From: Subject: Notch Pathway Inhibition Depletes Stem-like Cells and Blocks Engraftment in Embryonal Brain Tumors -- Fan et al. 66 (15): 7445 -- Cancer Research Date: Mon, 5 Apr 2010 12:12:07 +0200 MIME-Version: 1.0 Content-Type: multipart/related; type="text/html"; boundary="----=_NextPart_000_0000_01CAD4B9.3622F7A0" X-MimeOLE: Produced By Microsoft MimeOLE V6.00.2900.5579 This is a multi-part message in MIME format. ------=_NextPart_000_0000_01CAD4B9.3622F7A0 Content-Type: text/html; charset="Windows-1252" Content-Transfer-Encoding: quoted-printable Content-Location: http://cancerres.aacrjournals.org/cgi/content/full/66/15/7445 Notch Pathway Inhibition Depletes Stem-like Cells and = Blocks Engraftment in Embryonal Brain Tumors -- Fan et al. 66 (15): 7445 = -- Cancer Research 3D"Cancer 3D"
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[Cancer Research 66, 7445-7452, August 1, = 2006]
=A9 2006 American = Association=20 for Cancer Research

Molecular Biology, Pathobiology, and = Genetics

Notch Pathway Inhibition Depletes Stem-like Cells and Blocks = Engraftment in=20 Embryonal Brain Tumors

Xing = Fan1,=20 William Matsui2, Leila = Khaki1,=20 Duncan Stearns1, Jiong = Chun3,=20 Yue-Ming Li3 and Charles G.=20 Eberhart1,2

Departments of 1 Pathology and = 2=20 Oncology, Johns Hopkins University School of Medicine, Baltimore, = Maryland and=20 3 Molecular Pharmacology and Chemistry Program, Memorial=20 Sloan-Kettering Cancer Center, New York, New York

Requests for reprints: Charles G. Eberhart, = Department=20 of Pathology, Johns Hopkins University School of Medicine, Ross Building = 558,=20 720 Rutland Avenue, Baltimore, MD 21205. Phone: 410-502-5185; Fax: = 410-955-9777;=20 E-mail: ceberha{at}jhmi.edu .


3D"   =20 Abstract
Top
3D"Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
T= he Notch=20 signaling pathway is required in both nonneoplastic neural = stem cells=20 and embryonal brain tumors, such as medulloblastoma, which = are=20 derived from such cells. We investigated the effects of Notch = pathway=20 inhibition on medulloblastoma growth using pharmacologic = inhibitors=20 of 3D{gamma}-secretase. Notch blockade suppressed expression = of the=20 pathway target Hes1 and caused cell cycle exit, apoptosis, = and=20 differentiation in medulloblastoma cell lines. Interestingly, = viable=20 populations of better-differentiated cells continued to grow = when=20 Notch activation was inhibited but were unable to efficiently = form=20 soft-agar colonies or tumor xenografts, suggesting that a = cell=20 fraction required for tumor propagation had been depleted. It = has=20 recently been hypothesized that a small population of = stem-like cells=20 within brain tumors is required for the long-term propagation = of=20 neoplastic growth and that CD133 expression and Hoechst dye = exclusion=20 (side population) can be used to prospectively identify such=20 tumor-forming cells. We found that Notch blockade reduced the = CD133-positive cell fraction almost 5-fold and totally = abolished the=20 side population, suggesting that the loss of tumor-forming = capacity=20 could be due to the depletion of stem-like cells. Notch = signaling=20 levels were higher in the stem-like cell fraction, providing = a=20 potential mechanism for their increased sensitivity to = inhibition of=20 this pathway. We also observed that apoptotic rates following = Notch blockade were almost 10-fold higher in primitive=20 nestin-positive cells as compared with nestin-negative ones.=20 Stem-like cells in brain tumors thus seem to be selectively=20 vulnerable to agents inhibiting the Notch pathway. (Cancer = Res 2006;=20 66(15): 7445-52)


3D"   =20 Introduction
Top
Abstract
3D"Introduction
Materials and Methods
Results
Discussion
References
 
M= edulloblastoma=20 and other embryonal brain tumors are thought to arise = primarily from=20 neural stem/precursor cells of the ventricular zone and = cerebellar=20 external germinal layer (1=963).=20 Pathways such as Wingless, Hedgehog, and Notch, which control = the=20 specification, proliferation, and survival of nonneoplastic = neural=20 precursors, are also all aberrantly activated in such tumors, = suggesting a molecular link between neural stem cells and=20 medulloblastoma (4=969).=20 These developmentally significant signaling pathways are = attractive=20 therapeutic targets. For example, several groups have shown = that=20 pharmacologic inhibitors of Hh signaling block the = proliferation and=20 survival of medulloblastoma in vitro and in = vivo (10=9612).=20 Such therapeutic advances are clearly needed, as current = embryonal=20 brain tumor treatments are associated with significant side = effects=20 and often do not result in cures (13=9615).=20

In addition to arising from stem or precursor cells, = medulloblastoma=20 may also contain functionally important subsets of cells with = stem-like properties. It has recently been hypothesized that = in=20 many types of cancer, including medulloblastoma, such stem-like = cells=20 are uniquely capable of propagating tumor growth (16=9618).=20 This "cancer stem cell" hypothesis is based, in part, on = paradigms=20 explaining the development and repair of normal organs, in = which=20 only stem cells are thought to have a long-term capacity for=20 self-renewal and are therefore necessary for the generation = and=20 regeneration of tissues. Experimental support for the existence = of a=20 discrete cancer cell subpopulation required for tumor propagation=20 initially came from clonogenic assays, which showed that only = a=20 small portion of tumor cells could form colonies in vitro = or=20 engraft in vivo (19=9621).=20 Only recently the prospective isolation of cells uniquely = capable of=20 propagating neoplasms has been achieved, providing firmer = support for=20 the presence of cancer stem cells (22,=20 23).=20 This has been made possible by the characterization of = markers that=20 identify stem-like cells in tumor specimens. Two such = markers, CD133=20 and side population, have been used to prospectively isolate = a small=20 percentage of cells in brain tumors uniquely able to generate = tumor=20 neurospheres and xenografts (24=9627).=20 Interestingly, both markers were initially identified in=20 nonneoplastic stem cells (28=9631),=20 highlighting the similarities between normal and malignant = stem=20 cells.

To date, no agent has been shown to target the cancer stem cell=20 subpopulation in solid tumors. However, similarities in the=20 growth characteristics and gene expression patterns of benign = neural stem cells and brain tumor stem cells suggest that the = same signaling pathways may be required for survival and = growth=20 in both (18,=20 32=9635).=20 Notch is known to promote the survival and proliferation of=20 nonneoplastic neural stem cells and to inhibit their = differentiation=20 (36,=20 37).=20 Signaling is initiated by ligand binding, followed by = intramembranous=20 proteolytic cleavage of the Notch receptor by the 3D{gamma}=20-secretase=20 complex. Inhibitors of this complex slow the growth of=20 Notch-dependent tumors such as medulloblastoma and T-cell = leukemia=20 (8,=20 9,=20 38).=20 We therefore used a potent small-molecule 3D{gamma}=20-secretase=20 inhibitor to further investigate the role for Notch signaling = in=20 medulloblastoma, comparing the effects on overall tumor cell = mass to=20 those on cells expressing stem-like markers. Our data = indicate that=20 stem-like brain tumor cells may be especially vulnerable to = attacks=20 on molecular pathways, such as Notch, which are required in=20 their nonneoplastic cognate cells.


