From: Subject: Stem Cell-like Glioma Cells Promote Tumor Angiogenesis through Vascular Endothelial Growth Factor -- Bao et al. 66 (16): 7843 -- Cancer Research Date: Tue, 15 Jan 2008 15:00:56 +0100 MIME-Version: 1.0 Content-Type: multipart/related; type="text/html"; boundary="----=_NextPart_000_0000_01C85787.6EAC82A0" X-MimeOLE: Produced By Microsoft MimeOLE V6.00.2900.3198 This is a multi-part message in MIME format. ------=_NextPart_000_0000_01C85787.6EAC82A0 Content-Type: text/html; charset="Windows-1252" Content-Transfer-Encoding: quoted-printable Content-Location: http://cancerres.aacrjournals.org/cgi/content/full/66/16/7843 Stem Cell-like Glioma Cells Promote Tumor = Angiogenesis through Vascular Endothelial Growth Factor -- Bao et al. 66 = (16): 7843 -- Cancer Research 3D"Cancer 3D"Ubiquitin 3D"
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[Cancer Research 66, 7843-7848, August 15, = 2006]
=A9 2006 American = Association=20 for Cancer Research

Priority Reports

Stem Cell=96like Glioma Cells Promote Tumor Angiogenesis through = Vascular=20 Endothelial Growth Factor

Shideng=20 Bao1,5, Qiulian=20 Wu1,5, Sith=20 Sathornsumetee1,5, Yueling=20 Hao1,5, Zhizhong = Li6,=20 Anita B. Hjelmeland1,5, Qing=20 Shi1,5, Roger E. = McLendon2,=20 Darell D. Bigner1,2,5 and=20 Jeremy N.=20 Rich1,3,4,5,6=20

Departments of 1 Surgery, 2 = Pathology,=20 3 Medicine, and 4 Neurobiology; 5 = Preston=20 Robert Tisch Brain Tumor Center; and 6 Molecular Cancer = Biology=20 Program, Duke University Medical Center, Durham, North Carolina

Requests for reprints: Jeremy N. Rich, Preston = Robert=20 Tisch Brain Tumor Center, Duke University Medical Center, Box 2900, = Durham, NC=20 27710. Phone: 919-681-1693; Fax: 919-684-6514; E-mail: rich0001{at}mc.duke.edu .


3D"   =20 Abstract
Top
3D"Abstract
Introduction
Materials and Methods
Results and Discussion
References
 
M= alignant=20 gliomas are highly lethal cancers dependent on angiogenesis. = Critical=20 tumor subpopulations within gliomas share characteristics = with neural=20 stem cells. We examined the potential of stem cell=96like = glioma cells=20 (SCLGC) to support tumor angiogenesis. SCLGC isolated from = human=20 glioblastoma biopsy specimens and xenografts potently = generated=20 tumors when implanted into the brains of immunocompromised = mice,=20 whereas non-SCLGC tumor cells isolated from only a few tumors = formed=20 secondary tumors when xenotransplanted. Tumors derived from = SCLGC=20 were morphologically distinguishable from non-SCLGC tumor = populations=20 by widespread tumor angiogenesis, necrosis, and hemorrhage. = To=20 determine a potential molecular mechanism for SCLGC in = angiogenesis,=20 we measured the expression of a panel of angiogenic factors = secreted=20 by SCLGC. In comparison with matched non-SCLGC populations, = SCLGC=20 consistently secreted markedly elevated levels of vascular=20 endothelial growth factor (VEGF), which were further induced = by=20 hypoxia. In an in vitro model of angiogenesis,=20 SCLGC-conditioned medium significantly increased endothelial = cell=20 migration and tube formation compared with non-SCLGC tumor=20 cell=96conditioned medium. The proangiogenic effects of = glioma SCLGC on=20 endothelial cells were specifically abolished by the = anti-VEGF=20 neutralizing antibody bevacizumab, which is in clinical use = for=20 cancer therapy. Furthermore, bevacizumab displayed potent=20 antiangiogenic efficacy in vivo and suppressed growth = of=20 xenografts derived from SCLGC but limited efficacy against = xenografts=20 derived from a matched non-SCLGC population. Together these = data=20 indicate that stem cell=96like tumor cells can be a crucial = source of=20 key angiogenic factors in cancers and that targeting = proangiogenic=20 factors from stem cell=96like tumor populations may be = critical for=20 patient therapy. (Cancer Res 2006; 66(16): 7843-8) =


