From: Subject: Tumor Environment Dictates Medulloblastoma Cancer Stem Cell Expression and Invasive Phenotype -- Annabi et al. 6 (6): 907 -- Molecular Cancer Research Date: Mon, 7 Jul 2008 19:49:43 +0200 MIME-Version: 1.0 Content-Type: multipart/related; type="text/html"; boundary="----=_NextPart_000_0014_01C8E06A.9A1E95B0" X-MimeOLE: Produced By Microsoft MimeOLE V6.00.2900.5512 This is a multi-part message in MIME format. ------=_NextPart_000_0014_01C8E06A.9A1E95B0 Content-Type: text/html; charset="iso-8859-1" Content-Transfer-Encoding: quoted-printable Content-Location: http://mcr.aacrjournals.org/cgi/content/full/6/6/907 Tumor Environment Dictates Medulloblastoma Cancer = Stem Cell Expression and Invasive Phenotype -- Annabi et al. 6 (6): 907 = -- Molecular Cancer Research 3D"Molecular=20 3D"
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3D"Right Articles by B=E9liveau, R.=20

Angiogenesis, Metastasis, and the Cellular Microenvironment

Tumor Environment Dictates Medulloblastoma Cancer Stem Cell = Expression and=20 Invasive Phenotype

Borhane = Annabi1,=20 Shanti Rojas-Sutterlin2, Carl=20 Laflamme1, Marie-Paule = Lachambre2,=20 Yann=E8ve Rolland2, Herv=E9=20 Sartelet3 and Richard = B=E9liveau2=20

1 Laboratoire d'Oncologie = Mol=E9culaire,=20 D=E9partement de Chimie, Universit=E9 du Qu=E9bec =E0 Montr=E9al, = 2 Centre de=20 Canc=E9rologie Charles-Bruneau, H=F4pital Sainte-Justine-UQAM, and = 3=20 Department of Pathology, H=F4pital Sainte-Justine, Montreal, Quebec, = Canada=20

Requests for reprints: Richard = B=E9liveau,=20 Laboratoire de M=E9decine Mol=E9culaire, Universit=E9 du Qu=E9bec =E0 = Montr=E9al, C.P. 8888,=20 Succursale Centre-ville, Montreal, Quebec, Canada H3C 3P8. Phone: = 514-987-3000,=20 ext. 8551; Fax: 514-987-0246. E-mail: oncomol{at}nobel.si.uqam.ca


3D"   =20 Abstract
Top
Notes
3D"Abstract
Introduction
Results
Discussion
Materials and Methods
Disclosure of Potential...
Acknowledgements
References
 
T= he neural=20 precursor surface marker CD133 is thought to be enriched in = brain=20 cancer stem cells and in radioresistant DAOY = medulloblastoma-derived=20 tumor cells. Given that membrane type-1 matrix = metalloproteinase=20 (MT1-MMP) expression is a hallmark of highly invasive,=20 radioresistant, and hypoxic brain tumor cells, we sought to = determine=20 whether MT1-MMP and other MMPs could regulate the invasive=20 phenotype of CD133(+) DAOY cells. We found that when DAOY=20 medulloblastoma or U87 glioblastoma cells were implanted in = nude=20 mice, only those cells specifically implanted in the brain=20 environment generated CD133(+) brain tumors. Vascular = endothelial=20 growth factor and basic fibroblast growth factor gene = expression=20 increases in correlation with CD133 expression in those = tumors. When=20 DAOY cultures were induced to generate in vitro=20 neurosphere-like cells, gene expression of CD133, MT1-MMP, = MMP-9, and=20 MDR-1 was induced and correlated with an increase in = neurosphere=20 invasiveness. Specific small interfering RNA gene silencing = of either=20 MT1-MMP or MMP-9 reduced the capacity of the DAOY monolayers = to=20 generate neurospheres and concomitantly abrogated their = invasive=20 capacity. On the other hand, overexpression of MT1-MMP in = DAOY=20 triggered neurosphere-like formation which was further = amplified=20 when cells were cultured in neurosphere medium. Collectively, = we=20 show that both MT1-MMP and MMP-9 contribute to the invasive=20 phenotype during CD133(+) neurosphere-like formation in=20 medulloblastoma cells. Increases in MMP-9 may contribute to = the=20 opening of the blood-brain barrier, whereas increased MT1-MMP = would=20 promote brain tumor infiltration. Our study suggests that = MMP-9 or=20 MT1-MMP targeting may reduce the formation of brain tumor = stem=20 cells. (Mol Cancer Res 2008;6(6):907=9616)


3D"   =20 Introduction
Top
Notes
Abstract
3D"Introduction
Results
Discussion
Materials and Methods
Disclosure of Potential...
Acknowledgements
References
 
R= ecently,=20 a small population of cancer stem cells (CSC) in adult and = pediatric=20 brain tumors has been identified (1,= 2)= .=20 These CSC, once isolated from tumor tissues, form = neurospheres=20 when cultured in vitro and possess the capacity for = cell=20 renewal. Based on their high expression of the neural = precursor=20 cell surface marker CD133 (prominin-1), these CSC have been=20 further hypothesized to bear properties such as resistance to = apoptosis and resistance to drugs and to ionizing radiation = (3,= 4)= .=20 Interestingly, among primary human medulloblastoma and = glioblastoma=20 multiforme=96derived cells, only those cells expressing CD133 = on their=20 surfaces can initiate tumors in the brains of nonobese=20 diabetic/severe combined immunodeficient mice (5)= . In=20 fact, the injection of as few as 100 CD133(+) cells produces = a tumor=20 that could be serially transplanted and that is a phenocopy = of the=20 patient's original tumor, whereas injection of CD133(=96) = cells did not=20 cause a tumor. Such evidence highlights the fact that in = brain=20 tumors, and in other malignancies, the tumor clone is = functionally=20 heterogeneous, existing, however, in a cellular hierarchy = based on=20 small subpopulations of stem cells (6)= .=20