3D"   =20 Materials and Methods
Top
Abstract
Introduction
3D"Materials and = Methods
Results
Discussion
References
 
<= B>Cell=20 culture. The DAOY, PFSK, D283Med, and D425Med cell lines = were=20 obtained from the American Type Culture Collection and = maintained in=20 MEM (Invitrogen, Carlsbad, CA) supplemented with 10% fetal = bovine=20 serum (FBS) unless otherwise noted. Cell pools and stable = subclones=20 transfected with Notch2 intracellular domain (NICD2) were = generated=20 as previously described, and, unless otherwise noted, the = DAOY:NICD2=20 subclone used is the same as the one previously reported (8).=20 The low-passage medulloblastoma line MB2 was derived from a = tumor=20 resected at Johns Hopkins Hospital and analyzed at passage 8 = to 9. It=20 was finely minced, triturated, and maintained in MEM with 10% = FBS.=20 For treatment studies, cells were plated and allowed to grow=20 overnight in medium containing 10% FBS; then medium was = replaced the=20 next morning with low-serum (0.5% FBS) MEM containing -secretase inhibitor dissolved in DMSO at the = concentrations=20 indicated. RNA and protein extractions and all cell-based = assays were=20 done 48 hours after drug application unless otherwise noted. = All=20 experiments with error bars were done in triplicate and shown = as mean values with SE unless otherwise noted. Cell mass was=20 measured using CellTiter assays according to the instructions = of the manufacturer (Promega, Madison, WI). Cell number and=20 viability were assessed using the Guava PCA and Viacount = reagent=20 according to instructions (Guava Technologies, Heyward, CA).=20 Soft-agar assays were done as previously described, with = colonies=20 counted using an automated reader (8).=20

3D{gamma}-Secretase inhibitor synthesis. The potent 3D{gamma}=20-secretase=20 inhibitor=20 [11-endo]-N-(5,6,7,8,9,10-hexahydro-6,9-methanobenzo[= a][8]annulen-11-yl)-thiophene-2-sulfonamide=20 was listed as compound 18 in the recent report by Lewis et = al.=20 (39)=20 describing its synthesis and testing, and we refer to it as = GSI-18.=20 It was synthesized as previously described (39)=20 and its identity and quality were confirmed by nuclear = magnetic=20 resonance and mass spectral analysis. The biological activity = of this inhibitor against 3D{gamma}=20-secretase was=20 confirmed using in vitro and cell-based assays as = previously=20 described (40).=20

Immunocytochemistry. The cell lines DAOY and MB2 were = seeded=20 in 12-well tissue culture plates and allowed to adhere = overnight.=20 After treating with 2 =B5mol/L GSI-18 for 48 hours, cells = were=20 washed with PBS and fixed using 4% paraformaldehyde solution = in PBS=20 at room temperature for 30 minutes. Cells were then permeabilized=20 with 0.4% Triton X-100 in PBS for 5 minutes at room = temperature,=20 washed with PBS, and incubated in 5% bovine serum albumin = (BSA)-PBS=20 for 1 hour and then in 1:1,000 anti-nestin antibody = (Chemicon,=20 Temecula, CA) or 1:500 anti=96cleaved caspase-3 (Cell = Signaling=20 Technology, Beverly, MA) in 1% BSA-PBS for 2 hours. After = washing=20 with PBS, a final 60-minute incubation with a 1:300 dilution = of=20 Cy3-conjugated goat anti-mouse and Cy2-conjugated goat anti-rabbit=20 secondary antibodies (Jackson ImmunoResearch Laboratories, = West=20 Grove, PA) diluted in PBS containing 1% BSA was done. After=20 washing with PBS, cells were then counterstained with=20 4',6-diamidino-2-phenylindole (Vector Laboratories, = Burlingame, CA),=20 mounted, and visualized with fluorescence microscope (Zeiss, = Jena,=20 Germany). In the single-immunolabeling study (Fig.=20 6A and C), six high-power fields of DAOY = cultures=20 containing 147 to 333 (mean, 193) cells were photographed and = the=20 percentages of cells positive for nestin were scored in a = blinded=20 fashion. In the double-immunolabeling study (Fig.=20 6D-F), 10 high-power fields were photographed and=20 counted.



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  		Figure = 6.=20 Nestin-positive cells are especially sensitive to Notch = pathway=20 blockade. A, the fraction of DAOY cells expressing = high=20 levels of nestin is lower after GSI-18 exposure and higher = in a=20 subclone expressing activated Notch2 (NICD2). B and = C,=20 similar effects are seen following Notch blockade in the = low-passage=20 medulloblastoma cell line MB2. D to F, double=20 immunolabeling was used assess both differentiation status = (nestin)=20 and apoptosis (cleaved caspase-3) in DAOY cultures. = Significant=20 induction of cleaved caspase-3=96positive apoptotic cells = following=20 Notch blockade was limited to the nestin-positive = subpopulation.=20 G, overall apoptotic induction in DAOY cultures was = similar=20 when measured by counts of cleaved caspase-3 = immunofluorescent=20 (IF) cells or flow cytometric analysis of Annexin. *, = P < 0.01; ** P, < 0.001 (t = tests);=20 ns, not significant. =

 = ;
Flow=20 cytometric analyses. Flow cytometric analysis of S-phase = fraction=20 and cell cycle kinetics was done following fixation and = staining with=20 propidium iodide using a FACSCalibur (Becton Dickinson, San = Jose, CA)=20 with CELL Quest version 3.3 software (8).=20 CD133 studies were done using the same instrument, with = antibodies=20 from Miltenyi Biotec (Auburn, CA) according to the = instructions of=20 the manufacturer. In brief, cells were blocked in Fc receptor = blocking reagent and incubated with CD133/1 (AC133)-phycoerythrin=20 antibody (Miltenyi Biotec) for 10 minutes in the dark at = 4=B0C.=20 Then cells were washed and resuspended in 500 =B5L buffer = (PBS=20 containing 0.5% BSA and 2 mmol/L EDTA). Cells expressing = levels of=20 CD133 higher than those seen in immunoglobulin G (IgG) = controls were=20 considered positive. Experiments measuring CD133 were = repeated two to=20 three times for each line and error bars represent the mean = and SD.=20 For analyses of side population, cells (106/mL) = were=20 incubated with Hoechst 33342 (3 =B5mol/L; Molecular Probes, = Carlsbad,=20 CA) for 90 minutes at 37=B0C in DMEM containing 2% FBS. = Before=20 analysis, cells were washed and resuspended in 2 =B5g/mL = propidium=20 iodide (Sigma, St. Louis, MO). Cells were analyzed on a LSR = flow=20 cytometer equipped with 424/44-nm band pass and 670-nm long = pass=20 optical filters (Omega Optical, Brattleboro, VT). To ensure = proper=20 identification of side population cells, cells were incubated = as=20 above with the addition of 50 =B5mol/L verapamil = (Sigma).