3D"   =20 Introduction
Top
Abstract
3D"Introduction
Materials and Methods
Results and Discussion
References
 
A= ngiogenesis=20 is critical to tumor formation and maintenance (1).=20 Regulation of angiogenesis represents a complex process = involving=20 autocrine and paracrine growth factor loops with an interplay = between=20 tumor cells and the neovasculature (2).=20 Malignant gliomas are highly lethal neoplasms that exhibit = striking=20 angiogenesis with elevated expression of vascular endothelial = growth=20 factors (VEGFs), which promote blood vessel formation by=20 endothelial precursors (3,=20 4).=20 VEGFs are secreted or cell surface=96bound proteins expressed = by tumor=20 cells that bind to specific high-affinity transmembrane = receptors=20 primarily expressed on endothelial cells (5)=20 to promote endothelial cell proliferation, migration, and = survival.=20 We recently showed that a novel antiangiogenic receptor = kinase=20 inhibitor (ZD6474) was highly effective against multiple = central=20 nervous system cancer xenografts, including gliomas (6).=20 Receptor kinase inhibitors had limited benefit in clinical = trials in=20 gliomas (7,=20 8),=20 but frequent glioblastoma patient tumor responses were = observed using=20 a neutralizing anti-VEGF monoclonal antibody, bevacizumab = (Avastin),=20 in combination with the topoisomerase I inhibitor irinotecan = (9).=20 Improvements in the efficacy of these treatments will require = advances in our understanding of the molecular mechanisms = promoting=20 glioblastoma angiogenesis. Recent studies of glioblastomas = and other=20 brain cancers identified tumor subpopulations that share=20 characteristics with normal neural stem cells (10=9614).=20 Stem cell=96like glioma cells (SCLGC) express neural stem = cell markers=20 (including the cell-surface antigen prominin-1/CD133), are = capable of=20 self-renewal, form neurosphere-like spheroids, and = differentiate into=20 multiple nervous system lineages (neurons, astrocytes, and=20 oligodendrocytes; refs. 10=9613).=20 When xenotransplanted into the brains of immunocompromised = rodents,=20 human SCLGC show greater potential than non-SCLGC cancer = cells to=20 initiate tumor formation (12,=20 13).=20 The mechanisms responsible for the differential tumorigenic = capacity=20 of SCLGC remain unknown, but non-SCLGC do survive when = transplanted=20 intracranially (13).=20 As angiogenesis represents a critical step in tumor formation = (the=20 "angiogenic switch"), we examined whether SCLGC contribute to = tumor=20 formation through promoting angiogenesis. We now report that = SCLGC=20 enhance glioma angiogenesis through a VEGF-dependent = mechanism.=20


3D"   =20 Materials and Methods
Top
Abstract
Introduction
3D"Materials and = Methods
Results and Discussion
References
 
<= B>Chemicals=20 and reagents. Neutralizing anti-VEGF antibody, bevacizumab=20 (Avastin, Genentech, South San Francisco, CA), was purchased=20 from the Duke Hospital clinical pharmacy (Durham, NC). All = other=20 chemicals were purchased from Sigma (St. Louis, MO) unless = otherwise=20 specified.

Patient biopsy specimens. Specimens from patients = undergoing=20 biopsy for newly diagnosed or recurrent glioblastoma were = collected=20 under a Duke University Institutional Review Board=96approved = protocol. Pathologic diagnosis was confirmed by R.E.M.

Human glioma xenografts. D456MG xenograft was derived from = a=20 biopsy specimen from a 4-year-old child with glioblastoma. = D54MG=20 xenograft is the Duke subline of A-172, which was derived = from=20 a 54-year-old male with glioblastoma. Xenografts were = maintained=20 in the flanks of athymic BALB/c nu/nu mice and early = passages=20 were used to minimize genetic drift.

