cells. In a = rat model=20 of glioma, IQGAP1 also characterizes a subpopulation of=20 nestin+ amplifying tumor cells in glioblastoma-like = tumors=20 but not in tumors with oligodendroglioma features. We next = confirmed=20 that IQGAP1 represents a new marker that may help to = discriminate=20 human glioblastoma from oligodendrogliomas. In human = glioblastoma=20 exclusively, IQGAP1 specifies a subpopulation of amplifying=20 nestin+ cancer cells. Neoplastic IQGAP1+ = cells from=20 glioblastoma can be expanded in culture and possess all the=20 characteristics of cancer stem-like progenitors. The = similarities=20 between amplifying neural progenitors and glioblastoma = amplifying=20 cancer cells may have significant implications for = understanding the=20 biology of glioblastoma. (Cancer Res 2006; 66(18): = 9074-82)=20


3D"   =20 Introduction
Top
Abstract
3D"Introduction
Materials and Methods
Results
Discussion
References
 
G= liomas=20 are the most common primary malignant brain tumors and are = classified=20 into two major groups: oligodendrogliomas and astrocytomas, = including=20 glioblastomas. It is implicit in such definitions that these=20 neoplasms originate from either oligodendrocytes or = astrocytes. There=20 is, however, evidence that these brain tumors can also result = from=20 the transformation of undifferentiated glial progenitor cells = or=20 cells with stem cell characteristics (1=963).=20 The first indication that some brain tumors can arise from=20 transformation of neural stem cells or neural progenitors = comes from=20 mouse models, in which combined expression of Ras and Akt = oncogenes=20 under the control of the nestin promoter induced glioblastoma = formation (4).=20 In adult rodent brain, nestin is considered as a marker for = both=20 neural stem cell and neural progenitors (5,=20 6).=20 The identification of transformed neural stem cell=96like = cells in=20 cultures derived from human medulloblastomas and glioblastoma = tumors=20 has brought further support to the hypothesis that these = tumors=20 contain cancer stem cells that may participate in brain = tumorigenesis=20 (7=9611).=20 More recently, a population of brain tumor-initiating cells, = with=20 characteristics of stem cells = (nestin+/CD133+),=20 has been purified from human gliomas (8).=20 In the more aggressive glioblastomas, this population represents = up=20 to 30% of the total tumor cell population (8).=20 The neural stem cell concept for the origin of gliomas sheds = light on=20 their heterogeneity but also raises questions as to = understand=20 the high malignancy of some of these tumors, such as=20 glioblastoma (3).=20 A model has been proposed where cancer stem cells generate=20 transformed progenitor cells that divide rapidly but are = incapable=20 of complete differentiation in vivo (3).=20 The accurate identification and thorough characterization of = the=20 tumor amplifying progenitor cells is now essential to enhance = our=20 understanding of malignant gliomas. To reach this goal, it = will be=20 necessary to identify more definitive markers of these cells. = Moreover, if these markers have recognized specific = functions, they=20 might help to develop new therapeutic strategies for more = effective=20 cancer treatments.

We first report here that the IQGAP1 protein is a reliable = marker=20 of nestin+ amplifying neural progenitors in rat brain.=20 Mammalian IQGAP1 is considered to be a scaffolding protein at = the=20 crossroads of several signaling pathways involved in the = control of=20 cell adhesion (12,=20 13),=20 polarization (14,=20 15),=20 and directional migration (15,=20 16).=20 A recent study has identified IQGAP1 as a key component of = neuronal=20 motility signal transduction (17).=20 Several studies have also implicated IQGAP1 in epithelial=20 carcinogenesis and metastasis (18).=20 Consistent with its possible implication in tumorigenesis, = IQGAP1 is=20 highly abundant in rat and human glioma cell lines (19).=20 To investigate possible regulation of IQGAP1 during=20 neurocarcinogenesis, we analyzed IQGAP1 expression in a rat = model of=20 ethylnitrosourea (ENU)-induced glioma (20).=20 We show that IQGAP1 specifies a subpopulation of amplifying=20 tumor cells in glioblastoma-like tumors but not in tumors = with=20 oligodendroglioma features. We next confirmed in human glioma = the=20 specific expression of IQGAP1 in glioblastoma amplifying = cancer=20 cells. Our results may have considerable implications for = further=20 understanding the biology of these invasive tumors and the=20 development of specific and more effective therapies. =


3D"   =20 Materials and Methods
Top
Abstract
Introduction
3D"Materials and = Methods
Results
Discussion
References
 
<= B>Antibodies.=20 The following primary antibodies were used: IQGAP1 (H-109; = rabbit=20 polyclonal IgG, Santa Cruz Biotechnology, Inc., Tebu-bio, = France),=20 nestin (mouse monoclonal IgG, clone Rat-401, Developmental = Studies=20 Hybridoma Bank, Iowa City, IA), specific human nestin (mouse=20 monoclonal, Chemicon International, Inc., Euromedex, France), = NG2=20 (mouse monoclonal, Upstate Laboratories, Upstate, Euromedex, = France),=20 Olig-2 (rabbit polyclonal, generous gift from Dr. H. = Chneiweiss,=20 INSERM U114, Coll=E8ge de France, Paris, France), GFAP (mouse = monoclonal IgG, Chemicon; chicken polyclonal, Abcam, France; = rabbit=20 polyclonal IgG, DAKO Cytomation, S.A, France), PECAM (CD31; = mouse=20 monoclonal, BD PharMingen, BD Biosciences, France), specific = human=20 PECAM (CD31; mouse monoclonal, DAKO), Ki-67 (mouse monoclonal = IgG,=20 Novocastra Laboratories, Ltd., AbCys, S.A, France), specific = human=20 Ki-67 (rabbit polyclonal, Zymed Laboratories, Inc.,=20 Clinisciences, France), =DFIII-tubulin (Tuj-1; rabbit = polyclonal,=20 Eurogentec, France), =DF-tubulin (mouse monoclonal, a gift = from=20 Dr. D. Job, INSERM U366, Laboratoire du Cytosquelette, = Grenoble,=20 France), and CD133/1 and CD133/2 (mouse monoclonal, Miltenyi=20 Biotec, France). Secondary anti-mouse and anti-rat antibodies = conjugated to cyanin 3 or cyanin 5 were from Jackson = ImmunoResearch=20 Laboratories (Interchim, France). Secondary anti-mouse and = anti-rat=20 antibodies conjugated to Alexa Fluor 488 were from Molecular=20 Probes, Inc., (Invitrogen, France). Secondary anti-chicken = polyclonal=20 IgY (ab6569) was from Abcam.