Given that CD133 has been identified as a powerful CSC marker, = and=20 that its gene expression is significantly higher in the = recurrent=20 brain tumor tissue, we examined whether other molecular = players may=20 also contribute to the invasive potential of medulloblastomas. = Matrix=20 metalloproteinases (MMP) have been shown to be associated = with=20 glioblastoma (7,= 8)= and=20 medulloblastoma cell invasiveness (9,= 10). In=20 particular, levels of MMP-9 and membrane type-1 (MT1)=96MMP = expression=20 were increased in >75% of medulloblastoma tumor tissues = (11).=20 Whether the CD133(+)-CSC subpopulation of cells was also = targeted=20 remains unknown. When MMP-9 gene expression was = silenced in=20 DAOY medulloblastoma-derived cells, experimental in = vivo tumor=20 growth was inhibited in an intracranial animal model (12).=20 Moreover, in line with the CD133(+) tumor cell phenotype that = accounts for glioma stem cells' radioresistance (13),=20 the expression of MT1-MMP expression was also increased in=20 several cell line models that escaped radiation-induced = apoptosis (14,=20 15).=20 Previous reports from our laboratory have documented the = contribution=20 of MT1-MMP to the infiltrative and invasive phenotype of = brain=20 tumor=96derived cells (16, 17), and=20 strategies which inhibit either MMP-9 or MT1-MMP activities = and/or=20 expression may, furthermore, be envisioned to reduce = tumorigenicity=20 (17-19).=20 Whether expression of MMP-9 or MT1-MMP affects the = acquisition=20 of an invasive phenotype during neurosphere-like formation of = CSC is currently unknown.

In this study, we sought to examine the effect of tumor tissue=20 environment and the contribution of CD133(+) brain = tumor=96derived=20 CSC to tumor development in vivo. We also investigated the=20 in vitro expression of MMP-9 and MT1-MMP, two MMPs = which=20 contribute to the blood-brain barrier opening and to the=20 radioresistance phenotype of brain tumor cells in the = neurosphere=20 formation capacity of DAOY medulloblastoma cells.


3D"   =20 Results
Top
Notes
Abstract
Introduction
3D"Results
Discussion
Materials and Methods
Disclosure of Potential...
Acknowledgements
References
 
<= EM>The=20 Tissue Environment of Cell Implantation Dictates the Expression of = CD133(+)=20 Brain Tumor=96Derived Stem Cells
In an attempt to assess the = contribution=20 of CD133(+) CSC to experimental brain tumor growth, monolayer = cultures of DAOY medulloblastoma cells were trypsinized and = cell=20 suspensions were implanted either subcutaneously or by = stereotaxis=20 within the brain and left to develop for several weeks as=20 described in Materials and Methods. Histopathologic analysis = of=20 intracerebrally implanted human DAOY medulloblastoma cells = shows=20 well-defined but not encapsulated large malignant = proliferation=20 composed of a majority of small undifferentiated round cells = found=20 in normal mouse brain (Fig. = 1A1 ).=20 At high magnification, hematoxylin-phloxin-saffron staining = shows=20 that the tumor was highly cellular with numerous mitoses (Fig. = 1A2),=20 and presents an aggressive pattern with a limited area of = necrosis=20 (Fig.=20 1A3). The nuclei are often densely hyperchromatic, and = are=20 associated with poor cytoplasm. No fibrillar material and no = rosette=20 could be identified. Stromal elements were scant, consisting = of small=20 blood vessels. Moreover, some tumoral cells were found to = exhibit=20 membranous expression of CD133 (Fig. = 1A4,=20 arrows). Although subcutaneous tumor growth was = only=20 observed with implanted U87 glioblastoma cells, we found that = U87 and=20 DAOY cells implanted within the cerebral environment readily=20 developed into tumors. Intracerebral growth of U87 tumors was = routinely found to occur within the first 2 to 3 weeks, = whereas=20 significant intracerebral growth of DAOY tumors only occurred = after 9=20 to 11 weeks. Homogenates were then generated from the = individual=20 tumors and CD133 immunodetection was done. We found that = CD133=20 protein expression was only observed when U87 or DAOY cells = were=20 implanted within the cerebral environment (Fig. = 1B).=20 The origin of CD133 expression was further examined when = homogenates=20 from DAOY cell monolayers, control brain hemisphere, and=20 intracerebral DAOY-derived tumors were probed for CD133. We = found=20 that DAOY cell monolayers expressed low basal CD133 (Fig. = 1C, in=20 vitro), whereas CD133 expression was enriched in the = brain=20 hemisphere in which DAOY cells had been implanted (Fig. = 1C, in=20 vivo). Quantitative PCR was also done with the = control and=20 DAOY-derived tumors and confirmed the angiogenic phenotype of = DAOY-derived tumors as vascular endothelial growth factor and = basic=20 fibroblast growth factor gene expression were significantly = increased=20 in those tumors (Fig.=20 1D).