Purification and characterization of stem cell=96like = glioblastoma=20 cells. SCLGC were derived from tumors from patients or = xenografts=20 as previously described (10=9613).=20 Briefly, tumors were disaggregated, labeled with an = allophycocyanin-=20 or phycoerythrin-conjugated CD133 antibody (Miltenyi Biotec, = Auburn,=20 CA), and sorted by fluorescence-activated cell sorting = (FACS). Glioma=20 cells derived from xenografts were confirmed to be human = through FACS=20 analysis with the FITC-labeled 3B4 human specific antibody = (15).=20 Tumor spheroids were maintained and passaged as previously=20 described (13).=20 Immunofluorescence studies confirmed spheroid expression of = stem cell=20 markers and lineage markers when subjected to differentiation=20 conditions as previously described (16).=20

Intracranial tumor assays. CD133+ and = CD133=96=20 tumor cell populations were segregated by cell sorting. After = short-term culture, 10,000 cells were implanted into the = right=20 frontal lobes of athymic BALB/c nu/nu mice under a = Duke=20 University Institutional Animal Care and Use = Committee=96approved=20 protocol as previously described (6).=20 Mice were maintained for 4 weeks or until the development of=20 neurologic symptoms. Brains of euthanized mice were = collected, fixed=20 in formalin, paraffin embedded, and sectioned, or were frozen = rapidly=20 in liquid nitrogen for sections.

Tumor vascular quantification. Blood vessel density in = frozen=20 tumor sections was quantified as previously described (17).=20

Angiogenesis antibody array analysis. Conditioned media = were=20 harvested from matched CD133+ and CD133=96=20 glioblastoma tumor cell cultures grown in 60-mm plates in = neural=20 basal medium without growth factors for 24 hours. Hypoxia was = induced=20 through maintenance of cells in a closed syringe for 24 = hours.=20 TranSignal Human Angiogenesis Antibody Arrays (Panomics, = Fremont, CA)=20 were incubated with 2 mL of conditioned medium for 1.5 hours = and=20 then replaced with another 2 mL for 1.5 hours (total, 4 mL=20 conditioned medium, 3 hours of incubation) and processed = according to=20 the instructions of the manufacturer. Intensity of VEGF=20 expression was quantified with ImageJ software.7=20 Total mean intensity =3D area x mean=20 intensity.

VEGF ELISA. Human VEGF Quantikine ELISA Kits (R&D = Systems,=20 Minneapolis, MN) were used according to the directions of the = manufacturer. Two-hundred microliters of conditioned media = were=20 collected from triplicate samples.

Endothelial migration assays. Media conditioned by = CD133+=20 or CD133=96 populations for 24 hours were added to = the=20 bottom chambers of 24-well tissue culture plates in = triplicate.=20 Human microvascular endothelial cells (20,000) were added to = the=20 upper chambers of Transwell assays (BD Biosciences, Franklin=20 Lakes, NJ). In experiments with a VEGF neutralizing antibody, = bevacizumab or immunoglobulin G (IgG) control (final, 0.5 = mg/mL) was=20 added to conditioned media 30 minutes before addition of=20 endothelial cells. Cells were allowed to invade for 14 hours = and then=20 fixed, stained, and quantified.

Endothelial tube formation assays. Media conditioned by=20 CD133+ or CD133=96 populations for 24 = hours were=20 added to 2,000 human microvascular endothelial cells in = sextuplicate=20 wells of Matrigel-coated 96-well plates (BD Biosciences). In=20 VEGF neutralizing experiments, bevacizumab or IgG control=20 (final, 0.5 mg/mL) was added to conditioned media 30 minutes=20 before addition to endothelial cell cultures in triplicate. = Cells=20 were incubated for 16 hours, imaged, and quantified. =

Xenograft assays. Matched CD133+ and = CD133=96=20 glioma cellular populations were implanted in either s.c. or=20 intracranial locations with the specified cell number. After=20 establishment, tumor-bearing animals were treated with either = bevacizumab or a control IgG (5 mg/kg i.p. qd) for a total of = 21 days=20 (s.c.) or 19 days (intracranial) until harvest. Mice were = euthanized=20 and tumors or tumor-bearing brains were harvested, weighed, = and=20 examined.