Real-time reverse transcription-PCR. Quantitative reverse=20 transcription-PCR (RT-PCR) for Notch1, Notch2, and Hes1 was = done as=20 previously described (31),=20 with all reactions normalized to actin (Applied Biosystems, = Foster=20 City, CA). Commercially available Assay on Demand TaqMan = primers and=20 probes were used to measure mRNA for Tuj1 and the 3D{alpha}=206=20 subunit of the 3D{gamma}=20-aminobutyric=20 acid type A receptor (GABRA6). Each quantitative RT-PCR = reaction was=20 done in triplicate and error bars represent SE.

Protein analysis. Western blots contained 20 =B5g of = protein=20 per lane on a 10% Tris-glycine SDS-PAGE gel (Invitrogen) and=20 electrophoresing for several hours in 1x=20 TG-SDS buffer (Amresco, Solon, OH). Proteins were transferred = to=20 0.45-=B5m Optitran nitrocellulose (Schleicher & Schuell, = Keene, NH)=20 in 1x Tris-glycine buffer = (Amresco). Blots were blocked in PBS containing 5% nonfat dry = milk=20 powder and incubated overnight at 4=B0C with antibodies = directed=20 against Hes1 (kind gift of Dr. Tetsuo Sudo, Toray Industries, = Tebiro,=20 Kamakura, Japan; 1:2,000) or glyceraldehyde-3-phosphate = dehydrogenase=20 (Research Diagnostics, Flanders, NJ; 1:20,000). Blots were = then=20 washed several times with PBS containing 0.1% Tween 20 and = incubated=20 in peroxidase-conjugated IgG diluted 1:2,000 in blocking = solution.=20 After washing several times in PBS with 0.1% Tween 20, blots = were=20 developed with enhanced chemiluminescence reagent (Pierce, = Rockford,=20 IL) and exposed to film.

Statistical analysis. Statistical analyses were done using=20 GraphPad Prism 4 (GraphPad Software, San Diego, CA). Data = graphed=20 with error bars represent mean and SE from experiments done = in=20 triplicate unless otherwise noted. A two-sided Student's = t=20 test was used to determine the significance of any = differences.=20


3D"   =20 Results
Top
Abstract
Introduction
Materials and Methods
3D"Results
Discussion
References
 
<= B>Growth=20 of medulloblastoma cultures is slowed but not arrested by = Notch=20 blockade. Experiments were done using GSI-18, a potent = -secretase inhibitor with a sulfonamide core (39).=20 We first sought to determine what concentration of GSI-18=20 effectively inhibited Notch activity in tumor cells by = measuring=20 expression of the pathway target Hes1. GSI-18 at 2 =B5mol/L=20 reduced both mRNA and protein levels of Hes1 in DAOY cells by = >70% (Fig.=20 1A and B ), suggesting that this concentration = should=20 be sufficient to cause antitumor effects mediated by Notch = pathway=20 inhibition. GSI-18 levels <0.4 =B5mol/L did not affect = Hes1=20 mRNA expression (data not shown).



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  		Figure = 1. Notch=20 inhibition slowed growth of embryonal brain tumor cells. = A,=20 Hes1 mRNA levels, measured using quantitative RT-PCR and = normalized=20 to actin expression, are decreased by 0.4 =B5mol/L or higher = levels of=20 GSI-18. B, Hes1 protein levels are also reduced after = 48-hour=20 exposure to GSI-18. C, growth of DAOY viable cell = mass over 2=20 days is slowed in a dose-dependent fashion by GSI-18. = D,=20 NICD2 expression in a stable subclone rescues the growth = inhibition=20 caused by GSI-18. E, DAOY cells are less numerous and = smaller=20 after 2 days of Notch blockade; bar, 100 =B5m. F, the = number of=20 viable cells, expressed as a fraction of vehicle-treated = cultures,=20 is reduced after 48 hours of Notch pathway blockade in all = four=20 medulloblastoma/PNET cell lines tested. G, flow = cytometric=20 analysis of DAOY and PFSK cultures after 48 hours of 2 = =B5mol/L GSI-18=20 exposure revealed increases in the percentage of cells in=20 G1/G0 and decreases in the S and=20 G2-M fractions, graphed as percent change from = cells=20 treated with DMSO alone. H, expression of mRNAs = encoding the=20 neuronal markers Tuj1 and GABRA6 are induced by the 3D{gamma}=20-secretase inhibitor GSI-18; nd, not = detected. =

 = ;
Notch=20 pathway inhibition using GSI-18 slowed the growth of DAOY=20 medulloblastoma cultures. The increase in viable cell mass = over=20 2 days was reduced in a dose-dependent fashion by GSI-18 (Fig.=20 1C) but many tumor cells survived Notch pathway = inhibition=20 and continued to proliferate over this period. JC2, a -secretase inhibitor with a benzodiazepine core, = also slowed=20 but did not arrest growth in medulloblastoma cell mass when = used at=20 concentrations that effectively inhibited the Notch pathway,=20 indicating the findings were not specific to one structural = class of=20 compound (data not shown). DAOY cells stably transfected with = a NICD2=20 were used to further control for the specificity of the=20 pharmacologic effects. This truncated Notch receptor does not = require=20 ligand binding or 3D{gamma}=20-secretase=20 activity for nuclear translocation and signaling, and cells=20 expressing it should be insensitive to effects of GSI-18 = mediated by=20 Notch2 inhibition. NICD2 expression in a stable subclone we = have=20 previously described (8)=20 rescued the negative effects on DAOY cell mass (Fig.=20 1D). A second stable subclone, as well as a pool = of cells=20 into which NICD2 was introduced by transfection, was also = resistant=20 to the growth-inhibiting effects of GSI-18 (data not shown),=20 suggesting that this compound acts through Notch and not = other=20 pathways regulated by 3D{gamma}=20-secretase.=20

It has previously been reported that in pre-T cells, = down-regulation=20 of Notch activity reduces cellular metabolism and cell size = (41).=20 We also observed decreased cell size in medulloblastoma = cultures=20 following GSI-18 exposure (Fig.=20 1E). To rule out the possibility that our = measurements of=20 viable cell mass bioreductive capacity (CellTITER assay) were = being=20 altered by metabolic affects of Notch, we quantitated cell = number=20 using flow cytometry. The number of live cells in DAOY, = D283Med,=20 D425Med, and PFSK cultures exposed to 2 =B5mol/L GSI-18 for = 48 hours=20 was reduced as compared with vehicle-treated controls, but = the=20 reduction was less than that of cell mass (Fig.=20 1F). Thus, measures of both cell mass and cell = number show=20 a slowing, but not an arrest, of tumor growth under = conditions of=20 Notch blockade.