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  = 		FIGURE 1. The tissue = environment of=20 cell implantation dictates the expression of CD133(+) brain=20 tumor=96derived stem cells. Cultured DAOY monolayers were = trypsinized=20 and 106 cells injected either subcutaneously or=20 intracerebrally into nude mice. Tumors were left to develop = as=20 described in Materials and Methods. A. = Histopathologic=20 analysis of paraffin sections (3 =B5m) of intracerebrally = implanted=20 human DAOY medulloblastoma cells was done with=20 hematoxylin-phloxin-saffron staining and shows (1) = malignant=20 proliferation composed of a majority of small round cells=20 (arrow) found in normal mouse brain (*; = magnification, x100). At high magnification = (x400), = hematoxylin-phloxin-saffron=20 staining shows (2) that tumor is highly cellular with = numerous mitoses, and presents an aggressive pattern = (3) with=20 limited area of necrosis (magnification, x200). Some tumoral cells = (4) had=20 a membranous expression of CD133 (arrows). B.=20 Immunoblotting was used to assess CD133 protein expression = in=20 lysates (20 =B5g proteins) generated from subcutaneous and=20 intracerebral U87 glioblastoma-implanted or DAOY=20 medulloblastoma-implanted cells as described in Materials = and=20 Methods. C. Lysates (5 =B5g protein) from in = vitro=20 cultured DAOY cell monolayers (DAOY), contralateral = healthy=20 brain (Ctrl), and from intracerebrally implanted DAOY = cells=20 (Tumor) were assessed for CD133 expression.=20 Glyceraldehyde-3-phosphate dehydrogenase (GAPDH) = expression=20 was used as an internal loading control. D. Relative = gene=20 expression levels of CD133 (CD133), vascular = endothelial=20 growth factor (VEGF), and basic fibroblast growth = factor=20 (bFGF) were assessed by quantitative PCR using total = RNA=20 extracted from contralateral healthy brain (white = columns) or=20 from intracerebrally implanted DAOY tumors (black = columns). =

 = ;
Increased=20 CD133, MDR-1, MT1-MMP, and MMP-9 Expression Characterize the Invasive = Phenotype=20 of Neurosphere-Like DAOY Cells
Neurosphere-like brain CSC are = thought to=20 contribute to a subpopulation of CD133(+) brain CSC (4)= .=20 Neurosphere induction of DAOY cells was done according to = established=20 protocols (20-22), and=20 this process promoted the transition of adherent DAOY = monolayer=20 cells to neurosphere-like cells (Fig. = 2A ).=20 Total RNA was isolated from monolayers and from = neurosphere-like DAOY=20 cells and semiquantitative reverse transcription-PCR (RT-PCR) = was=20 done. We found that gene expression of CD133, MDR-1, HuR, = MMP-9, and=20 MT1-MMP all increased in neurosphere-like DAOY cells (Fig. = 2B).=20 Although the increase in CD133 cell surface expression was = confirmed=20 in cells cultured in neurospheres by flow cytometry (data not = shown),=20 the increases in MMP-9 and in MT1-MMP were both confirmed = when=20 conditioned media were isolated from serum-starved monolayers = and=20 from neurosphere-like DAOY cells and we observed a massive = increase=20 in extracellular proMMP-9 gelatinolytic activity, as assessed = by=20 gelatin zymography (Fig. = 2C)=20 from the latter medium. Although the latent proMMP-2 = extracellular=20 levels remained unchanged between monolayers and = neurosphere-like=20 cells, the active forms of MMP-2 were exclusively produced in = neurospheres, most likely due to an increased MT1-MMP = activity (Fig. = 2C).=20 Cell migration was also assessed by seeding monolayers and=20 neurosphere-like DAOY cells on top of modified Boyden = chambers. We=20 found that the invasive capacity of neurosphere-like DAOY = cells was=20 significantly increased when compared with DAOY cells grown = into=20 monolayers (Fig.=20 2D).



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  = 		FIGURE 2. Increased = CD133, MDR-1,=20 MT1-MMP, and MMP-9 expression characterize the invasive = phenotype of=20 neurosphere-like DAOY cells. A. Representative phase = contrast=20 pictures of DAOY monolayers and neurosphere-like cells were = taken=20 after 48 h of culture. B. Total RNA was extracted = from DAOY=20 monolayers and neurosphere-like cells as described in = Materials and=20 Methods. Semiquantitative RT-PCR was done and cDNA amplicons = for=20 MMP-9, HuR, CD133, MDR-1, MT1-MMP, and = glyceraldehyde-3-phosphate=20 dehydrogenase were revealed by electrophoresis using agarose = gels as=20 described in Materials and Methods. C. Conditioned = medium=20 from DAOY monolayers and neurosphere-like cells were = assessed for=20 their MMP-9 and MMP-2 secretion and activation levels as = described=20 in Materials and Methods. D. DAOY monolayers and=20 neurosphere-like cells were trypsinized and seeded (5 x 104 cells) on=20 gelatin-coated filters in modified Boyden chambers. = Migration was=20 allowed to proceed for 16 h at 37=B0C. Cells on filters were = then=20 fixed and stained; one out of five representative stainings = for each=20 condition. Columns, mean of a representative experiment in = which=20 five random fields per filter were counted for each = condition; bars,=20 SD. =