Statistical analysis. Descriptive statistics were = generated=20 for all quantitative data with presentation of means =B1 = SEs.=20 Significance was tested by one-way ANOVA using the SAS = Enterprise=20 Guide 3.0 (Cary, NC).


3D"   =20 Results and Discussion
Top
Abstract
Introduction
Materials and Methods
3D"Results and = Discussion
References
 
<= B>Derivation=20 of SCLGC. Central nervous system neoplastic stem cells = were=20 defined through their phenotypic similarities to neural stem = cells=20 (10=9614).=20 Prior reports investigated SCLGC from patient tumor biopsy = specimens=20 (10=9613),=20 but we additionally generated short-term cultures from=20 glioblastoma xenografts derived from human patient biopsy = specimens=20 that were maintained in immunocompromised mice in either s.c. = or=20 intracranial locations. Human biopsy specimens validate = biological=20 processes directly in patient cancers, whereas human glioma=20 xenografts permit the purification of large numbers of viable = tumor cells. The CD133 cell-surface stem cell marker was used = to select for a cell population enriched for SCLGC (13).=20 Although the fraction of CD133+ tumor cells varied = between=20 sources, we detected between 2.9% and 4.3% of tumor cells = expressed=20 the CD133+ marker and formed spheroids (data not = shown).=20 We derived separate short-term cultures of CD133+ = and=20 CD133=96 tumor cells through tumor disaggregation, = labeling=20 with CD133 antibody, and FACS sorting. The CD133+=20 population was >95% pure in repeated FACS analysis (data = not=20 shown). The tumor cell populations derived from human glioma=20 xenografts grown in mice were composed nearly exclusively of = human=20 tumor cells (>99%) without significant contamination from = murine=20 cells through analysis with 3B4 antihuman antibody (data not=20 shown).

Cultured CD133+ glioma cells from biopsy specimens and=20 xenografts formed neurosphere-like spheroids when grown in = stem cell=20 medium (Supplementary Fig. S1A). These spheroids were = capable=20 of generating new spheroids under limiting passage conditions = consistent with self-renewal (data not shown), expressed = neural stem=20 cell markers (CD133, Nestin, Sox 2, and Musashi 1; = Supplementary Fig.=20 S1B), and underwent multilineage differentiation = (neuronal,=20 astrocytic, and oligodendrocytic) under prodifferentiation = conditions=20 (Supplementary Fig. S2). In contrast, CD133=96 = tumor cells=20 grew in an adherent fashion without spheroid formation, = expressed=20 only astrocytic markers, and underwent senescence on = fulfilling the=20 criteria of two distinct tumor cell populations: SCLGC and=20 non-SCLGC.

Tumors generated from CD133+ glioma population display=20 increased tumor vascularity, necrosis, and hemorrhage. = Recent=20 studies of stem cell=96like cancer cells have suggested that=20 tumorigenesis is dichotomized between the SCLGC and non-SCLGC = populations (12,=20 13).=20 To investigate the tumorigenic capacity of our glioma = subpopulations,=20 10,000 CD133=96 or CD133+ glioma cells = derived=20 from multiple human glioblastoma patient specimens or two = human=20 glioma xenografts (D456MG and D54MG) were implanted into the=20 right frontal lobes of athymic nude mice. Regardless of tumor = source, every brain implanted with the CD133+ tumor = cells=20 displayed gross evidence of highly angiogenic and hemorrhagic = tumors, in stark contrast to the brains implanted with=20 CD133=96 tumor cells (Fig.=20 1A and data not shown). Pathologic analysis of the = brains=20 implanted with CD133+ glioma cells showed large, = highly=20 proliferative and vascular tumors with widespread necrosis = and=20 hemorrhage (Fig.=20 1C and data not shown). No mice implanted with=20 CD133=96 tumor cells from human biopsy specimens or = the=20 majority of xenografts displayed evidence of brain tumor = formation=20 (data not shown). D456MG xenograft-derived CD133=96 = tumor=20 cells formed small tumors (in two of six mice in replicate=20 experiments; Fig.=20 1B), permitting a comparison of vascularity = between brains=20 bearing CD133+ and CD133=96 xenografts. With = CD31=20 immunostaining, we observed that tumors derived from = CD133+=20 cells were markedly more vascular than tumors from = CD133=96=20 tumor cells (Fig.=20 1D). Therefore, angiogenic potential is a critical = difference between the in vivo tumor phenotypes of = glioma=20 SCLGC and non-SCLGC cells.