Decreased proliferation and increased neuronal = differentiation=20 following Notch inhibition. Flow cytometric analysis = showed=20 that 2 =B5mol/L GSI-18 increased the G1-G0 = cell=20 fraction and decreased the S-phase and G2-M = fractions of=20 DAOY and PFSK cell lines (Fig.=20 1G), suggesting that cell cycle exit likely plays = a role=20 in its antigrowth effects. Notch pathway down-regulation has = also=20 been linked to cellular differentiation in both normal = development=20 and in neoplasms (42,=20 43)=20 and we therefore examined whether Notch inhibition caused = cellular=20 differentiation. 3D{gamma}=20-Secretase=20 inhibition in DAOY cells increased RNA levels of two markers = of=20 cerebellar neuronal differentiation, Tuj1 and GABRA6, in a=20 dose-dependent fashion (Fig.=20 1H). One of these neuronal markers, GABRA6, is=20 specifically found in cerebellar granule cells in the brain, = where=20 its expression is induced as they mature (44).=20 Its induction after Notch pathway inhibition suggests that = the=20 differentiation pathway being actuated resembles that in = normal=20 cerebellar granule neuron precursors, and highlights the = similarities=20 between the DAOY line and developing cerebellum.

Notch blockade by 3D{gamma}=20-secretase=20 inhibitors suppresses tumor formation. We next examined = the=20 effects of Notch pathway blockade on tumor formation in = vitro=20 and in vivo. We first used a clonogenic assay to = determine=20 whether cells capable of forming anchorage-independent = colonies were=20 depleted by GSI-18. Vehicle-treated DAOY cultures seeded in = soft agar=20 formed 50 colonies per field on average (Fig.=20 2 ). This number dropped to 4 when an equal number of = viable=20 cells was counted and seeded after 48 hours of treatment with = GSI-18=20 and increased to 119 in the presence of constitutive Notch2=20 activation. Thus, whereas many tumor cells continued to grow = in 2=20 =B5mol/L GSI-18, their clonogenicity in soft agar was = suppressed by=20 >90%.



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  		Figure = 2. Notch=20 signaling is required for the formation of colonies in = soft-agar.=20 Forty-eight hours of exposure to 2 =B5mol/L GSI-18 before = seeding in=20 soft agar significantly reduced clonogenic potential of DAOY = cells.=20 This effect could be rescued by NICD2 expression in a stable = subclone (**, P < 0.001). =

 = ;
To=20 determine the effects of Notch blockade on the formation of = tumor=20 xenografts, DAOY and DAOY:NICD2 cultures were treated with = either 2=20 =B5mol/L GSI-18 in DMSO or DMSO alone, and the viable cells = remaining=20 after 48 hours were counted using trypan blue. Five hundred = thousand=20 viable cells from each group were then mixed with Matrigel = and=20 injected s.c. in athymic (nude) mice. Large xenografts formed = at the=20 sites of all 12 control injections, including vehicle-treated = DAOY=20 cells (n =3D 4; Fig.=20 3A ), vehicle-treated DAOY:NICD2 cells (n = =3D 4), and=20 GSI-18-treated DAOY:NICD2 cells refractory to Notch = inhibition=20 (n =3D 4). In contrast, only one very small lesion = formed among=20 the four sites injected with 500,000 DAOY cells that had been = pretreated with 2 =B5mol/L GSI-18, suggesting that while = viable, the=20 cancer cells were no longer tumorigenic (Fig.=20 3B and C). To rule out the possibility that = cells=20 were alive but moribund following 3D{gamma}=20-secretase=20 inhibition, the experiment was repeated with cells counted = after a=20 recovery period. After 2 days of treatment, followed by 24 = hours of=20 recovery in medium containing 10% FBS and no 3D{gamma}=20-secretase=20 inhibitor, both GSI-18-treated and vehicle-treated cells = proliferated=20 at similar rates, suggesting that any overall effects on = growth had=20 normalized (Fig.=20 3D). When equal numbers of these "recovered" cells = were=20 injected into mice, GSI-18-treated cultures were still unable = to form=20 tumors (n =3D 4) whereas bulky tumor xenografts formed = in all 12=20 controls. D425Med and D283Med cells also failed to engraft = (n=20 =3D 2 animals D425Med, n =3D 3 animals D283Med) when = pretreated=20 for 48 hours with GSI-18, whereas vehicle-treated cells = injected on=20 the contralateral flank formed large tumors at all but one = site (Fig.=20 3E).



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  		Figure = 3. Notch=20 pathway inhibition blocks xenograft formation. A to = C,=20 bulky xenografts developed at all 12 sites injected with = cells in=20 which Notch signaling was active. This included = vehicle-treated DAOY=20 (n =3D 4), vehicle-treated DAOY:NICD2 (n =3D = 4), and 2=20 =B5mol/L GSI-18=96treated DAOY:NICD2 (n =3D 4; = A). Viable=20 cells remaining following Notch blockade with 2 =B5mol/L = GSI-18 formed=20 a tumor mass (B) at only one of four injection sites. = D, after recovering for 24 hours in media containing = 10% FBS,=20 GSI-18- and vehicle-treated cultures have identical = proliferation=20 rates as determined by flow cytometric analysis of S-phase = fraction=20 (inset). Nevertheless, cells that had experienced = Notch=20 pathway blockade were still unable to efficiently form = tumors, with=20 small lesions developing at only two of four injection = sites. As=20 before, large xenografts formed at all 12 control sites. = E,=20 D425Med cells treated with GSI-18 for 48 hours also failed = to=20 generate xenografts (arrow) whereas vehicle-treated = cells=20 always did (asterisk). F and G, in vivo = administration of GSI-18 i.p. for 5 days after s.c. tumor = injection=20 also blocked engraftment of DAOY (arrow) but not of=20 DAOY:NICD2 (asterisk). =

 = ;
As=20 a test of the requirement for ongoing Notch activity during = tumor=20 engraftment, we treated animals with GSI-18 after s.c. = injections of=20 DAOY and DAOY:NICD2 cells into their left and right flanks. A = treatment group of four animals received i.p. injections = containing=20 0.5 mg GSI-18 in DMSO for 5 consecutive days, beginning on = the day of=20 xenograft initiation, whereas the control group was treated = with=20 vehicle alone. DAOY cells failed to engraft in three of the = four=20 GSI-18-treated animals whereas vehicle-treated animals all = developed=20 tumors (Fig.=20 3F and G). Tumors also developed in both = vehicle-=20 and GSI-18-treated animals at sites of DAOY:NICD2 injection. = No=20 behavioral or physical changes were noted in the animals = treated with=20 GSI-18.

