From: Subject: Multifaceted Resistance of Gliomas to Temozolomide -- Bocangel et al. 8 (8): 2725 -- Clinical Cancer Research Date: Sun, 17 Feb 2008 18:31:11 +0100 MIME-Version: 1.0 Content-Type: multipart/related; type="text/html"; boundary="----=_NextPart_000_0031_01C87193.4532D6B0" X-MimeOLE: Produced By Microsoft MimeOLE V6.00.2900.3198 This is a multi-part message in MIME format. ------=_NextPart_000_0031_01C87193.4532D6B0 Content-Type: text/html; charset="Windows-1252" Content-Transfer-Encoding: quoted-printable Content-Location: http://clincancerres.aacrjournals.org/cgi/content/full/8/8/2725 Multifaceted Resistance of Gliomas to Temozolomide -- = Bocangel et al. 8 (8): 2725 -- Clinical Cancer Research 3D"Clinical 3D"
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Clinical Cancer Research Vol. 8, 2725-2734, August 2002
=A9 = 2002 American = Association for Cancer Research

Experimental Therapeutics, Preclinical=20 Pharmacology

Multifaceted Resistance of Gliomas to Temozolomide1=20

Dora B. Bocangel, Sydney=20 Finkelstein, S. Clifford Schold, Kishor K.=20 Bhakat, Sankar Mitra and Demetrius M. = Kokkinakis2=20

Department of Pathology, The University of Pittsburgh = Cancer=20 Institute, Pittsburgh, Pennsylvania 15261 [S. F., S. C. S., D. M. K.], = and The=20 University of Texas Medical Branch at Galveston, Galveston, Texas 77555 = [D. B.=20 B., K. K. B., S. M.]


3D"   =20 ABSTRACT
Top
3D"ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
 
<= I>Purpose=20 and Experimental Design: The contributions of=20 O6-methylguanine-DNA-methyltransferase(MGMT), = p53=20 status, mismatch repair, and apoptotic response to the resistance = of=20 glial tumors to temozolomide (TMZ) were tested using seven=20 established human glial tumor cell lines in culture and = xenografts=20 in athymic mice.

Results: Resistance to TMZ was only marginally dependent = on=20 MGMT activity, because subtoxic doses of TMZ easily = eliminated=20 MGMT reserves for at least 18 h after treatment. Resistance = to=20 TMZ varied most notably with the p53 status of the tumor. = Tumors with=20 wild-type (wt) p53 and a functional p53 response to DNA = damage (SWB40=20 and SWB61) were most sensitive. The p21-related cell cycle = arrest was=20 intimately linked to TMZ toxicity because tumors with wt p53 = but=20 lacking a robust increase in p21 protein level (D-54) were = resistant=20 to TMZ. In contrast, tumors with a dysfunctional p53 cycle = and a weak=20 cell cycle response to DNA damage (SWB39 and SWB77) were = extremely=20 unresponsive to treatment even with the aid of MGMT = inactivators.=20 Notable exceptions to the above were observed with the p53 = mutated=20 tumors SWB33 and SWB95, which were arrested by TMZ in = G1-S=20 and consequently underwent apoptosis despite their failure to = express=20 p21.

Conclusions: By testing a limited number of glial tumors = in=20 cell culture and also as xenografts, we have shown that = mobilization=20 of the p53 in response to TMZ damage is likely to induce a = cell=20 cycle arrest and apoptosis in glial tumors. Additional = pathways=20 linking cell cycle arrest and apoptosis contribute to the = efficacy=20 of TMZ against p53 mutated glial tumors. The unusual = resistance=20 of tumors, of which the cell cycle was not arrested in = response=20 to TMZ treatment, was associated with allelic losses during=20 regrowth of treated tumors. Nevertheless such resistance was=20 not related to dysfunctional mismatch repair.


3D"   =20 INTRODUCTION
Top
ABSTRACT
3D"INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
 