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  		Figure 1. SCLGC form more = vascular=20 and necrotic tumors when grown in the brains of = immunocompromised=20 mice. Ten thousand cells derived from CD133=96 or = CD133+ tumor cell populations cultured from = D456MG=20 xenografts were implanted into the right frontal lobes of = athymic=20 nude BALB/c mice. Mice were sacrificed after 28 days. = A, four=20 pairs of representative brains bearing tumors derived from=20 CD133=96 and CD133+ cells. B = and=20 C, pathologic morphology of brain tumors derived from = CD133=96 and CD133+ populations. The = brains were=20 fixed in formalin, paraffin embedded, cut into 5-=B5m = sections, and=20 then stained with H&E. B, two of six brains with=20 CD133=96 tumor cells implanted had tumor = formation (x400). C, in contrast, = all brains=20 implanted with CD133+ tumor cells displayed large = tumors=20 with widespread necrosis, hemorrhage, and neoangiogenesis = (x400). D, the blood = vessel=20 density in tumors derived from CD133=96 and=20 CD133+ cells was measured. Tumor-bearing brains = were snap=20 frozen, cut into 6-=B5m frozen sections, fixed, = immunostained with rat=20 anti-mouse CD31 antibody (or IgG control antibody), and=20 counterstained with hematoxylin. Representative images = (x400). The densities of CD31 = stained=20 blood vessels were quantified. *, P =3D 0.0002, = vascular=20 density of tumors derived from CD133+ cells = versus=20 CD133=96 cells (Student's t test). =

 = ;
Stem=20 cell=96like glioma cancer cells express elevated levels of = VEGF. To=20 determine potential molecular mechanisms underlying the = differential=20 vascular phenotypes of SCLGC and non-SCLGC derived tumors, we = compared the expression of regulators of angiogenesis = secreted by=20 CD133+ and CD133-cells. Patterns of angiogenesis = regulator=20 expression differed between specimens but revealed modest = changes in=20 angiogenin, interleukin-8, interleukin-6, and basic = fibroblast growth=20 factor (Fig.=20 2 and Supplementary Fig. S3). However, VEGF levels in=20 CD133+ glioma cell conditioned media were = consistently=20 up-regulated 10- to 20-fold compared with CD133=96 = media (Fig.=20 2 and Supplementary Fig. S3) in populations derived from = both=20 patient biopsies and human glioma xenografts. Increased VEGF=20 secretion in CD133+ versus CD133=96 = cells was=20 also confirmed through VEGF ELISA (Fig.=20 2D and Supplementary Fig. S3C). = Furthermore, both=20 CD133+ and CD133=96 glioma tumor cells = increased=20 VEGF expression in response to hypoxia, but CD133+ = tumor=20 cells expressed elevated VEGF levels relative to the=20 CD133=96 cells under hypoxic conditions (Fig.=20 2 and Supplementary Fig. S3C). In summary, SCLGC=20 consistently expressed higher levels of VEGF than the = non-SCLGC under=20 normoxic and hypoxic conditions.