Notch regulates the percentage of medulloblastoma cells = expressing=20 stem/precursor markers. The data presented above suggest = that=20 while viable and proliferative following Notch pathway = blockade,=20 medulloblastoma cultures are altered in some way, blocking = their=20 ability to form soft-agar colonies and tumor xenografts. It = has=20 been shown that stem-like "side-populations" in established = brain=20 tumor cell lines are uniquely able to form xenografts (25,=20 26).=20 Thus, cancer stem cells seem to be able to persist in = established=20 brain tumor lines maintained for many years in culture. = Because=20 stem-like tumor cells are thought to be critical for = xenograft=20 formation, we sought to determine if this subpopulation might = be=20 especially sensitive to Notch pathway blockade.

We first examined the requirement for ongoing Notch activity = in=20 CD133-positive cells. Singh et al. (24,=20 33)=20 have shown that only CD133-positive medulloblastoma and = glioblastoma=20 brain tumor cells are able to form multipotent neurosphere = clones or=20 tumor xenografts. Another type of brain tumor, ependymoma, = also=20 seems to contain a small fraction of CD133-positive cells=20 uniquely capable of engrafting in immunocompromised mice (27).=20 In the adherent embryonal brain tumor cell lines DAOY and = PFSK,=20 flow cytometric analysis revealed that 9.9% and 10.8% of = cells,=20 respectively, expressed CD133 on their surface (Fig.=20 4A and B ). These CD133-positive fractions = fell=20 within the 6.1% to 45.4% range (mean, 19.7%) reported in = primary=20 medulloblastoma (33).=20 The D283Med and D425Med lines, which have elevated c-Myc = levels and=20 grow in suspension, contained higher percentages of = CD133-positive=20 cells. Sorting of DAOY and PFSK cultures generated = populations=20 enriched 3D~3-fold for cells expressing CD133 and negative = fractions in=20 which <1% of cells were CD133 positive. Interestingly, = mRNA levels=20 of Hes1, a marker of Notch pathway activity, were elevated=20 4-fold in the CD133-enriched fraction of DAOY and 5-fold in = the=20 CD133-enriched fraction of PFSK (Fig.=20 4C). This suggests that Notch signaling is = especially=20 active in stem-like cancer cells and supports the possibility = that=20 Notch pathway inhibition may target this population. =



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  		Figure = 4. The=20 CD133-positive population in medulloblastoma is regulated by = Notch.=20 A, flow cytometric analysis was used to define the = population=20 of cells with CD133 expression elevated above the highest = level of=20 background fluorescence (dashed line). Cultures were=20 evaluated following 48-hour exposure to either 2 =B5mol/L = GSI-18 or=20 vehicle. B, the CD133-positive subpopulation in all = four=20 medulloblastoma/PNET lines examined was reduced by 2 = =B5mol/L GSI-18=20 (*, P < 0.01). Constitutive activation of Notch2 = in a pool=20 of DAOY cells transfected with NICD2 (P) as well as = in two=20 stable subclones (C1 and C2) rendered the=20 CD133-expressing subpopulation insensitive to 3D{gamma}=20-secretase inhibitor. C, Hes1 mRNA levels = were=20 elevated in CD133-enriched preparations as compared with=20 CD133-depleted ones, suggesting Notch activity is higher in=20 stem-like cells. =

 = ;
Gain=20 or loss of Notch pathway activity modulated the size of the=20 CD133-expressing stem-like subpopulation (Fig.=20 4B). This fraction was elevated from 9.9% to = >17% in a=20 pool of DAOY cells transfected with a plasmid encoding the=20 constitutively active NICD2 and in two stable subclones = derived from=20 such a pool. In contrast, Notch pathway inhibition using = GSI-18=20 reduced the CD133-positive stem-like fraction 3-fold to 3.3%=20 (P < 0.01). As expected, NICD2 expression rescued = the=20 effects of GSI-18 on the CD133-positive cell fraction. A = 4.8-fold=20 reduction in the percentage of CD133-positive cells seen in = PFSK=20 cultures was also statistically significant (P < = 0.01).=20 Decreases in the stem-like fraction were also observed in the = D283Med and D425Med lines but were less pronounced. =

Side population was analyzed to obtain a second measure of the=20 effects of Notch on stem-like tumor cells. DAOY cultures = contained=20 a Hoechst 33342=96excreting side population of 1.9% (Fig.=20 5A ). The multiple drug resistance pumps mediating = dye=20 efflux are verapamil sensitive (28),=20 and adding verapamil to the medulloblastoma culture abolished = Hoechst=20 excretion, verifying that this was a bona fide side = population.=20 Consistent with our hypothesis that Notch activity regulates=20 stem-like cancer cells, constitutive activation of Notch2 = increased=20 the side population almost 4-fold to 7.3%, whereas Notch = inhibition=20 essentially ablated it, with only 0.01% of remaining cells = negative=20 for dye (Fig.=20 5A and B). NICD2 expression protected the = side=20 population from GSI-18 exposure, but not from verapamil, = indicating=20 that the effect of GSI-18 was specifically mediated through = its=20 effects on Notch signaling. Small side populations were also = present=20 in the PFSK, D283Med, and D425Med cell lines and were ablated = by both=20 verapamil (data not shown) and 2 =B5mol/L GSI-18 (Fig.=20 5B). Thus, Notch pathway blockade depletes the = stem-like=20 subpopulation defined either by CD133 or by side = population.=20



View = larger=20 version (40K):
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  		Figure = 5. Notch=20 blockade ablates side population. A, a = verapamil-sensitive=20 side population is present in DAOY cultures and is ablated = by GSI-18=20 treatment. NICD2 expression in a stable subclone increases = the size=20 of the side population almost 4-fold and rescues the effects = of the=20 3D{gamma}=20-secretase inhibitor. B, similar effects = are seen in=20 PFSK, D283Med, and D425Med medulloblastoma lines. =

 = ;
Notch=20 blockade induces apoptosis in nestin-positive medulloblastoma=20 cells. We next examined if stem or progenitor-like cells=20 expressing nestin might be especially prone to apoptosis = following=20 Notch pathway blockade. Expression of the intermediate = filament=20 nestin was used to directly visualize poorly differentiated=20 cells, as CD133 immunofluorescence was too dim to reliably = score=20 by eye. Nestin mRNA levels were not significantly elevated in = CD133-enriched DAOY populations, suggesting that the two = markers are=20 not equivalent (data not shown). This is not unexpected, as = Lee et=20 al. (45)=20 also found that only 20% of CD133-positive cells in the = postnatal=20 cerebellum also expressed nestin. Nevertheless, nestin was = one=20 of the first markers of neural stem cells to be identified (46)=20 and its expression has been shown in a subset of cells within = neurospheres derived from primary human medulloblastoma, = suggesting=20 it marks stem-like cells in these tumors (32,=20 33).=20 We detected nestin protein in both established (DAOY) and = low-passage=20 (MB2) medulloblastoma cultures. Nestin staining was present = in=20 the cytoplasm and was variable in intensity, with only 10% of = DAOY cells expressing high levels whereas almost half of MB2=20 cells were strongly nestin positive (Fig.=20 6A and B ). We reasoned that = medulloblastoma cells=20 expressing high levels of nestin might represent a stem-like=20 subpopulation and we therefore correlated their percentage = with=20 varying levels of Notch activity. In DAOY cells, constitutive = Notch2=20 activation up-regulated the strongly nestin-positive fraction = of=20 cells almost 5-fold to 47.7% (P < 0.001) whereas = Notch=20 blockade using the 3D{gamma}=20-secretase=20 inhibitor GSI-18 reduced this population 4-fold to 2.4% = (P=20 < 0.01; Fig.=20 6C). A significant reduction was also observed in MB2 = cells=20 following Notch blockade.