Transplacental administration of ENU. All procedures on = animals=20 were approved by Institut National de la Sant=E9 et de = la=20 Recherche M=E9dicale in compliance with European and French = law. OFA=20 Sprague-Dawley strain adult rats were provided by Charles = River=20 Laboratories (France). Pregnant rats were injected i.v. via = tail vein=20 with 60 mg/kg ENU (Sigma-Aldrich, France) at gestational day = 19 (20).=20

Human tumors. Tumor samples were obtained during surgery = from=20 patients of the Neurological Hospital of Lyon (Lyon, France). = Inform consent was obtained for all patients before the = surgery=20 as approved by the Research Ethics Board at the Hospices = Civils=20 de Lyon (Lyon, France). All patients had surgery for the = first=20 time and never received chemotherapy or radiotherapy. Samples = were collected immediately after surgical resection, snap = frozen=20 in liquid nitrogen, and stored at =96196=B0C in liquid = nitrogen=20 (NeuroBioTec Banques, Biological Resources Center of Hospices = Civils=20 de Lyon). A sample of glioblastoma 280, which was used for = sphere=20 culture, was progressively frozen in RPMI 1640/20% FCS/10% = DMSO and=20 then stored at =96196=B0C in liquid nitrogen before to be = used in=20 culture. Hemalin phloxine saffron (HPS)=96stained slide of = all frozen=20 samples was reviewed by a neuropathologist (A.J.) and graded = with the=20 WHO grading classification to confirm the diagnosis and = exclude=20 samples without typical aspects of the tumor. All samples = containing=20 significant regions of normal brain (>10%) and/or = excessively=20 large amounts of necrotic material were excluded. Clinical=20 presentation of all patients was reviewed by physicians (F.D. = and=20 J.H.) to select only patients with typical clinical and=20 radiological presentation of glioblastomas, low-grade=20 oligodendrogliomas, or anaplastic oligodendrogliomas. Using = all these=20 clinical and histologic criteria, nine glioblastomas (samples = no.=20 280, 410, 431, 492, 581, 532, 596, 658, and 733) and nine=20 oligodendrogliomas (grade 2 WHO oligodendroglioma samples no. = 344,=20 409, 512, 559, and 592; grade 3 WHO oligodendroglioma samples = no.=20 450, 552, 701, and 756) were selected.

Immunohistochemistry. Three- to 8-month-old animals were = deeply=20 anesthetized and killed by transcardial perfusion of saline=20 solution (150 mmol/L NaCl) followed by 4% paraformaldehyde.=20 After 24 hours in 4% paraformaldehyde, brains were = cryopreserved=20 and 20-=B5m cryostat (Leica CM 3000 Camera, AG, Germany) = sections=20 were cut. Cryopreserved human biopsies were cut into 20-=B5m = cryostat=20 sections and postfixed with 4% paraformaldehyde. Cryosections = were=20 permeabilized in TBS containing 0.2% Triton X-100 and blocked = in 5%=20 normal goat serum-TBS (NGS-TBS). After incubation with = primary=20 antibodies in NGS-TBS overnight at 4=B0C, sections were = washed in TBS=20 and stained with the appropriate secondary antibodies. = Sections were=20 counterstained with nuclear marker Hoechst 33258 (1 =B5g/mL). = Images=20 were obtained with a Carl Zeiss, AG, Germany (Axiovert 200 M) = microscope and with Leica (TCS SP2) confocal microscope. =

Immunocytochemistry. Cells were fixed with 4% = paraformaldehyde=20 in PBS and permeabilized with 0.2% Triton X-100. After = incubation=20 with primary antibodies in NGS-TBS overnight at 4=B0C, cells = were=20 washed in TBS and stained with the appropriate secondary = antibodies.=20 For CD133 immunostaining, neurospheres were fixed and = partially=20 permeabilized with 4% paraformaldehyde.

Western blotting. Cultured neurospheres and postsurgical = human=20 glioma samples were lysed in SDS sample buffer. Proteins were = run on 6% SDS-PAGE gel and transferred to a nitrocellulose = membrane.=20 Immunoblotting was done with the different antibodies = described=20 above and revealed with adequate secondary antibodies coupled = to peroxidase. Blots were revealed by chemiluminescence = according=20 to the manufacturer's instructions (enhanced = chemiluminescence,=20 Amersham Biosciences, GE Healthcare, France). All Western = blot=20 analyses were done in duplicates.