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  		Figure 2. SCLGC express = elevated=20 level of VEGF and hypoxia induces increased VEGF expression. = A and B, to determine if SCLGC differentially = express=20 proangiogenic factors, we used commercial antibody arrays = (Panomics=20 TranSignal Human Angiogenesis Antibody Array) to compare the = expression levels of regulators of angiogenesis in = conditioned media=20 from matched CD133+ and CD133=96 = glioma=20 cultures. Media conditioned for 24 hours from short-term=20 CD133=96 or CD133+ glioma cultures = derived from=20 a patient biopsy specimen under normoxic (A) or = hypoxic=20 (B) conditions were collected. Cells were maintained = under=20 hypoxic conditions for 24 hours. Membranes were processed = based on=20 kit instructions. The intensity of VEGF expression was = quantified=20 with ImageJ software. C, total mean intensity of VEGF = blot=20 was calculated based on the product of area and mean = intensity. *,=20 P =3D 0.0036, hypoxic versus normoxic conditions of=20 CD133=96 conditioned medium (ANOVA); **, P = =3D 0.001,=20 CD133+ conditioned medium versus = CD133=96=20 conditioned medium (ANOVA); ***, P =3D 0.005, hypoxic = versus=20 normoxic conditions of CD133+ conditioned medium = (ANOVA).=20 D, VEGF expression levels in media conditioned for 24 = hours=20 from glioblastoma patient specimen cell populations grown in = 24-well=20 plates were measured using a VEGF Quantikine ELISA (R&D = Systems)=20 according to the directions of the manufacturer. Triplicate = samples=20 were collected for each sample. *, P =3D 0.0002, = normoxic=20 CD133+ medium versus CD133=96 medium = (ANOVA);=20 **, P =3D 0.0094, hypoxic versus normoxic conditions = of=20 CD133+ conditioned medium (ANOVA); P =3D = 0.011,=20 hypoxic CD133+ medium versus hypoxic = CD133=96=20 medium (ANOVA). =

 = ;
SCLGC=20 induce endothelial cell migration and tube formation. = VEGF and=20 other angiogenic factors potently regulate endothelial = behavior in=20 new vasculature formation. In in vitro models of = angiogenesis,=20 angiogenic factors promote endothelial cell migration and/or = induce=20 formation of vascular tubular structures when cultured on = Matrigel.=20 We tested the ability of conditioned media from both=20 CD133+ and CD133=96 cells to modify = endothelial=20 cell phenotypes. CD133+ glioma cell conditioned medium=20 consistently increased migration of human microvascular = endothelial=20 cells as compared with CD133=96 conditioned medium = (Supplementary Fig. S4). The addition of conditioned medium = from=20 CD133+ glioma cultures also promoted endothelial = cell tube=20 formation in vitro by increasing human microvascular=20 endothelial cell tube length, number of branch points, and = tube=20 complexity (Supplementary Fig. S5). Together these results = suggest=20 that CD133+ cells produce proangiogenic factors = that can=20 directly modify endothelial cell behavior.

Targeting VEGF inhibits effects of SCLGC on endothelial = cells.=20 Methods to inhibit tumor-associated angiogenesis are under=20 development, including anti-VEGF antibodies and low molecular = weight=20 VEGF receptor tyrosine kinase inhibitors. One neutralizing=20 anti-VEGF antibody, bevacizumab/Avastin, binds to human = VEGF-A=20 ligand to prevent endothelial cell receptor activation and = has=20 shown combinatorial efficacy with irinotecan (CPT-11) in=20 high-grade glioma patients (9).=20 To determine if the increased levels of VEGF in = CD133+=20 glioma conditioned media represent the mechanism through = which=20 CD133+ glioma cells promote in vitro measures = of=20 angiogenesis, we examined the effect of bevacizumab antibody = in our=20 endothelial cell assays. Similar to the above studies, = conditioned=20 medium from CD133+ cells derived from a human = glioblastoma=20 specimen or a human xenograft, mixed with the IgG control = antibody,=20 induced a striking increase in human microvascular = endothelial=20 cell migration (Fig.=20 3A and Supplementary Fig. S6A) and tube = formation=20 (Fig.=20 3B and Supplemental Fig. S6B). Addition of = bevacizumab=20 to neutralize VEGF in CD133+ glioma conditioned medium=20 blocked its proangiogenic effects on endothelial cell = migration (Fig.=20 3A and Supplementary Fig. S6A) and tube = formation=20 (Fig.=20 3B and Supplementary Fig. S6B) to levels = equal to=20 the effects of CD133=96 glioma conditioned medium. = In=20 contrast, bevacizumab displayed only marginal effects on = human=20 microvascular endothelial cells exposed to non-SCLGC = conditioned=20 medium. Thus, the effects of SCLGC on endothelial cell = behavior are=20 dependent on VEGF activity and bevacizumab specifically = blocks the=20 effects of SCLGC on endothelial cell behavior in cell culture = assays.