 = ;
MT1-MMP=20 and MMP-9 Contribute to the Invasive Phenotype and Contribute to the=20 Neurosphere-Like Formation Process in DAOY Cells
We next = assessed the=20 effects of MMP-9 and MT1-MMP activities in promoting = neurosphere-like=20 formation and invasion using RNA interference technology. = DAOY=20 monolayer cells were transiently transfected with small = interfering=20 RNA to specifically down-regulate either MMP-9 or MT1-MMP = gene=20 expression as described in Materials and Methods. = Transfection=20 efficiencies were monitored either through the protein = expression of=20 MMP-9 or through the MT1-MMP=96mediated activation of = proMMP-2 using=20 gelatin zymography. We found that basal levels of proMMP-9 in = DAOY=20 monolayers (Fig. = 3A,=20 monolayers ) as well as the proMMP-9 induced in=20 neurosphere-like DAOY cells (Fig. = 3A,=20 neurospheres) were significantly decreased in=20 siMMP-9=96transfected cells when compared with = mock-transfected cells.=20 MT1-MMP was also efficiently silenced and this was reflected = by the=20 complete inability of neurosphere-like DAOY cells to activate = latent proMMP-2 into its active MMP-2 form (Fig. = 3A,=20 neurospheres). MT1-MMP pro- and active forms of = protein=20 expression are further shown to be efficiently and = specifically=20 diminished using immunoblotting in siMT1-MMP=96transfected = cells but=20 not in siMMP-9=96transfected cells (Fig. = 3B,=20 exposition 30 s). Moreover, the increased proMMP-2=20 activation observed in neurospheres by zymography (Fig.=20 3A) also correlates with MT1-MMP proteolytic activation = as=20 seen by the appearance of the well-documented 45 kDa MT1-MMP=20 immunoreactive inactive form (Fig. = 3B,=20 exposition 2 min). Glyceraldehyde-3-phosphate=20 dehydrogenase protein expression was used as an internal = loading=20 control and remained unaffected throughout the conditions. = When=20 neurosphere-like formation was monitored, we found a = significant=20 decrease in neurosphere-like formation in cells whose MT1-MMP = or MMP-9 had been silenced, as can be seen in images recorded = at two different magnifications (x10=20 versus x4; Fig. = 3C).=20 Cell migration was also assessed with mock-transfected cells = as=20 well as with DAOY monolayers and neurosphere-like DAOY cells=20 that were transfected with MT1-MMP and MMP-9 silencers (Fig.=20 3D). The induced migration observed in neurosphere-like = DAOY=20 cells was completely abolished in those cells when either=20 MT1-MMP or MMP-9 gene expression was silenced (Fig. = 3D,=20 neurospheres). No significant decreases were = observed in=20 siMT1-MMP or in siMMP-9 DAOY cells from monolayer cultures = (Fig. = 3D,=20 monolayers).



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  = 		FIGURE 3. MT1-MMP and = MMP-9 control=20 the neurosphere-like formation process in DAOY cells and = contribute=20 to their invasive phenotype. A. Gene silencing using = siRNA=20 was used to down-regulate the expression of MT1-MMP and = MMP-9 in=20 DAOY cell monolayers (top) or DAOY neurospheres=20 (bottom) as described in Materials and Methods. = Conditioned=20 medium from each respective condition was harvested 48 h=20 posttransfection and the extent of either MT1-MMP or MMP-9 = silencing=20 assessed using gelatin zymography. B. MT1-MMP = immunoblotting=20 was done with cell lysates isolated from A. = Autoradiograms=20 are shown at 30-s vs. 2-min expositions in order to = appreciate=20 MT1-MMP down-regulation (30 s exposition), and the = appearance of the=20 43 to 45 kDa inactive immunoreactive MT1-MMP that is = generated=20 during proMMP-2 activation (2 min exposition).=20 Glyceraldehyde-3-phosphate dehydrogenase (GAPDH) was used as = an=20 internal loading control. C. Phase contrast = (magnification,=20 x10 and x4) microscopy enabled the = visualization=20 of the decrease in neurosphere-like formation in cells from = which=20 MT1-MMP or MMP-9 had been silenced. D. Cell migration = was=20 also assessed 48 h posttransfection in modified Boyden = chambers as=20 described in Materials and Methods for control (white=20 columns) monolayers and neurosphere-like DAOY cells, and = cells=20 in which MMP-9 (black columns) and MT1-MMP (gray=20 columns) gene expression was silenced. Columns, mean of = a=20 representative experiment in which five random fields per = filter=20 were counted for each condition; bars, SD. =

 = ;
Overexpression=20 of MT1-MMP Triggers Neurosphere-Like DAOY Differentiation
We = further=20 assessed the specific contribution of MT1-MMP toward the = control of=20 neurosphere-like DAOY formation. We first transiently = transfected=20 DAOY monolayers with cDNA encoding a recombinant MT1-MMP = protein=20 fused to green fluorescent protein (GFP; ref. 23).=20 Transfection efficiency was monitored using fluorescence = microscopy=20 and was confirmed by the expression of fluorescent cells (Fig. = 4A ).=20 Moreover, recombinant MT1-MMP was also found to be active as = its=20 expression led to proMMP-2 activation and to an increase in = proMMP-9=20 secretion as assessed by gelatin zymography (Fig. = 4B).=20 Mock- and MT1-MMP=96transfected DAOY monolayers were then = trypsinized=20 and cultured either in monolayer medium or in neurosphere = medium for=20 24 hours. Phase contrast pictures were taken in order to = monitor for=20 neurosphere-like formation in each culture condition. We = found that=20 mock-transfected cells were, as expected, still able to = adhere and=20 grow as monolayers when cultured in monolayer medium, = although they=20 formed neurosphere-like cells when cultured under neurosphere = medium=20 (Fig. = 4C,=20 phase contrast pictures). In contrast, when=20 MT1-MMP=96transfected DAOY monolayer cells were seeded in = monolayer=20 medium, we observed that very few GFP-positive cells adhered = to the=20 culture dishes but rather formed neurosphere-like cells (Fig. = 4C,=20 phase contrast pictures). This was also evident = through=20 fluorescence visualization. Recombinant MT1-MMP overexpression = was=20 thus found to enhance neurosphere-like DAOY formation as = shown=20 through phase contrast and fluorescent microscopy imaging (Fig.=20 4C).



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  = 		FIGURE 4. Overexpression = of MT1-MMP=20 triggers neurosphere-like DAOY differentiation. A. = DAOY cell=20 monolayers were transiently transfected with a plasmid = encoding=20 GFP-MT1-MMP as described in Materials and Methods. = Representative=20 pictures were taken in phase contrast (top) and = fluorescence=20 (bottom) in order to show transfection efficacy. = B.=20 Conditioned medium from mock and GFP-MT1-MMP=96transfected = cells were=20 assessed for proMMP-2 activation by the expression of the=20 recombinant MT1-MMP protein using gelatin zymography as = described in=20 Materials and Methods. C. Mock or = GFP-MT1-MMP=96transfected=20 cells were trypsinized and then seeded either in monolayer = medium or=20 neurosphere medium. Representative pictures were then taken = in phase=20 contrast and fluorescence in order to monitor the extent of=20 MT1-MMP=96mediated neurosphere-like formation. =