We used double immunofluorescence to study cell death in = medulloblastoma=20 cells positive or negative for nestin. The basal apoptotic = rate=20 was measured using antibodies specific for cleaved caspase-3. = In DAOY cultures to which vehicle was added for 48 hours, the = apoptotic rate was low in both nestin-negative (26 of 1,841;=20 1.4%) and nestin-positive (4 of 160; 2.5%) cells (Fig.=20 6D-F). However, after 48 hours of treatment with 2 = =B5mol/L=20 GSI-18, the apoptotic rate increased to 37% in the = nestin-positive=20 population (23 of 62 cells) whereas apoptosis in the=20 better-differentiated cells lacking nestin only increased to = 3.9% (40=20 of 1,017 cells). Interestingly, nestin was less evenly = distributed in=20 the apoptotic cells and was sometimes observed surrounding = the=20 degenerating nuclei. Such cagelike perinuclear nestin = staining has=20 been previously described in mitotic cells (47).=20 Our immunofluorescent assessment of cell death using cleaved=20 caspase-3 corresponds relatively well to apoptotic induction = measured=20 by flow cytometric analysis of Annexin staining, suggesting = that our=20 manual counting procedure is accurate (Fig.=20 6G). Taken together, these data indicate that the = survival=20 of stem-like tumor cells is more sensitive to Notch pathway=20 inhibition than the survival of better-differentiated = cells.=20


3D"   =20 Discussion
Top
Abstract
Introduction
Materials and Methods
Results
3D"Discussion
References
 
I= n this=20 study, we examined the effects of Notch pathway inhibition on = the=20 growth and xenograft formation of medulloblastoma. We found = that=20 Notch blockade using the 3D{gamma}=20-secretase=20 inhibitor GSI-18 slowed the growth of tumor cells in = vitro but=20 had a much more dramatic effect on the formation of colonies = in soft=20 agar and tumor xenografts in nude mice. Indeed, our most = striking=20 finding was that large numbers of viable, rapidly = proliferating=20 cells were not able to generate bulky xenografts if they had=20 previously been treated with GSI-18, whereas equal numbers of = vehicle-treated cells always formed large tumors. Systemic = (i.p.)=20 treatment of animals with GSI-18 also blocked xenograft = formation=20 with no apparent side effects, indicating this agent may be=20 effective therapeutically in preventing tumor metastasis or = regrowth=20 following debulking. We believe that these dramatic effects = on tumor=20 propagation are mediated by depletion of cancer stem cells, = as=20 subpopulations expressing the stem cell marker CD133, as well = as the=20 stem-like side population, were profoundly reduced by Notch=20 blockade. These results must be extended to primary tumors or = additional low-passage lines and might provide a first = indication=20 that stem-like cells can be successfully ablated from brain=20 tumors.

The targeted depletion of stem-like cells we observe following=20 Notch pathway blockade contrasts sharply with prior reports = of=20 cancer stem cell survival following standard chemotherapies. = For=20 example, Wulf et al. (48)=20 showed higher efflux of chemotherapeutic agents and better = survival=20 in leukemic side population cells as compared with non-side=20 population cells. Based on this and on similar studies, it = has been=20 suggested that the efflux pumps which define side population = also=20 function to remove toxic chemotherapy drugs from cancer stem = cells=20 (reviewed in refs. 49,=20 50).=20 In support of this concept, treatment of neuroblastoma cell=20 lines with mitoxantrone actually increases the side = population,=20 suggesting that stem-like cancer cells are relatively = resistant to=20 this chemotherapeutic agent and accumulate as more=20 differentiated cells are killed (51).=20 Thus, conventional chemotherapies effectively remove the=20 better-differentiated cells while leaving most stem-like = cells alive.=20 In contrast, Notch blockade depletes stem-like cells but = leaves many=20 better-differentiated cells capable of limited growth = intact.=20

We examined only one type of malignant brain tumor in this = study,=20 but our findings may be applicable to other neoplasms as = well.=20 The Notch pathway is known to regulate stem cells in a wide=20 variety of tissues and Notch blockade seems to affect = survival=20 and proliferation of multiple types of cancer (52,=20 53).=20 For example, Notch is activated by translocation or mutation = in=20 >50% of T-cell acute lymphoblastic leukemia, and = anti-Notch=20 therapies have been shown to slow acute lymphoblastic = leukemia=20 growth in vitro (38).=20 Aberrantly activated Notch signaling has also been documented = in=20 lung, breast, salivary gland, and pancreatic carcinoma (54=9657).=20 3D{gamma}-Secretase inhibitors may therefore be useful in = targeting=20 stem-like cancer cells in a wide range of neoplasms. =

In the future, multiagent chemotherapeutic regimens may target=20 both stem-like and better-differentiated cells. Drugs = blocking=20 Notch signaling, or other pathways required in stem cells = such=20 as Wnt and Hedgehog, will be used to deplete the cancer stem=20 cell population, and traditional chemotherapeutic agents can = be=20 used at the same time to debulk the larger mass of tumor = cells. This=20 will effect a rapid removal of both subpopulations and might=20 circumvent the possibility that some differentiated tumor = cells can=20 dedifferentiate and repopulate the stem cell fraction (58).=20 Another potential complication of cancer stem cell=96directed = therapies=20 is that nonneoplastic stem cells may also be depleted by such = strategies. This is of particular concern in children who = will=20 presumably require stem cells for the maintenance and repair = of a=20 host of tissues over the course of their lives. Of note, we = found=20 that i.p. injections of GSI-18 for 5 days blocked tumor = formation=20 with no obvious ill effects on the animal's health over the=20 subsequent months. Indeed, it has recently been shown that = inhibition=20 of 3D{gamma}-secretase activity using small-molecule drugs can = actually=20 enhance long-term memory in rodents (59).=20

In summary, we show that in the malignant brain tumor = medulloblastoma,=20 Notch pathway blockade depletes a population of cells = required=20 for in vivo tumor formation by suppressing proliferation = and=20 inducing apoptosis or differentiation in stem-like cells. Our = data suggest that Notch pathway blockers may be the first of = a=20 new class of chemotherapeutic agents=97those targeting cancer = stem=20 cells.