Rat neurosphere culture. Three-month-old rat was killed by=20 decapitation. Brains were removed and placed in PBS and the=20 ventricular walls were dissected, transferred in dissociation = medium=20 containing trypsin (5,000 units; Sigma), 0.67 mg/mL = hyaluronidase=20 (2,000 units/mg; Sigma), and 0.2 mg/mL kynurenic acid = (Sigma),=20 and kept 30 minutes in incubator (37=B0C, 5% CO2). = Tissues=20 were washed in DMEM with 20% fetal bovine serum (FBS) to=20 inactivate the enzyme activity and then carefully triturated = with a=20 Pasteur glass pipette. After homogenization, cells were=20 centrifuged and resuspended in chemically defined medium:=20 proliferation neurosphere medium (DMEM/F12/B27complement/0.1% = bovine=20 serum albumin) supplemented with 20 ng/mL epidermal growth=20 factor (EGF) and 20 ng/mL basic fibroblast growth factor = (bFGF;=20 ref. 21).=20

Primary human tumor sphere culture. Human tumor sample=20 corresponding to glioblastoma 280 was intensively washed in = growth=20 factor serum-free neural stem cell medium (9)=20 acutely dissociated in trypsin/EDTA solution. After = filtration,=20 primary tumor cells were cultivated in noncoated bacterial = dishes in=20 DMEM/F12 medium containing B27 complement and 20 ng/mL of = both EGF=20 and bFGF and leukemia inhibitory factor (1,000 units; = Chemicon).=20 For differentiation experiments, neurospheres were plated = onto=20 polylysine-coated (Sigma) glass coverslips in a defined = medium=20 containing DMEM/F12/B27 supplemented with either 3% FBS or in = 48-hour=20 starved conditioned medium of EaHY endothelial cell = line.

Intracranial cell transplantation into nonobese = diabetic-severe=20 combined immunodeficient mice. Purified CD133+ = cells from=20 a human glioblastoma were injected stereotactically into=20 immunodepressive nonobese diabetic-severe combined = immunodeficient=20 (NOD-SCID) mouse frontal cortex as described previously (8).=20 Two months after cell injection, mouse brains were embedded = in=20 paraffin. Paraffin-embedded, 5-=B5m formalin-fixed tissue = sections=20 were mounted on microscope slides. Tissue sections were then=20 treated as described previously (8).=20


3D"   =20 Results
Top
Abstract
Introduction
Materials and Methods
3D"Results
Discussion
References
 
<= B>IQGAP1=20 is expressed by amplifying neural progenitors in the adult = rat=20 brain. Affinity-purified antibodies against an = NH2-terminal=20 epitope that is conserved in rodent and human protein were = used=20 to probe IQGAP1 protein in adult rat brain. The specificity = of=20 these antibodies was first shown by Western blot and indirect=20 immunofluorescence analysis using mouse brain derived from = wild-type=20 and iqgap1=96/=96 animals (data provided to = reviewers=20 for examination). In adult rat brain extracts, IQGAP1 = antibodies=20 recognize a single protein band with the expected molecular=20 weight of IQGAP1 (Mr 180 kDa; Fig.=20 1A, lane 1 ). By immunohistochemistry analyses on = rat=20 brain sections, we determined IQGAP1 immunoreactivity in = endothelial=20 cells, in the epithelial ependymal cells lining the lateral=20 ventricles, and in neural progenitor cells of the germinal = anterior=20 subventricular zone (aSVZ) and of the rostral migratory = stream (RMS;=20 Fig.=20 1B and C). In the aSVZ, IQGAP1 is = associated with=20 clusters of neural progenitor cells coimmunostained with = nestin=20 marker (Fig.=20 1B, a and b). These IQGAP1+ cells were = stained by a mitotic nuclear marker antigen Ki-67 (Fig.=20 1B, c and d), suggesting that they = correspond to=20 amplifying neural progenitors. In the RMS, IQGAP1 persists in = proliferating neural progenitors, which are closely = associated with=20 blood vessels (Fig.=20 1C, a-c).



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  		Figure 1. IQGAP1 is = expressed in=20 amplifying neural progenitor cells in adult rat brain. = A,=20 Western blot analysis of total adult rat brain extract = (lane=20 1) and of neurospheres derived from adult rat SVZ = (lane=20 2) with anti-IQGAP1, anti-nestin, anti-GFAP, or = anti-=DF-tubulin=20 (tub.). B, confocal microscope analysis of = coronal rat=20 brain section showing the aSVZ double immunostained with = IQGAP1=20 antibodies (a and c) and either nestin = (b) or=20 Ki-67 (d) antibody. LV, lateral ventricle; = CPu,=20 caudate nucleus. Bar, 20 =B5m. C, optical = microscope=20 analysis of saggital section of rat brain RMS triple = immunostained=20 with Hoechst for DNA (a), IQGAP1 antibodies = (b), and=20 Ki-67 antibody (c). BV, blood vessel. = Bar, 20=20 =B5m. D, neurospheres derived from adult rat SVZ = grown in the=20 presence of EGF and FGF were double labeled with IQGAP1 = (a)=20 and nestin (b) antibodies. Bar, 20 =B5m. =

 = ;
Amplifying=20 neural progenitors have been isolated from adult rat SVZ and = grown as=20 neurospheres as previously described for mice neural = progenitors (21).=20 Western blot (Fig.=20 1A, lane 2) and indirect immunofluorescence (Fig.=20 1D) on neurospheres confirmed the coexpression of = IQGAP1=20 and nestin in neural progenitors. The glial marker GFAP is = not=20 detected in neurospheres (Fig.=20 1A, lane 2), whereas the protein is highly = abundant in=20 total brain extracts (Fig.=20 1A, lane 1).