 = ;

3D"   =20 Discussion
Top
Notes
Abstract
Introduction
Results
3D"Discussion
Materials and Methods
Disclosure of Potential...
Acknowledgements
References
 
A= mong=20 brain tumors in children, the highly metastatic medulloblastomas=20 represent 3D~25% of all pediatric intracranial neoplasms (24).=20 Although modern neurosurgical and radiotherapy techniques = combined=20 with chemotherapy regimens result in prolonged free survival=20 rates, the long-term prognosis is poor and the quality of = life=20 of these patients is generally poor (25).=20 Recently, an isolated CD133(+) cell subpopulation from human = brain=20 tumors was shown to exhibit stem cell properties (5)= and is=20 thought to play a pivotal role in brain tumor initiation, = growth, and=20 recurrence (5,= 26).=20 Consequently, a better understanding of the potential = contribution of=20 brain tumor=96derived CSC will help develop new clinical = approaches in=20 order to improve the efficiency of current treatment. In the = present=20 study, we identified and evaluated new biological and = molecular=20 features regulating the invasive phenotype associated with = the=20 formation of neurosphere-like CD133(+) = medulloblastoma-derived CSC.=20 Using RNA interference technology, we provided evidence for = crucial=20 roles for MMP-9 and for MT1-MMP, two major actors in cell = invasion,=20 metastasis, and resistance to radiation, in CD133(+) = neurosphere-like=20 formation in DAOY medulloblastoma cells.

It is noteworthy that as few as 100 CD133(+) cells from a brain=20 tumor fraction were found to be capable of tumor initiation = in=20 nonobese diabetic/severe combined immunodeficiency mouse = brains (5)= . The use=20 of an intracerebral implantation model versus a flank = implantation=20 model in our current study, further added to the stringency = of our=20 experiments, proving that CD133 expression only arose from = implanted=20 brain tumor cells within a cerebral environment, possibly=20 attributable to increased angiogenesis as reflected by high = vascular=20 endothelial growth factor and basic fibroblast growth factor=20 transcript levels. Gene expression profiles of experimental = brain=20 tumors grown as subcutaneous flank xenografts, intracerebral=20 xenografts, and cells grown in vitro have been shown = to be=20 different suggesting that the tissue environment dictates the = experimental tumor phenotype (27, 28).=20 Intracerebral models can more closely mimic the actual = environment of=20 glioma- and medulloblastoma-derived CD133(+) CSC growth (29). The=20 demonstration that CD133(+) cells express increased MDR-1 = transcript=20 levels (this study; ref. 30)=20 also reveals issues important to drug delivery and to the=20 blood-brain barrier environment that can now be addressed in = terms of=20 chemoresistance or angiogenic phenotype.

The CD133(+) fraction among medulloblastomas, which initiated=20 tumors upon intracranial transplantation into the nonobese=20 diabetic/severe combined immunodeficiency mouse forebrain, = also=20 correlated closely with an in vitro primary sphere = formation=20 assay that was used to quantify stem cell properties (6)= .=20 Although brain tumor stem cell properties have recently been = studied=20 in nonadherent neurospheres (31), the=20 expression of selected markers was found to vary between = nonadherent=20 spheres and adherent monolayer cells, but no data was = available as to=20 MMP involvement in neurosphere-like formation. The = identification and=20 demonstration, in our current study, that MT1-MMP plays a = role in=20 medulloblastoma neurosphere-like formation provides support = for the=20 need to design new routes that use MT1-MMP as a therapeutic = target.=20 Indeed, based on blocking its activity with inhibitors, = antibodies,=20 or RNA interference, novel anticancer approaches using the = inhibition=20 of MT1-MMP activity have already been described (32). Work=20 with MT1-MMP shows that interference with its RNA expression=20 decreases tumor cell migration and invasion (33, 34). This=20 approach has already been shown to be possible in endothelial = cells=20 in which interference of MT1-MMP RNA expression decreased the = capacity to form capillary tubes in the Matrigel system (35).=20 Although speculative, it is tempting to suggest that = therapeutic use=20 of interference RNA approaches could also target the MT1-MMP=20 functions involved in the formation of neurosphere-like = CD133(+)=20 brain CSC. Evidence provided from our own study suggests that = inhibiting MT1-MMP and MMP-9 gene expression significantly = impairs=20 neurosphere-like formation and abrogates invasive properties = (Fig. = 3).=20 The potential therapeutic use of interference RNA is = currently being=20 investigated (36-38).=20

It is still unclear whether CD133 expression plays a causative,=20 contributing, or correlative role in the formation of the CSC = population. Still, CD133-expressing CSC have been implicated = in=20 a number of key processes, including tumor repopulation, = resistance=20 to therapy, increased aggressiveness, and angiogenesis (5,= 13). Among=20 the important implications that arise from our study is the=20 radioresistant phenotype ascribed to CD133-expressing CSC. A = recent=20 study has, in fact, provided evidence that CD133-expressing = glioma=20 cells in vivo and in culture are relatively resistant = to=20 radiation (13).=20 Moreover, DAOY medulloblastoma cells that express CD133 were = also=20 shown to be radioresistant when compared with CD133(=96) = cells (4)= . Given=20 that MT1-MMP expression is also correlated with brain tumor=20 recurrence, increased invasiveness, and radioresistance (15), one=20 can hypothesize in light of our observations that MT1-MMP = triggers=20 CD133(+) neurosphere-like formation in medulloblastoma cells, = and=20 that targeting of MT1-MMP functions and/or expression may = alter the=20 radioresistant and invasive phenotype of brain CSC. As such, = the=20 expression of a major group of MT-MMP has recently been found = elevated in gliomas (39), from=20 which CD133(+) CSC isolated from fresh brain tumor specimens = were=20 found to escape the lethal damage of ionizing radiation (13). New=20 possibilities for abrogating the tumor-promoting function of = MT1-MMP,=20 other than the conventional protease inhibitor-based = approach, have=20 recently been envisioned (32, 40, 41).=20