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  		Figure 3. VEGF = neutralizing=20 antibody blocks SCLGC-induced endothelial cell migration and = tube=20 formation. A, a VEGF neutralizing antibody, = bevacizumab,=20 blocks SCLGC-induced endothelial cell migration. Media = conditioned=20 for 24 hours by CD133=96 or CD133+ = cultures=20 isolated from a patient glioblastoma patient specimen were = added to=20 the bottom chambers of 24-well tissue culture plates. = Bevacizumab or=20 an IgG antibody control (antibody final concentration, 0.5 = mg/mL)=20 was added to conditioned media 30 minutes before addition to = endothelial cell cultures. Human microvascular endothelial = cells=20 (20,000) were added to the upper chambers of Transwell = assays (BD=20 Biosciences). Cells were allowed to invade for 14 hours, = fixed,=20 stained, imaged, and quantified. Representative images. *, = P=20 =3D 0.0003, CD133+ conditioned medium versus=20 CD133=96 conditioned medium (ANOVA); **, P = =3D 0.0005,=20 bevacizumab-treated CD133+ conditioned medium = versus IgG=20 control (ANOVA). B, VEGF neutralizing antibody blocks = SCLGC-induced endothelial cell tube formation. Cultures of=20 CD133=96 or CD133+ glioma cells = derived from a=20 patient glioblastoma patient specimen were used to condition = media=20 for 24 hours. To these media were added human microvascular=20 endothelial cells grown at a density of 40,000 cells/mL with = 50 =B5L=20 of cells added to sextuplicate wells of Matrigel-coated = 96-well=20 plates (BD Biosciences). Bevacizumab or an IgG antibody = control=20 (final concentration, 0.5 mg/mL) was added to conditioned = media 30=20 minutes before addition to endothelial cell cultures. The=20 endothelial cells were incubated in the conditioned media = for 16=20 hours and then imaged. Representative images. *, P = <=20 0.0001, CD133+ conditioned medium versus=20 CD133=96 conditioned medium (ANOVA); **, P = <=20 0.0001 bevacizumab-treated CD133+ conditioned = medium=20 versus IgG control (ANOVA). =

 = ;
Bevacizumab=20 specifically targets SCLGC tumor growth in vivo. = To=20 confirm the relevance of the in vitro results, we examined = the=20 effects of inhibiting the VEGF axis through the use of bevacizumab. = We quantified the therapeutic effects of bevacizumab on s.c.=20 xenografts derived from matched SCLGC and non-SCLGC tumor = cell=20 populations. Bevacizumab potently inhibited the growth of=20 SCLGC-derived xenografts with a reduction in tumor weight,=20 vascularity, and hemorrhage (Fig.=20 4 ). In contrast, the small tumors derived from non-SCLGC = tumor=20 cells were not significantly inhibited in growth by = bevacizumab.=20 Parallel results were noted in intracranial studies = (Supplementary=20 Fig. S7A).



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  		Figure 4. VEGF = neutralizing=20 antibody bevacizumab specifically suppresses SCLGC tumor = growth and=20 hemorrhage in vivo. A, treatment with = VEGF-neutralizing=20 antibody, bevacizumab, inhibits the in vivo tumor = growth of=20 xenografts derived from SCLGC and blocks the SCLGC-induced = tumor=20 hemorrhage in vivo. CD133+ cells (100,000) = isolated from D456MG xenografts were implanted s.c. into two = groups=20 (five animals per group) of athymic nude BALB/c mice. = Tumor-bearing=20 animals were treated with either bevacizumab (5 mg/kg i.p. = qd) or=20 control IgG (5 mg/kg i.p. qd) for a total of 21 days until = harvest.=20 Mice were euthanized and tumors were harvested, weighed, and = examined. Representative tumor-bearing mice and dissected = tumors=20 from the two groups. SCLGC-derived tumors from the control = IgG group=20 showed rapid tumor growth with extensive hemorrhage, but = treatment=20 with the VEGF neutralizing antibody bevacizumab = significantly=20 suppressed SCLGC tumor growth in vivo and = dramatically=20 reduced the tumor hemorrhage of xenografts derived from = SCLGC.=20 B, the VEGF neutralizing antibody bevacizumab shows = limited=20 efficacy against xenografts derived from non-SCLGC tumor = cells.=20 CD133=96 cells (100,000) derived from D456MG = xenografts=20 were implanted s.c. into two groups of athymic nude BALB/c = mice.=20 Tumor-bearing animals (five animals per group) were treated = with=20 either bevacizumab (5 mg/kg i.p. qd) or control IgG (5 mg/kg = i.p.=20 qd) for a total of 21 days until harvest. Mice were = euthanized and=20 tumors were harvested, weighed, and examined. Representative = tumor-bearing animals and dissected tumors from the two = groups. The=20 tumors derived from CD133=96 cells were small and = did not=20 display significant hemorrhage. Bevacizumab treatment did = not=20 significantly inhibit the growth of the xenografts derived = from=20 CD133=96 cells. C, the tumor weights for = tumors from=20 (A) and (B) were quantified. *, P < = 0.001,=20 bevacizumab treatment versus control IgG. **, P > = 0.5,=20 bevacizumab treatment versus control IgG. =