IQGAP1 specifies a population of nestin+ tumor cells in = a=20 rat model of glioblastoma-like tumor. In differentiated = cells=20 of the adult rat brain, IQGAP1 immunoreactivity is below the=20 detection limit. However, IQGAP1 protein is highly abundant = in rat=20 and human cell lines derived from glioma (19).=20 We therefore investigated possible regulation of IQGAP1 = expression=20 during neurocarcinogenesis.

In the rat, a single transplacental injection ENU into pregnant=20 female rat at E19 induces the development of brain tumors in=20 virtually 100% of offspring after several months (20).=20 Many animals developed more than one intraparenchymal tumors. = Three months after injection, 25 intraparenchymal tumors in = 10=20 rats were examined for their histologic and immunophenotypic=20 characteristics. Immunohistochemical characterizations = included=20 expression of the astrocyte marker (GFAP), the = oligodendrocyte=20 progenitor markers (Olig-2/NG2), and the neural progenitor = markers=20 (nestin and IQGAP1). Two types of tumors have been = distinguished=20 based on these criteria. Representative results are shown in = Figs.=20 2 and 3=20 .



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  		Figure 2. = Immunohistochemical=20 characterization of rat oligodendroglioma-like tumors.=20 Representative oligodendroglioma-like tumor in the angle of = the=20 lateral ventricle between the corpus callosum and the = caudate=20 nucleus from a 90-day-old rat exposed to ENU and double=20 immunostained with either Olig-2 (A) or NG2 = (B)=20 antibodies or with IQGAP1 (C) and GFAP (D) = antibodies.=20 Bar, 200 =B5m. =

 = ;


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  		Figure 3. = Immunohistochemical=20 characterization of rat glioblastoma-like tumors. = Representative=20 glioblastoma-like tumor in the cortex above the corpus = callosum from=20 a 90-day-old rat. A and B, low-power view = section=20 immunostained with IQGAP1 (green, A and B) and = GFAP=20 (red, B) antibodies shows clusters of = IQGAP1+=20 cells surrounded by GFAP+ astrocytes. Dashed = line,=20 tumor is outlined. Bar, 200 =B5m. C to = E, double=20 immunostaining with IQGAP1 and nestin antibodies shows that = clusters=20 of IQGAP1+ cells (green, C and E) = express=20 nestin (red, D and E). Bar, 20 =B5m. = F to=20 H, double immunostaining with anti-GFAP (green, = f and=20 h) and anti-Ki-67 (red, G and H) = antibodies=20 shows that tumor cells labeled with Ki-67 are not = GFAP+.=20 Bar, 50 =B5m. I to L, cluster of=20 IQGAP1+ cells stains with Hoechst for DNA = (I) and=20 double immunostained with anti-IQGAP1 (J and = L) and=20 anti-Ki-67 (K and L) antibodies shows that = tumor cells=20 labeled with Ki-67 correspond to IQGAP1+ cells.=20 Bar, 50 =B5m. =

 = ;
Nineteen=20 primitive hyperplasic lesions examined have histologic=20 characteristics that resemble human oligodendroglioma. Figure=20 2 shows a representative image of such hyperplasic lesion = located in the angle of the lateral ventricle between the = corpus=20 callosum and the caudate nucleus. Histologically, these = tumors show=20 moderate cellularity with relatively monomorphous round = nuclei and=20 an arborized capillary network. As reported for human=20 oligodendrogliomas (22),=20 the majority of tumor cells have a uniform phenotype characterized = by=20 intense immunoreactivities for the oligodendrocyte precursor = markers,=20 including the nuclear transcription factor Olig-2 and the = cell=20 surface NG2 proteoglycan (Fig.=20 2, A and B) and the platelet-derived growth = factor-3D{alpha} receptor (data not shown). Within these tumors, = IQGAP1=20 immunoreactivity is exclusively confined to the capillary = network (Fig.=20 2, c). A costaining with the endothelial marker = PECAM=20 confirmed the restriction of IQGAP1 in oligodendroglioma-like = endothelial cells (Supplementary Fig. S1). These tumors also=20 incorporate reactive astrocytes identified based on their = morphology=20 and immunoreactivity for GFAP marker (Fig.=20 2, d). Tumor cells, as well as reactive astrocytes, are=20 not stained with nestin antibodies, and only very few cells=20 express the proliferation-associated Ki-67 antigen (data not=20 shown). Low mitotic index is also a feature of human=20 oligodendroglioma.

The second type of parenchymal tumor is histologically more=20 heterogeneous and reveals an apparent complexity of = phenotypes=20 that closely resembled human glioblastoma. These tumors are=20 characterized by clusters of IQGAP1+ cells surrounded = by=20 GFAP+ cells (Fig.=20 3, a and b). The IQGAP1+ cells are=20 coimmunostained with nestin (Fig.=20 3, c-e). The tumor GFAP+ cells have mixed=20 phenotypes depending on their localization within the tumor=20 bulk. The GFAP+ astrocyte population, which unsheathed=20 clusters of IQGAP1+/nestin+ cells, can = be=20 colabeled with nestin. In contrast, GFAP+ = astrocytes,=20 which accumulate to the periphery of the tumors, are=20 nestin=96 (data not shown). These nestin=96 = astrocytes=20 are likely associated with reactive gliosis that accompanies=20 tumor development. The cellular heterogeneity of the tumors = is=20 also illustrated by the presence of many tumor cells with = strong NG2=20 immunoreactivity (data not shown). However, in contrast to=20 oligodendroglioma-like tumors, the NG2+ tumor cells are = totally=20 devoid of nuclear Olig-2 immunoreactivity (data not shown). = We=20 noted a large number of proliferating Ki-67+ cells in = these=20 tumors in agreement with a malignant grade. Most of the=20 Ki-67+ cells form clusters unsheathed within = astrocyte=20 processes (Fig.=20 3, f-h). Double immunostaining with Ki-67 and = IQGAP1=20 antibodies shows that most of the Ki-67+ cells are = IQGAP1+ (Fig.=20 3, i-l), indicating that IQGAP1+ cells = are part=20 of the proliferating component of the tumor. Hoechst staining = does=20 not reveal fragmented nuclei, confirming that = Ki-67+ cells=20 are not undergoing apoptosis (Fig.=20 3, i).