We have also identified increased levels of MMP-9 that = correlated=20 with neurosphere-like formation and to MT1-MMP increased = expression.=20 Known functions for MMP-9 include liberation of vascular = endothelial=20 growth factor during angiogenesis (42), and=20 disruption of the blood-brain barrier (43, 44). More=20 interesting are the less documented functions of MMP-9 = recently=20 reported in the promotion of thrombosis through increased = tissue=20 factor expression (45),=20 the latter being thought to contribute to tumor = growth/regulating=20 properties of CD133(+) CSC through increased tissue = factor=96dependent=20 procoagulant activity (46). In=20 fact, clinical and experimental evidence suggests that high = levels of=20 tissue factor are correlated with increasing cancer = aggressiveness=20 and procoagulant tendencies (47).=20 Furthermore, a crucial role of nuclear factor 3D{kappa}=20B in = tumor=20 stem cell biology has recently been inferred in which it = regulates=20 the expression of genes that are involved in essential = processes=20 during the initiation and progression of various cancer types = such as proliferation, migration, and apoptosis (48).=20 Consistent with that observation, a correlation was found = between=20 proMMP-9 expression and MT1-MMP=96mediated activation of = proMMP-2=20 in specific conditions such as in=20 12-O-tetradecanoylphorbol-13-acetate=96activated = HT1080=20 fibrosarcoma cells (49). This=20 phenomenon is thought to be mediated through nuclear factor = B=20 activation (50, 51),=20 and the promoter region of the MT1-MMP contains nuclear = factor B=20 binding sites (52).=20

Finally, our study focused on the well-established method of=20 neurosphere cell cultures that enabled us to study the in=20 vitro CSC phenotype. As such, the successful isolation = and=20 establishment of a novel, long-term, primary, = neurosphere-like cell=20 line from highly aggressive anaplastic medulloblastoma was = reported=20 (53),=20 and such a model will help shed light into the MMP functions = of=20 CD133(+) CSC. Our study is thus among the first to provide an = in=20 vitro model for potential MMP involvement in the CSC invasive=20 phenotype. Direct evidence for the role of these MMPs will be = obtained through the direct isolation and characterization of = CD133(+) CSC. In conclusion, the involvement of MMP-9 and = MT1-MMP=20 in CD133(+) neurosphere formation and in their acquisition of = an invasive phenotype and/or resistance to therapy phenotype=20 could thus affect a provisional stem cell niche formation = process=20 that would, in part, support the emerging tumor. MMP-9 and = MT1-MMP=20 targeting in CSC may constitute promising new targets for = anticancer=20 therapies in destroying brain tumor stem cells.


3D"   =20 Materials and Methods
Top
Notes
Abstract
Introduction
Results
Discussion
3D"Materials and = Methods
Disclosure of Potential...
Acknowledgements
References
 
<= EM>Materials
SDS=20 and bovine serum albumin were purchased from Sigma. Cell = culture=20 media was obtained from Life Technologies. Electrophoresis = reagents=20 were purchased from Bio-Rad. The enhanced chemiluminescence = reagents=20 were from Amersham Pharmacia Biotech. Microbicinchoninic acid = protein=20 assay reagents were from Pierce. The polyclonal antibody = against=20 CD133 and the monoclonal antibody against = glyceraldehyde-3-phosphate=20 dehydrogenase were purchased from Abcam and Advanced = Immunochemical,=20 Inc., respectively. The polyclonal antibody against MT1-MMP=20 (AB815) was from Chemicon. Horseradish = peroxidase=96conjugated=20 donkey anti-rabbit and anti-mouse IgG secondary antibodies = were=20 from Jackson ImmunoResearch Laboratories. All other reagents=20 were from Sigma-Aldrich, Canada.

Cell Culture and Neurosphere-Like Formation
The human = DAOY=20 medulloblastoma cell line was purchased from American Type = Culture=20 Collection and was maintained in Eagle's MEM containing 10% = (v/v)=20 calf serum (HyClone Laboratories), 2 mmol/L of glutamine, 100 = units/mL of penicillin, and 100 mg/mL of streptomycin. Cells = were=20 incubated at 37=B0C, with 95% air and 5% CO2.=20 Neurosphere-like formation was triggered in a defined = serum-free=20 neural stem cell medium (54)=20 containing Ex Vivo 15 (Lonza), 20 ng/mL of basic fibroblast = growth=20 factor, 20 ng/mL of epidermal growth factor (Wisent), 20 = ng/mL of=20 leukemia-inhibitory factor (Sigma), and 1x neural survival factor-1 (Lonza). =

Intracranial Tumor Model
All animal experiments were = evaluated=20 and approved by the Institutional Committee for Good Animal = Practices=20 (Universit=E9 du Qu=E9bec =E0 Montr=E9al, Quebec, Canada). = Intracerebral=20 tumor implantation was done as previously described with some = modifications (55).=20 Anesthetized 5- to 10-week-old Crl:CD-1-nuBR female nude mice = (Charles River) were placed in a stereotaxic frame; viable = DAOY=20 medulloblastoma (2 x 106) = or U87=20 glioblastoma cells (5 x=20 104) in 5 =B5L of medium without serum were then = implanted=20 into the right corpus striatum at a depth of 3.5 mm at a = point=20 2.5 mm lateral to the midline and 1.5 mm anterior to the = bregma.=20

Subcutaneous Xenograft Model
Tumor implantation was done = as=20 described previously (56).=20 Briefly, DAOY medulloblastoma or U87 glioblastoma cells were=20 harvested by trypsinization using a trypsin/EDTA solution. = Cells=20 were washed thrice with PBS that was free of both = Ca2+ and=20 Mg2+, and then centrifuged. The resulting pellet = was=20 resuspended in 1% methylcellulose in serum-free MEM at a=20 concentration of 2.5 x=20 106 cells per 100 =B5L. Animals were anesthetized by=20 oxygen/isoflurane inhalation and tumors were established by = s.c.=20 injection of 100 =B5L from the cell suspension into the right = flank=20 of female Crl:CD-1-nuBR nude mice.