3D"   =20 Acknowledgments =
 
Grant support:=20 Alzheimer's Association, Zenith Fellowship (Y-M. Li), NIH = grant=20 1R01AG026660-01, The Children's Cancer Foundation of = Baltimore,=20 Fellowship from the American Brain Tumor Association (X. = Fan),=20 Burroughs Wellcome Fund Career Award in the Biomedical = Sciences (C.G.=20 Eberhart), and NIH grant K08 NS43279.

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 Josh Copeland for assistance with Western blots, Dr.=20 Tetsuo Sudo for his generous gift of Hes1 antiserum, and Dr.=20 J.C. Zuniga-Pflucker for his suggestions on Notch inhibition=20 and cell size.

Received 3/13/06. Revised 5/17/06. Accepted 5/25/06.


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Discussion
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Z. Li, H. Wang, C. E. Eyler, A. B. Hjelmeland, and J. N. = Rich
Turning Cancer Stem Cells Inside Out: An = Exploration of=20 Glioma Stem Cell Signaling Pathways
J. Biol. Chem.,=20 June 19, 2009; 284(25): 16705 - 16709.
[Abstract]<= /A>=20 [Full = Text]=20 [PDF] =
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S. Puget, J. Grill, A. Valent, I. Bieche, C. = Dantas-Barbosa, A.=20 Kauffmann, P. Dessen, L. Lacroix, B. Geoerger, B. Job, et=20 al.
Candidate Genes on Chromosome 9q33-34 Involved = in the=20 Progression of Childhood Ependymomas
J. Clin. Oncol.,=20 April 10, 2009; 27(11): 1884 - 1892.
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M. E. Mullendore, J.-B. Koorstra, Y.-M. Li, G. J. = Offerhaus, X.=20 Fan, C. M. Henderson, W. Matsui, C. G. Eberhart, A. Maitra, and G. = Feldmann
Ligand-dependent Notch Signaling Is Involved = in Tumor=20 Initiation and Tumor Maintenance in Pancreatic = Cancer
Clin.=20 Cancer Res., April 1, 2009; 15(7): 2291 - 2301.
[Abstract]=20 [Full=20 Text] [PDF= ]=20
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J.N. Rich and C.E. Eyler
Cancer Stem Cells in = Brain=20 Tumor Biology
Cold Spring Harb Symp Quant Biol,=20 March 27, 2009; (2009) sqb.2008.73.060v1.
[Abstract]=20 [PDF]=20
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T. Shimizu, T. Kagawa, T. Inoue, A. Nonaka, S. Takada, = H.=20 Aburatani, and T. Taga
Stabilized {beta}-Catenin = Functions=20 through TCF/LEF Proteins and the Notch/RBP-J{kappa} Complex To = Promote=20 Proliferation and Suppress Differentiation of Neural Precursor=20 Cells
Mol. Cell. Biol., December 15, 2008; = 28(24):=20 7427 - 7441.
[Abstract]=20 [Full = Text]=20 [PDF] =
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T.J. Pierfelice, K.C. Schreck, C.G. Eberhart, and N.=20 Gaiano
Notch, Neural Stem Cells, and Brain=20 Tumors
Cold Spring Harb Symp Quant Biol,=20 November 19, 2008; (2008) sqb.2008.73.013v2.
[Abstract]=20 [PDF]=20
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B. A. Emmenegger and R. J. Wechsler-Reya
Stem = Cells and=20 the Origin and Propagation of Brain Tumors
J Child = Neurol,=20 October 1, 2008; 23(10): 1172 - 1178.
[Abstract= ]=20 [PDF] =
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L. Sang, H. A. Coller, and J. M. = Roberts
Control of the=20 Reversibility of Cellular Quiescence by the Transcriptional = Repressor=20 HES1
Science, August 22, 2008; 321(5892): = 1095 -=20 1100.
[Ab= stract]=20 [Full=20 Text] [PDF]=20
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B. T. Kawasaki, E. M. Hurt, T. Mistree, and W. L.=20 Farrar
Targeting Cancer Stem Cells with=20 Phytochemicals
Mol. Interv., August 1, 2008; = 8(4):=20 174 - 184.
= [Abstract]=20 [Ful= l=20 Text] [PDF]= =20
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X. Fan and C. G. Eberhart
Medulloblastoma = Stem=20 Cells
J. Clin. Oncol., June 10, 2008; = 26(17): 2821 -=20 2827.
[Abstrac= t]=20 [Full=20 Text] [PDF] =
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A. Ocana and A. Pandiella
Identifying Breast = Cancer=20 Druggable Oncogenic Alterations: Lessons Learned and Future = Targeted=20 Options
Clin. Cancer Res., = February 15, 2008; 14(4):=20 961 - 970.
[Abstract]=20 = [Full=20 Text] [PDF]= =20
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C. Tang, B. T. Ang, and S. Pervaiz
Cancer = stem cell:=20 target for anti-cancer therapy
FASEB J,=20 December 1, 2007; 21(14): 3777 - 3785.
[Abstract]= =20 [Full=20 Text] [PDF]=20
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J. N. Rich
Cancer Stem Cells in Radiation=20 Resistance
Cancer Res., October 1, 2007; = 67(19):=20 8980 - 8984.
[Abstract]=20 [F= ull=20 Text] [PDF]=20
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A. Khandelwal, D. Chandu, C. M. Roe, R. Kopan, and R. S. = Quatrano
Moonlighting activity of presenilin in plants = is=20 independent of {gamma}-secretase and evolutionarily=20 conserved
PNAS, August 14, 2007; 104(33): = 13337 -=20 13342.
[Abstract]= =20 [Full=20 Text] [PDF]=20
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F. Baliko, T. Bright, R. Poon, B. Cohen, S. E. Egan, and = B. A.=20 Alman
Inhibition of Notch Signaling Induces Neural=20 Differentiation in Ewing Sarcoma
Am. J. Pathol.,=20 May 1, 2007; 170(5): 1686 - 1694.
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F. Zindy, T. Uziel, O. Ayrault, C. Calabrese, M. = Valentine, J. E.=20 Rehg, R. J. Gilbertson, C. J. Sherr, and M. F. = Roussel
Genetic=20 Alterations in Mouse Medulloblastomas and Generation of Tumors De = novo=20 from Primary Cerebellar Granule Neuron = Precursors
Cancer Res.,=20 March 15, 2007; 67(6): 2676 - 2684.
[Abstract]=20 [Fu= ll=20 Text] [PDF]=20
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C. D. Peacock, Q. Wang, G. S. Gesell, I. M. = Corcoran-Schwartz, E.=20 Jones, J. Kim, W. L. Devereux, J. T. Rhodes, C. A. Huff, P. A. = Beachy,=20 et al.
Hedgehog signaling maintains a tumor = stem cell=20 compartment in multiple myeloma