IQGAP1 expression identifies tumor amplifying cells in human=20 glioblastoma. Having identified IQGAP1 as a specific = marker=20 of amplifying tumor cells in a rat model of glioblastoma, we=20 next investigated whether IQGAP1 might also help to = discriminate=20 human glioblastoma from oligodendroglioma. We first compared=20 the expression of IQGAP1 and nestin in nine human = glioblastoma=20 and nine human oligodendroglioma (grades 2 and 3) by Western=20 blot (Fig.=20 4A ). Results show that nestin is highly expressed = in=20 tumors classified as glioblastoma and almost undetectable in=20 oligodendroglioma with low or anaplastic features. Western = blot=20 analysis also reveals a correlation between nestin expression = and=20 IQGAP1 content in all glioblastoma extracts. Significant = nestin=20 expression was observed only in one oligodendroglioma = (patient 756).=20 Interestingly, this tumor had characteristics of glioblastoma = in some=20 regions. In contrast, the astrocyte marker GFAP does not = discriminate=20 glioblastoma from oligodendroglioma.



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  		Figure 4. = Immunohistochemical=20 characterization of human glioma. A, samples of human = brain=20 tumors, representing grade 2 or 3 oligodendroglioma = (O2 and=20 O3) and glioblastoma (GBM), were analyzed by = Western=20 blot for =DF-tubulin, GFAP, nestin, and IQGAP1 content. = B,=20 triple immunofluorescence analysis of low-grade = oligodendroglioma=20 (patient 559; a-d), high-grade oligodendroglioma = (patient=20 552; e-h), and glioblastoma (patient 596; i-l) = stained=20 with PECAM antibodies for endothelial cells (a, e, = and=20 i), GFAP (b, f, and j), and IQGAP1 = (c,=20 g, and k). Bar, 40 =B5m. =

 = ;
Triple=20 indirect immunofluorescence analysis with IQGAP1, GFAP, and = the=20 endothelial marker PECAM (Fig.=20 4B) reveals that, within low-grade = oligodendroglioma (Fig.=20 4B, a-d) and in anaplastic oligodendroglioma = characterized=20 by higher vascular development (Fig.=20 4B, e-h), IQGAP1 immunoreactivity is exclusively = associated=20 with endothelial cells. This contrasts with glioblastoma, = where=20 IQGAP1 immunoreactivity is present both in endothelial cells=20 and also in a cell population that is not stained with GFAP = (Fig.=20 4B, i-l). In all glioblastoma, the=20 IQGAP1+/GFAP=96 cells are = preferentially located=20 around blood vessels.

Based on these observations, we did a systematic = characterization=20 of the IQGAP1+/GFAP=96 cells in human = glioblastoma=20 biopsies. Representative results obtained with glioblastoma = sample=20 280 are shown.

HPS coloration on tumor sections shows histologic features of = a=20 human glioblastoma (Supplementary Fig. S2a). A GFAP staining = done on=20 the same tumor sample shows that certain tumor cell subtypes = are not=20 positive for this astrocyte marker showing the cell = heterogeneity in=20 human glioblastoma (Supplementary Fig. S2b). We next used = indirect=20 immunofluorescence to refine the immunologic phenotype of the = different tumor cell populations (Fig.=20 5, A-I ). Triple immunostaining with GFAP, nestin, and=20 IQGAP1 reveals clusters of cells coexpressing IQGAP1 and = nestin=20 surrounded by GFAP+ cells (Fig.=20 5, A-C). The GFAP+ tumor cells, which = surround=20 the IQGAP1+/nestin+ clusters, remain heavily=20 stained with nestin (Fig.=20 5, A and B). At higher magnification, the=20 IQGAP1+/nestin+ clusters show a clear = colocalization=20 of IQGAP1 and nestin (Fig.=20 5, D-F). Triple immunostaining with IQGAP1, GFAP, = and the=20 endothelial marker PECAM confirms that the IQGAP+ = cells=20 accumulate around blood vessels (Fig.=20 5, G-I). On serial sections of this human = glioblastoma=20 sample, we also analyzed the proliferation status of the = different=20 tumor cell populations (Fig.=20 5, J-R). Low magnification observation of the = tumor double=20 immunostained with GFAP and Ki-67 clearly shows that the = majority of=20 proliferating cells (Ki-67+) are located within = clusters=20 surrounded by GFAP+ cells (Fig.=20 5, J-L). Triple immunostaining with GFAP, nestin, = and=20 Ki-67 constantly revealed that the clusters of = Ki-67+=20 cells correspond to nestin+/GFAP=96 = cells (Fig.=20 5, M-O). It has not been possible to do colabeling = of=20 Ki-67 with IQGAP1 due to the rabbit origin of the two antibodies.=20 Nevertheless, taking into account that clusters of=20 nestin+/GFAP=96 cells are = IQGAP1+ (Fig.=20 5, D-F) and that clusters of = nestin+/GFAP=96=20 cells are Ki-67+ (Fig.=20 5, M-O), we can logically conclude that=20 Ki-67+/nestin+/GFAP=96 cells = correspond to=20 IQGAP1+ tumor cells. There are some=20 nestin+/GFAP+ cells present within the = tumor=20 mass that are also Ki-67+ (Fig.=20 5, P-R). These cells may correspond to tumor cells = that=20 have acquired more differentiated phenotype but still retain = the=20 capacity to proliferate.