Histology and Immunocytochemistry
Mouse brains were fixed = in 10%=20 buffered formalin and paraffin-embedded. For routine = histologic=20 examination, 3-=B5m-thick sections were stained with=20 hematoxylin-phloxin-saffron. Immunohistochemistry was done on = paraffin-embedded sections using the biotin-streptavidin = peroxidase=20 LSAB kit in conjunction with an automated DAKO immunostainer=20 (DakoCytomation). An antibody against CD133 (1:100, rabbit=20 polyclonal; Abcam) was applied. First, for antigen retrieval, = deparaffinized and rehydrated sections were treated using a = pressure=20 cooker [citrate buffer (pH 6.0), 1:10, 30 min]. Then the = sections=20 were mounted in the DAKO autostainer, covered with=20 H2O2 for 5 min, followed by a 5-min = application=20 of Ultra V block (LabVision). The slides were then incubated = for 60=20 min with the diluted antibody at room temperature, followed = by=20 application of the labeled biotin-streptavidin reagents = according to=20 the manufacturer's instructions (LSAB+ System HRP-Kit; DAKO). = 3,3'-Diaminobenzidine (DAKO) was used as a chromogen. A = section of=20 human fetal liver was used in the same slide as a specific, = positive=20 control (57).=20 Normal mouse or rabbit IgG at the same concentration as the=20 primary antibody served as negative controls. Slides were = then=20 incubated with this solution instead of primary antibody. = Tissues=20 were analyzed and photographed using a Zeiss Axioplan = microscope.=20

Total RNA Isolation and Semiquantitative RT-PCR = Analysis
Total=20 RNA was extracted from monolayers or neurosphere-like DAOY = cells=20 using the TRIzol reagent (Life Technologies). One microgram = of total=20 RNA was used for first-strand cDNA synthesis followed by = specific=20 gene product amplification with the One-step RT-PCR Kit = (Invitrogen).=20 Primers for CD133 (Santa Cruz Biotechnology), MDR-1 (forward, = 5'-ATTCAACTATCCCACCCGACCG-3'; reverse, = 5'-CCTTTGCTGCCCTCACAATCTC-3'),=20 MT1-MMP (forward, 5'-ATTGATGCTGCTCTCTTCTGG-3'; reverse,=20 5'-GTGAAGACTTCATCGCTGCC-3'), HuR (forward,=20 5'-TCGCAGCTGTACCACTCGCCAG-3'; reverse, = 5'-CCAAACATCTGCCAGAGGATC-3'),=20 and for MMP-9 (forward, 5'-AAGATGCTGCTGTTCAGCGGG-3'; reverse, = 5'-GTCCTCAGGGCACTGCAGGAT-3') were all derived from human = sequences.=20 PCR conditions were optimized so that the gene products were=20 examined at the exponential phase of their amplification and=20 the products were resolved on 1.8% agarose gels containing 1=20 =B5g/mL of ethidium bromide.

cDNA Synthesis and Real-time Quantitative RT-PCR
Total = RNA was=20 extracted from fresh tumor tissue or cell cultures as = described=20 above. For cDNA synthesis, 3D~=201 =B5g total = RNA=20 was reverse-transcribed into cDNA using high-capacity cDNA = reverse=20 transcription kit (Applied Biosystems). cDNA was stored at = =9680=B0C=20 for PCR. Gene expression was quantified by real-time = quantitative=20 PCR using iQ SYBR Green Supermix (Bio-Rad). DNA amplification = was carried out using Icycler iQ5 (Bio-Rad) and product = detection=20 was done by measuring the binding of the fluorescent dye SYBR = Green I to double-stranded DNA. All the primer sets were = provided=20 by Qiagen. The relative quantities of target gene mRNA = against=20 an internal control, 18S rRNA, were measured by following a=20 3D{Delta}CT method. An amplification plot that had been the = plot of=20 fluorescence signal versus cycle number was drawn. The = difference=20 (3D{Delta}CT) between the mean values in the = triplicate=20 samples of target gene and those of 18S rRNA were calculated = by iQ5=20 Optical System Software version 2.0 (Bio-Rad) and the = relative=20 quantified value was expressed as 2 3D{Delta}=20CT.=20

RNA Interference
RNA interference experiments were done = using=20 HiPerFect (Qiagen). A small interfering RNA (20 nmol/L) = against=20 MT1-MMP (siMT1-MMP) and mismatch small interfering RNA were=20 synthesized by EZBiolab Inc., and annealed to form duplexes. = The=20 sequence of the siMT1-MMP used in this study was derived from = the=20 human MT1-MMP gene (NM_004995)=20 and is as follows: 5'-CCAGAAGCUGAAGGUAGAAdTdT-3' (sense) and=20 5'-UUCUACCUUCAGCUUCUGGdTdT-3' (antisense; ref. 58). A=20 small interfering RNA against human MMP-9 (siMMP-9; GenBank=20 accession number, NM-004994) and mismatch small interfering = RNA with=20 no known homology to mammalian genes were synthesized = (Qiagen)=20 against the following published target sequences for MMP-9:=20 5'-AACATCACCTATTGGATCCAAACTAC-3', nucleotides 377 to 403. The = sequence of the siMMP-9 used in this study is as follows:=20 5'-CAUCACCUAUUGGAUCCAAdTdT-3' (sense) and=20 5'-UUGGAUCCAAUAGGUGAUGdTdT-3' (antisense). Evaluation of the=20 transient knockdown duration was done by real-time quantitative=20 RT-PCR, and the targeted gene expression was found to be = routinely=20 diminished by 65% to 90%, 24 to 48 h posttransfection (data = not=20 shown).