 = ;
The=20 limited fraction of stem-like cells in gliomas may be critical = for=20 tumor growth not only through their capacity for self-replication = but=20 also through a paracrine effect supporting non-stemlike tumor = cells=20 by inducing neovascularization. Although the VEGF axis is a=20 particularly appealing molecular target in cancer, the = determinants=20 of patient response to these agents remain unclear. VEGF = levels and=20 microvascular density have not been correlated with patient = response=20 in clinical trials of bevacizumab for systemic cancers (18).=20 Our results suggest that only a subpopulation of the tumor = may be=20 critical for driving VEGF-mediated tumor angiogenesis as the = effects=20 of a VEGF neutralizing antibody (bevacizumab) predominantly = disrupt=20 the angiogenic effects of a fraction of the tumor, the stem = cell=96like=20 cancer cells.

Jain (19)=20 has established vascular "normalization" as a potential key = response=20 to antiangiogenic therapies, in addition to the vascular = pruning=20 caused through targeting angiogenesis. Bevacizumab may be = effective=20 as a cancer therapy when combined with chemotherapy by = improving=20 chemotherapy delivery specifically to the stem cell=96like = tumor cells=20 that would be expected to be proximal to the tumor = vasculature due to=20 VEGF expression. Indeed, we frequently detect = CD133+ tumor=20 cells in locations proximal to blood vessels (Supplementary = Fig.=20 S7B). Therapies directed to target VEGF-expressing = cells may=20 exhibit specificity against cancer stem cells. VEGF receptors = are not=20 expressed by SCLGC (data not shown); thus, targeting VEGF may = not=20 have a direct effect on cancer stem cells but rather = paracrine=20 effects on endothelial cells and (possibly) other cancer = cells. In=20 conclusion, our studies suggest that the tumor subpopulation = that=20 shares characteristics with stem cells can contribute to = tumor=20 malignancy and may be a key target of antiangiogenic = therapies.=20


3D"   =20 Acknowledgments =
 
Grant support:=20 Pediatric Brain Tumor Foundation of the United States, = Accelerate=20 Brain Cancer Cure, Childhood Brain Tumor Foundation (J.N. = Rich), and=20 Southeastern Brain Tumor Foundation (A.B. Hjelmeland); NIH = grants=20 NS047409, NS054276, and 1 P50 CA 108786 (J.N. Rich) and NIH = grants=20 NS20023 and CA11898 and NIH grant M01 RR 30, General Clinical = Research Center Program, National Center for Research = Resources,=20 National Cancer Institute Specialized Program of Research = Excellence=20 1 P20 CA096890, Federal Consulting Group grants, and a grant = from the=20 Pediatric Brain Tumor Foundation of the United States (D.D.=20 Bigner).

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.


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

A.B. Hjelmeland is a Paul = Brazen/American Brain=20 Tumor Association Fellow. J.N. Rich is a Damon Runyon-Lilly = Clinical=20 Investigator, supported by the Damon Runyon Cancer Research=20 Foundation, and a Sidney Kimmel Cancer Foundation = Translational=20 Scholar.

7 http://rsb.info.nih.gov/ij/.=20

Received 3/17/06. Revised 5/25/06. Accepted 7/ 6/06.


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

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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_01C85787.6EAC82A0 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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