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  		Figure 5. IQGAP1 = expression=20 specifies tumor amplifying cells in human glioblastoma. = Human=20 glioblastoma (patient 280) sections were analyzed by = indirect=20 immunofluorescence and confocal microscopy. A to = C,=20 triple indirect immunofluorescence analysis with anti-GFAP=20 (blue), anti-nestin (red), and anti-IQGAP1=20 (green) antibodies shows that=20 nestin+/IQGAP1+ cells form clusters = surrounded=20 by GFAP+/nestin+ cells. Bar, 80 = =B5m.=20 D to F, higher magnification of the=20 nestin+/IQGAP1+ clusters shows overlap = between=20 the two markers. Bar, 40 =B5m. G to I, = triple=20 immunostaining with anti-GFAP (blue), anti-IQGAP1=20 (green), and anti-PECAM (red) antibodies shows = that=20 IQGAP1+ cells form perivascular niches surrounded = by=20 GFAP+ cells. Bar, 40 =B5m. J to = L,=20 double immunostaining with anti-GFAP and anti-Ki-67 = antibodies shows=20 that cells with the highest mitotic index are located within = clusters surrounded by GFAP+ cells. Bar, = 80 =B5m.=20 M to O, higher magnification of a cluster of=20 nestin+/GFAP=96 cells triple = immunostained with=20 anti-GFAP (blue), anti-nestin (red), and = anti-Ki-67=20 (green) antibodies shows that=20 nestin+/GFAP=96 cells actively = proliferate.=20 Bar, 20 =B5m. P to R, triple = immunostaining with=20 anti-GFAP (blue), anti-nestin (red), and = anti-Ki-67=20 (green) antibodies shows that some cells that form = the tumor=20 mass and that express both nestin and GFAP are also able to=20 proliferate. Bar, 20 =B5m. =

 = ;
IQGAP1+/nestin+=20 cells derived from glioblastoma have in vitro and = in=20 vivo characteristics of amplifying cancer progenitor = cells.=20 To confirm that the = IQGAP1+/nestin+/GFAP=96=20 cells present in human glioblastoma represent the tumor=20 amplifying cells, we produced neurospheres from postsurgery = specimens=20 of glioblastoma 280 as described in Materials and Methods.=20 Western blot analysis revealed that IQGAP1 is highly = expressed in=20 the total tumor extract (Fig.=20 6A, lane 1 ) and in the corresponding cancerous=20 neurospheres (Fig.=20 6A, lane 2). These cancerous neurospheres do not = express=20 GFAP, whereas the protein is present in the original total = tumor=20 extract (Fig.=20 6A, lanes 1 and 2). Two recognized marker = of=20 tumorigenic glioblastoma stem-like progenitors were then = chosen to=20 characterize the expanded spheres: nestin and CD133 (8,=20 11).=20 Double indirect immunofluorescence reveals that the=20 IQGAP1+ cells within neurospheres express both nestin = and=20 CD133 (Fig.=20 6B and C). The intensity of staining between = IQGAP1=20 and nestin may vary among cells. These differences might = either=20 reflect subtle heterogeneity of neurosphere cells or are due = to=20 a difference in antigen accessibility. The neurospheres can = be=20 dissociated in a single cell and they are able to reform a = secondary=20 neurospheres for a long time, confirming their self-renewal = potency.=20 These cells have been expanded for >30 passages with an = average=20 doubling time estimated to 3 days. Moreover, the cell=20 immunophenotypes remained constant throughout passages.



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  		Figure 6. = IQGAP1+ cells=20 derived from glioblastoma have in vitro and in = vivo=20 characteristics of amplifying cancer cells. A, sample = of=20 human glioblastoma (280; lane 1) and corresponding=20 neurospheres (lane 2) was analyzed by Western blot = for GFAP,=20 IQGAP1, and =DF-tubulin content. B, 280 = glioblastoma-derived=20 neurospheres grown in the presence of EGF and FGF were = double=20 labeled with IQGAP1 (a) and nestin (b) = antibodies.=20 Bar, 20 =B5m. C, 280 glioblastoma-derived = neurospheres=20 grown in the presence of EGF and FGF were double labeled = with IQGAP1=20 (a) and CD133 (b) antibodies. Bar, 20 = =B5m.=20 D, immunohistochemical characterization of human = glioblastoma=20 xenograft. a and b, section of mouse = xenografted tumor=20 derived from human CD133+ glioblastoma tumor = cells was=20 stained for DNA with Hoechst (a) and immunostained = with=20 IQGAP1 antibodies (b). Dashed line, tumor is = outlined.=20 Bar, 200 =B5m. c and d, xenograft was = double=20 labeled with IQGAP1 (c) and CD133 (d) = antibodies.=20 Bar, 20 =B5m. =