Cell Transfection Method
Subconfluent DAOY monolayer = cells were=20 transiently transfected with 10 =B5g of the cDNA encoding the = full-length (Wt) MT1-MMP fused to GFP (59) using=20 LipofectAMINE 2000 (Invitrogen). Mock transfections of U87 = cultures=20 with pcDNA (3.1+) were used as controls. Transfected cells = were left=20 to recuperate and were used 48 h posttransfection. The = occurrence of=20 MT1-MMP=96specific gene expression and function was evaluated = by=20 semiquantitative RT-PCR, immunoblotting procedures, and = validated by=20 assessing MT1-MMP=96mediated proMMP-2 activation by gelatin=20 zymography (Figs. = 3 and=20 4)= .=20

Gelatin Zymography
Gelatin zymography was used to assess = the=20 proMMP-9, proMMP-2, and MMP-2 extracellular levels. Briefly, = an=20 aliquot (20 =B5L) of the culture medium was subjected to = SDS-PAGE in a=20 gel containing 0.1 mg/mL of gelatin. The gels were then = incubated in=20 2.5% Triton X-100 and rinsed in nanopure distilled = H2O.=20 Gels were further incubated at 37=B0C for 20 h in 20 mmol/L = of NaCl, 5=20 mmol/L of CaCl2, 0.02% Brij-35, 50 mmol/L of = Tris-HCl=20 buffer (pH 7.6), then stained with 0.1% Coomassie brilliant = blue=20 R-250, and destained in 10% acetic acid and 30% methanol in=20 H2O. Gelatinolytic activity was detected as = unstained=20 bands on a blue background.

Immunoblotting Procedures
Proteins from control and = treated cells=20 were separated by SDS-PAGE. After electrophoresis, proteins = were=20 electrotransferred to polyvinylidene difluoride membranes = which were=20 then blocked for 1 h at room temperature with 5% nonfat dry = milk in=20 TBS (150 mmol/L NaCl, 20 mmol/L Tris-HCl; pH 7.5) containing = 0.3%=20 Tween 20 (TBST). Membranes were further washed in TBST and = incubated=20 with the primary antibodies (1:1,000 dilution) in TBST = containing=20 3% bovine serum albumin, followed by a 1-h incubation with=20 horseradish peroxidase=96conjugated antirabbit or antimouse = IgG=20 (1:2,500 dilution) in TBST containing 5% nonfat dry milk.=20 Immunoreactive material was visualized by enhanced = chemiluminescence=20 (Amersham Biosciences).

Analysis of DAOY Cell Migration
DAOY cell migration was = assessed=20 using modified Boyden chambers. The lower surfaces of = transwells=20 (8-=B5m pore size; Costar) were precoated with 1 mg/mL of = gelatin for 2=20 h at 37=B0C. The transwells were then assembled in a 24-well = plate=20 (Fisher Scientific, Ltd.). The lower chamber was filled with=20 serum-free medium. Monolayer or neurosphere-like DAOY cells = were=20 collected by trypsinization, washed, and resuspended in = serum-free=20 medium at a concentration of 5 x=20 105 cells/mL; 5 x = 104=20 cells were then inoculated onto the upper side of each = modified=20 Boyden chamber. The plates were placed at 37=B0C in 5%=20 CO2/95% air and migration left to proceed for 16 = h. Cells=20 that had migrated to the lower surfaces of the filters were = fixed=20 with 10% formalin phosphate and stained with 0.1% crystal = violet-20%=20 methanol (v/v). Images of at least five random fields per = filter were=20 digitized (100x = magnification). The=20 average number of migrating cells per field was quantified = using=20 Northern Eclipse software (Empix Imaging Inc.). Migration = data are=20 expressed as a mean value derived from at least three = independent=20 experiments.

Statistical Data Analysis
Data are representative of = three or=20 more independent experiments. Statistical significance was = assessed=20 using Student's unpaired t test. Probability values of = <0.05 were considered significant, and an asterisk (*) = identifies=20 such significance in each figure.


3D"   =20 Disclosure of Potential Conflicts of Interest =
Top
Notes
Abstract
Introduction
Results
Discussion
Materials and Methods
3D"Disclosure of = Potential...
Acknowledgements
References
 
N= o=20 potential conflicts of interest were disclosed.


3D"   =20 Acknowledgements
Top
Notes
Abstract
Introduction
Results
Discussion
Materials and Methods
Disclosure of Potential...
3D"Acknowledgements
References
 
W= e thank=20 Dr. Anthony Regina and Isabelle Lavall=E9e for their = assistance in=20 handling and treating the mice.


3D"    Notes=20
Top
3D"Notes
Abstract
Introduction
Results
Discussion
Materials and Methods
Disclosure of Potential...
Acknowledgements
References
 
<= A=20 name=3D"">Grant support: B. Annabi holds a = Canada Research=20 Chair in Molecular Oncology from the Canadian Institutes of = Health=20 Research. This study was funded by grants from the Natural = Sciences=20 and Engineering Research Council of Canada, the Canadian = Institutes=20 of Health Research, the Charles-Bruneau Foundation, and the = Claude=20 Bertrand Chair in Neurosurgery (R. B=E9liveau), and from the=20 Natural Sciences and Engineering Research Council of Canada = (B.=20 Annabi).

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

Received 12/ 3/07; revised 1/26/08; accepted 2/ 3/08.


3D"   =20 References
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Introduction
Results
Discussion
Materials and Methods
Disclosure of Potential...
Acknowledgements
3D"References
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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; 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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_0014_01C8E06A.9A1E95B0 Content-Type: application/octet-stream Content-Transfer-Encoding: quoted-printable Content-Location: http://mcr.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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