PNAS, = March 6, 2007;=20 104(10): 4048 - 4053.
[Abstract]<= /A>=20 [Full = Text]=20 [PDF] =
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C.-Y. Lee, R. O. Andersen, C. Cabernard, L. Manning, K. = D. Tran,=20 M. J. Lanskey, A. Bashirullah, and C. Q. Doe
Drosophila = Aurora-A kinase inhibits neuroblast self-renewal by regulating = aPKC/Numb=20 cortical polarity and spindle orientation
Genes & = Dev.,=20 December 15, 2006; 20(24): 3464 - 3474.
[Abstr= act]=20 [Full=20 Text] [PDF] =
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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_01CAD4B9.3622F7A0 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 if (name =3D=3D "background-position") {=0A= e.style.backgroundPosition =3D value;=0A= }=0A= else if (name =3D=3D "background-position-x") {=0A= e.style.backgroundPositionX =3D value;=0A= }=0A= else if (name =3D=3D "background-position-y") {=0A= e.style.backgroundPositionY =3D value;=0A= }=0A= else if (name =3D=3D "background-repeat") {=0A= e.style.backgroundRepeat =3D value;=0A= }=0A= else if (name =3D=3D "behavior") {=0A= e.style.behavior =3D value;=0A= }=0A= else if (name =3D=3D "border") {=0A= e.style.border =3D value;=0A= }=0A= else if (name =3D=3D "border-bottom") {=0A= e.style.borderBottom =3D value;=0A= }=0A= else if (name =3D=3D "border-bottom-color") {=0A= e.style.borderBottomColor =3D value;=0A= }=0A= else if (name =3D=3D "border-bottom-style") {=0A= e.style.borderBottomStyle =3D value;=0A= }=0A= else if (name =3D=3D "border-bottom-width") {=0A= e.style.borderBottomWidth =3D value;=0A= }=0A= else if (name =3D=3D "border-collapse") {=0A= e.style.borderCollapse =3D value;=0A= }=0A= else if (name =3D=3D "border-color") {=0A= e.style.borderColor =3D value;=0A= }=0A= else if (name =3D=3D "border-left") {=0A= e.style.borderLeft =3D value;=0A= }=0A= else if (name =3D=3D "border-left-color") {=0A= e.style.borderLeftColor =3D value;=0A= }=0A= else if (name =3D=3D "border-left-style") {=0A= e.style.borderLeftStyle =3D value;=0A= }=0A= else if (name =3D=3D "border-left-width") {=0A= e.style.borderLeftWidth =3D value;=0A= }=0A= else if (name =3D=3D "border-right") {=0A= e.style.borderRight =3D value;=0A= }=0A= else if (name =3D=3D "border-right-color") {=0A= e.style.borderRightColor =3D value;=0A= }=0A= else if (name =3D=3D "border-right-style") {=0A= e.style.borderRightStyle =3D value;=0A= }=0A= else if (name =3D=3D "border-right-width") {=0A= e.style.borderRightWidth =3D value;=0A= }=0A= else if (name =3D=3D "border-style") {=0A= e.style.borderStyle =3D value;=0A= }=0A= else if (name =3D=3D "border-top") {=0A= e.style.borderTop =3D value;=0A= }=0A= else if (name =3D=3D "border-top-color") {=0A= e.style.borderTopColor =3D value;=0A= }=0A= else if (name =3D=3D "border-top-style") {=0A= e.style.borderTopStyle =3D value;=0A= }=0A= else if (name =3D=3D "border-top-width") {=0A= e.style.borderTopWidth =3D value;=0A= }=0A= else if (name =3D=3D "border-width") {=0A= e.style.borderWidth =3D value;=0A= }=0A= else if (name =3D=3D "bottom") {=0A= e.style.bottom =3D value;=0A= }=0A= else if (name =3D=3D "clear") {=0A= e.style.clear =3D value;=0A= }=0A= else if (name =3D=3D "clip") {=0A= e.style.clip =3D value;=0A= }=0A= else if (name =3D=3D "color") {=0A= e.style.color =3D value;=0A= }=0A= else if (name =3D=3D "cssText") {=0A= e.style.Sets =3D value;=0A= }=0A= else if (name =3D=3D "cursor") {=0A= e.style.cursor =3D value;=0A= }=0A= else if (name =3D=3D "direction") {=0A= e.style.direction =3D value;=0A= }=0A= else if (name =3D=3D "display") {=0A= e.style.display =3D value;=0A= }=0A= else if (name =3D=3D "font") {=0A= e.style.font =3D value;=0A= }=0A= else if (name =3D=3D "font-family") {=0A= e.style.fontFamily =3D value;=0A= }=0A= else if (name =3D=3D "font-size") {=0A= e.style.fontSize =3D value;=0A= }=0A= else if (name =3D=3D "font-style") {=0A= e.style.fontStyle =3D value;=0A= }=0A= else if (name =3D=3D "font-variant") {=0A= e.style.fontVariant =3D value;=0A= }=0A= else if (name =3D=3D "font-weight") {=0A= e.style.fontWeight =3D value;=0A= }=0A= else if (name =3D=3D "height") {=0A= e.style.height =3D value;=0A= }=0A= else if (name =3D=3D "ime-mode") {=0A= e.style.imeMode =3D value;=0A= }=0A= else if (name =3D=3D "layout-flow") {=0A= e.style.layoutFlow =3D value;=0A= }=0A= else if (name =3D=3D "layout-grid") {=0A= e.style.layoutGrid =3D value;=0A= }=0A= else if (name =3D=3D "layout-grid-char") {=0A= e.style.layoutGridChar =3D value;=0A= }=0A= else if (name =3D=3D "layout-grid-line") {=0A= e.style.layoutGridLine =3D value;=0A= }=0A= else if (name =3D=3D "layout-grid-mode") {=0A= e.style.layoutGridMode =3D value;=0A= }=0A= else if (name =3D=3D "layout-grid-type") {=0A= e.style.layoutGridType =3D value;=0A= }=0A= else if (name =3D=3D "left") {=0A= e.style.left =3D value;=0A= }=0A= else if (name =3D=3D "letter-spacing") {=0A= e.style.letterSpacing =3D value;=0A= }=0A= else if (name =3D=3D "line-break") {=0A= e.style.lineBreak =3D value;=0A= }=0A= else if (name =3D=3D "line-height") {=0A= e.style.lineHeight =3D value;=0A= }=0A= else if (name =3D=3D "list-style") {=0A= e.style.listStyle =3D value;=0A= }=0A= else if (name =3D=3D "list-style-image") {=0A= e.style.listStyleImage =3D value;=0A= }=0A= else if (name =3D=3D "list-style-position") {=0A= e.style.listStylePosition =3D value;=0A= }=0A= else if (name =3D=3D "list-style-type") {=0A= e.style.listStyleType =3D value;=0A= }=0A= else if (name =3D=3D "margin") {=0A= e.style.margin =3D value;=0A= }=0A= else if (name =3D=3D "margin-bottom") {=0A= e.style.marginBottom =3D value;=0A= }=0A= else if (name =3D=3D "margin-left") {=0A= e.style.marginLeft =3D value;=0A= }=0A= else 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