 = ;
A=20 property of tumorigenic glioblastoma stem-like progenitors = grown as=20 neurospheres is their multipotency (9,=20 11).=20 To examine the in vitro multipotency of the 280=20 glioblastoma-derived neurospheres, cells were cultured in = different=20 culture conditions. Neurospheres were firstly plated onto=20 polylysine-coated coverslips in a low serum-containing = medium.=20 Results show that cells spread out from the spheres and = differentiate=20 down astrocyte lineage, which characterizes the original = tumor=20 phenotype. Most of the cells express GFAP, and many of them = coexpress=20 nestin and still proliferate as revealed by Ki-67 staining=20 (Supplementary Fig. S3A). Only rare cells express the = neuronal marker=20 Tuj-1 (data not shown). To analyze the neurogenic potential = of the=20 glioblastoma amplifying cancer cells, we plated neurospheres = onto=20 polylysine-coated slides in conditioned medium of endothelial = cells.=20 Enhancement of neuron production from multipotent neural = progenitors=20 by factors secreted by endothelial cells has been previously=20 reported (23).=20 In this culture condition, after 4 days, most of the = glioblastoma-derived=20 cells express the neuronal marker Tuj-1 (Supplementary Fig.=20 S3B). As observed by others (9),=20 a fraction of cells were colabeled with both neuronal and = glial=20 markers. This abnormal type of cells likely reflects aberrant = differentiation program in tumor neural progenitors. =

CD133+ cells can be purified from human glioblastoma, and = as=20 few as 100 CD133+ cells can produce a tumor when = injected=20 into the brain of NOD-SCID mouse (8).=20 Analysis of IQGAP1 immunoreactivity in the xenograft at an = early=20 stage of the neoplastic process reveals that most of the = amplifying=20 tumor cells are heavily immunostained with IQGAP1 antibodies = (Fig.=20 6D, a and b). Double immunofluorescence = staining=20 reveals that the IQGAP1+ xenograft tumor cells do = also=20 express CD133 immunoreactivity (Fig.=20 6D, c and d), confirming the specific = expression of=20 IQGAP1 and CD133 in glioblastoma amplifying cancer progenitor = cells=20 in vivo.


3D"   =20 Discussion
Top
Abstract
Introduction
Materials and Methods
Results
3D"Discussion
References
 
D= etailed=20 investigation of IQGAP1 expression in adult rat brain by = indirect=20 immunofluorescence has revealed a restricted pattern of = accumulation=20 of the protein in brain endothelial cells, in the epithelial=20 ependymal cells lining the ventricles, and in amplifying = neural=20 progenitor cells abundant in the germinative SVZ and RMS. We = have=20 confirmed the expression of IQGAP1 protein in amplifying = neural=20 progenitors isolated from adult rat SVZ and grown as = neurospheres=20 in vitro. In the rat brain and in neurosphere cells,=20 IQGAP1+ cells also express the neural progenitor = marker=20 nestin. The IQGAP1+/nestin+ neural progenitors=20 associate as dense clusters and are generally concentrated = around=20 blood vessels. This location places neural progenitor cells = in=20 close proximity to the endothelial cells, facilitating=20 interaction and communication between these two cell types. = These=20 cellular interactions are important to control neural = progenitor=20 self-renewal and differentiation (23=9625).=20 In a rat model of glioblastoma-like tumors, IQGAP1 is also = expressed=20 by a subpopulation of nestin+/GFAP=96 = cells. The=20 mitotic cells present in the tumors express IQGAP1, = indicating that=20 the IQGAP1+/nestin+ cells are part of the=20 proliferating component of the tumor. Our results corroborate = previous study showing that, in ENU-induced rat glioma,=20 nestin+ cells frequently incorporated = bromodeoxyuridine=20 (BrdUrd), whereas other tumor cells expressing GFAP were only = rarely=20 colabeled with BrdUrd (20).=20 Rat cell lines can be derived from ENU-induced glioma. One = example is=20 the C6 cell line used as a cellular model of brain glioma. A = side=20 population of tumorigenic cancer stem-like cells persists in = the C6=20 glioma cell line (26).=20 We have purified C6 side population cells by flow cytometry = (26)=20 and shown that they express both IQGAP1 and nestin (data not = shown).=20 These observations suggest that the=20 IQGAP1+/nestin+ cells may be important = in the=20 early stages of brain tumorigenesis. Several possibilities = exist for=20 the source of such cells. One possibility is that a precursor = cell or=20 a differentiated cell in the parenchyma undergoes = transformation,=20 after which it expresses nestin and IQGAP1. Alternatively, a=20 nestin+/IQGAP1+ neural progenitor in = the SVZ=20 and the RMS could migrate to this area after transformation. = Very=20 recent studies have shown that amplifying neural progenitors = capable=20 of proliferation and multipotential differentiation can = indeed=20 migrate to the brain parenchyma to produce new neurons and = glia (27).=20

In contrast to rat glioblastoma, = IQGAP1+/nestin+ tumor=20 cells are absent in rat tumors with oligodendroglial = phenotypes.=20 Because oligodendroglioma-like tumors express oligodendrocyte = progenitor markers (Olig-2/NG2), it is likely that that these = tumors=20 are related to oligodendrocyte progenitors as already = suggested=20 for human oligodendrogliomas (22).=20 Oligodendrogliomas might arise from a stem cell that acquires = oligodendrocyte progenitor phenotypes determined by = environment (3)=20 or might directly derive from multipotent oligodendroglial=20 progenitors (28).=20 The exact origin of oligodendrogliomas remains to be further=20 studied. To validate our results with rat brain tumor model, = we=20 next studied IQGAP1 expression in human oligodendroglioma and = glioblastoma. We confirmed that IQGAP1 is a reliable marker = that may=20 help to distinguish oligodendroglioma from glioblastoma.=20 Although in both tumors IQGAP1 is expressed by endothelial = cells,=20 only in glioblastoma it specifies a population of amplifying=20 tumor cells. Remarkably, IQGAP1 is absent from the astrocytic = contingency of the tumors, which often induces bias in brain = tumor=20 classification. IQGAP1 may thus represent a protein marker = that may=20 have significant implication in the classification of human = brain=20 tumors. The human glioblastoma IQGAP1+ cells can = be=20 expanded in vitro as neurospheres and exhibit features = of=20 multipotent glioblastoma tumorigenic neural precursors (Fig.=20 6; Supplementary Fig. S3). In vivo, the amplifying = IQGAP1+ cancer cells are surrounded by tumor cells = that=20 have down-regulated IQGAP1 expression and express the=20 differentiation-associated marker antigen GFAP. Nonetheless, = GFAP=20 expression does not correlate with full differentiation, as = the cells=20 still express the stem/progenitor cell marker nestin. = Although, these=20 GFAP+/nestin+ cells are still able to = proliferate,=20 in vivo and in vitro, they have lost their = tumorigenicity=20 (8).=20 All together, these findings suggest that the amplifying=20 IQGAP1+ cancer cells are closer to a multipotent=20 progenitor cells and represent the most aggressive cancer = cell=20 population in glioblastoma. The clusters of = IQGAP1+ tumor=20 cells most likely correspond to the glioblastoma amplifying = cancer=20 cells that represent up to 30% of the glioblastoma tumor cell = population (8)=20 and maybe the cell population, which has to be target for = more=20 effective cancer therapies of glioblastoma. The close = association=20 between IQGAP1+ amplifying cancer cells with blood = vessels=20 might contribute to maintain cancer cells undifferentiated = with high=20 tumorigenic potential. Several studies have already pointed = out that=20 endothelial cells are important in the regulation of neural=20 progenitor proliferation and differentiation (23=9625).=20 The close association between amplifying cancer cells and = endothelial=20 cells also raises the possibility that the tumorigenic cells = may use=20 blood vessels to migrate and disseminate throughout the brain = parenchyma. Indeed, in both rat and human glioblastomas, the=20 perivascular clusters of amplifying cancer cells are not = concentrated=20 within a single tumor area but are found dispersed within the = tumor mass. The migratory potential of tumorigenic cells = could=20 explain the local recurrence of gliomas after surgical = resection=20 or radiotherapy that targets the tumor mass but does not=20 necessarily include the zones where cancer cells might have = migrated.=20 The IQGAP1 signaling pathway might play an essential role in = the=20 control of these migration and invasion processes. IQGAP1 is = a=20 key component of cell motility signal transduction (16=9618).=20 In neural precursors, in response to intracellular Ca2+ = elevation, IQGAP1 forms a complex with Rho family GTPases, = CLIP-170=20 and Lis1, and enhances neuronal motility (17).=20 In endothelial cells, IQGAP1 interacts with the vascular = endothelial=20 growth factor (VEGF) receptor 2 (VEGF-R2) to promote = endothelial cell=20 migration (16).=20 VEGF-R2 is also expressed by neural progenitors and mediates = the=20 chemotactic activities of VEGF on neural progenitors (29).=20 We have found that neurospheres derived from wild-type mice=20 respond to the VEGF-mediated chemokinesis but not those = derived=20 from iqgap1 null mice, suggesting that IQGAP1 signaling=20 pathway might play an essential role in the control of neural = progenitor migration.4=20 Considering the similarities between IQGAP1+ amplifying=20 neural progenitors and IQGAP1+ glioblastoma amplifying=20 cancer cells, the proposed function of IQGAP1 in the = regulation=20 of neural progenitor migration can be extended to the = amplifying=20 tumor cells in human glioblastoma. A better understanding of=20 the IQGAP1 signaling in amplifying tumor cells may open new=20 avenue to develop pharmacologic approach aiming to neutralize = these cells, which represent the most aggressive cell type in = glioblastoma.


3D"   =20 Acknowledgments =
 
Grant support:=20 Association pour la Recherche sur le Cancer grant 4725 and = R=E9gion=20 Rh=F4ne-Alpes Emergence grant 8HC04H00 (J. Baudier) and = Institut=20 National du Cancer grant PL114 (J. Baudier and J. = Honnorat).=20

The costs of publication of this article were defrayed in part = by=20 the payment of page charges. This article must therefore be = hereby=20 marked advertisement in accordance with 18 U.S.C. = Section 1734=20 solely to indicate this fact.

We thank Dr. H. Chneiweiss for generous gift of Olig-2 = antibodies,=20 Prof. J. LaMarre (Guelph University, Guelph, Ontario, Canada) = for critical reading of the article, Dr. D. Grunwald for = assistance=20 in confocal microscopy analysis, and Dr. J.C. Deloulme for = advices=20 in neurosphere cultures.


3D"   =20 Footnotes
 
Note: Supplementary data for this = article are=20 available at Cancer Research Online (http://cancerres.aacrjournals= .org/).=20

J. Honnorat and J. Baudier contributed = equally to=20 this work.

4 L. Balenci, A. Bernards, = and J.=20 Baudier, unpublished data.

Received 2/27/06. Revised 7/ 1/06. Accepted 7/25/06.


3D"   =20 References
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Abstract
Introduction
Materials and Methods
Results
Discussion
3D"References
&nb= sp;

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Molecular=20 Cancer Research Cell Growth=20 & Differentiation
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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_0000_01C85785.EFA3B790 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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