T= he=20 prognosis for 20,000 new cases of brain tumors per year in = the United=20 States alone is particularly abysmal. Median survival in = patients=20 with glioblastoma multiforme is less than a year even when = treated=20 with the most aggressive regimens of cytoreductive surgery,=20 radiation, and chemotherapy (1)=20 . The propensity of individual neoplastic cells to migrate = away from=20 the primary brain tumor mass, along white matter pathways (2)=20 , renders treatments directed solely at that main tumor mass = of=20 palliative benefit only. To date, no treatment has been = developed=20 that can prevent residual neoplastic cells that remain viable = after surgery and radiation therapy to proliferate and cause=20 these tumors to recur. Alkylating drugs such as BCNU3=20 and = N-(2-chloroethyl)-N'-cyclohexyl-N-nitrosourea=20 have been somewhat effective against anaplastic astrocytomas = (3=20 ,=20 4) , but their action is limited by the presence of mechanisms = of=20 resistance, one of the most prominent of which is the up-regulation = of MGMT during neoplastic progression (5=20 ,=20 6) . MGMT confers resistance in tumors to agents that = exert their=20 cytotoxic action via the formation of=20 O6-alkylguanine adducts that either form = lethal=20 double-strand cross-links (7)=20 , as is the case with bifunctional nitrosoureas [BCNU and=20 N-(2-chloroethyl)-N'-cyclohexyl-N-nitrosourea],= =20 or initiate mismatch abortive repair and DNA fragmentation,=20 which results in cell death, as is the case with TMZ, = procarbazine,=20 and other DNA methylating agents (8=20 ,=20 9) . The involvement of MGMT in the resistance of brain = tumors to=20 DNA alkylating drugs has been demonstrated with the use of = MGMT=20 inactivators such as BG or dBG, which enhance the efficacy of = a=20 variety of DNA alkylating agents against brain tumor = xenografts in=20 mice (10,=20 11,=20 12)=20 . These advances have promoted the general notion that drugs = that=20 have been marginally active against brain tumors in the past = could be=20 successfully reintroduced in combination with MGMT = inhibitors, and a=20 number of clinical trials have been completed or are = currently in=20 progress to determine the feasibility of such a strategy (13,=20 14,=20 15)=20 . Unlike BCNU, the resistance to which tends to be linked = mainly and=20 directly to the expression of MGMT, the resistance of glial = tumors to=20 monofunctional alkylating agents seems to follow a more = complex=20 pattern than simple dependence on MGMT levels, and may be = controlled=20 by additional DNA repair processes, apoptotic pathways, or = cell cycle=20 check points. These processes may not be entirely = independent. A=20 correlation between wt-p53 suppression of MGMT transcription, = and a=20 related decrease in resistance to chloroethylnitrosoureas has = been=20 reported (16)=20 ; and in general, wt-p53-containing cell lines have = lower=20 MGMT levels than those in mutant p53-containing cells (17,=20 18,=20 19)=20 . Signaling between MMR and p53 has also been suggested (20)=20 . wt-p53 plays a key role in mediating cell death of tumor = cells=20 through DNA damage-induced activation of apoptotic = mechanisms.=20 Activation of Bax, DR5, and Fas/APO1 or by protein-protein=20 interactions with key elements in DNA synthesis or repair = facilitates=20 apoptosis (21,=20 22,=20 23)=20 . p53 can induce cell arrest (when the genome is = damaged to a=20 limited extent, providing time to repair the DNA) or it can = trigger=20 apoptosis when damage is too severe for repair (21,=20 22)=20 . Inactivation of p53 during malignancy allows highly damaged = cells=20 to survive and to accumulate mutations, thus increasing their = propagation to oncogenic transformation, and possible = acquisition of=20 additional resistance to cytotoxic agents, through selection = of=20 clones with inactivated cell cycle checkpoints. Given the = role of p53=20 in cell cycle progression and survival, and its recently = reported=20 interactions with DNA repair pathways it is likely that p53 = status=20 could predict the outcome of treatment of certain types of=20 tumors.

In this study we have examined seven high-grade glial tumors = in=20 terms of their resistance to TMZ both in cell culture and = also in=20 xenografts; their p53, MGMT, and MMR status; their cell cycle = response to DNA damage; and their ability to undergo apoptosis = in=20 response to DNA damage. These systematic investigations have = yielded=20 several new pieces of information regarding mechanisms of = resistance=20 of glial tumors to methylating agents and are likely to set = the stage=20 for clinical trials using such agents in combination with = procedures=20 to overcome the nonresponsiveness of the cell cycle of the = most=20 resistant glial neoplasms to DNA damage (24)=20 .


3D"   =20 MATERIALS AND METHODS
Top
ABSTRACT
INTRODUCTION
3D"MATERIALS AND = METHODS
RESULTS
DISCUSSION
REFERENCES
 
<= STRONG>Chemicals.
BG=20 and dBG were synthesized and purified according to methods = published=20 previously (25=20 ,=20 26) and donated to us by Dr. Robert Moschel. TMZ was a = gift by=20 Schering-Plough Inc. (Madison, NJ).

Cell Culture and Treatment Conditions.
All of the = cell=20 lines used in this study (SWB 33, 39, 40, 61, 77, 95, and = D54) were=20 derived from human high-grade gliomas. They were grown in 5% = fetal=20 bovine serum (Life Technologies, Inc., Gaithersburg, MD) in = Eagle=92s=20 minimum essential medium-3D{alpha}=20=20 modification (Life Technologies, Inc.) supplemented with = lysine,=20 valine, methionine and leucine (100 =B5M = each),=20 nonessential amino acids (1:100 dilution of stock; Life = Technologies,=20 Inc.), 1 mM sodium pyruvate, 1 = =B5M 3D{alpha}=20-hydroxycobalamin, 10 =B5M = folic acid,=20 and 0.2 mg/ml gentamicin. LoVo cells were obtained from = American Type=20 Culture Collection, and grown in Ham=92s F12 medium = containing 10%=20 fetal bovine serum (Life Technologies, Inc.). All of the = cells were=20 grown at 37=B0C in 5% CO2 and tested routinely for = Mycoplasma contamination with Hoechst 33258 = stain.

Animals/Tumors.
Four-week-old BALB/c-nu/nu = athymic=20 mice were purchased from Harlan Labs (San Diego, CA). Mice = were=20 maintained under barrier conditions and given sterilized food = (Harlan=20 Teklad laboratory diet) and water. s.c. tumors grew on = injection of 3=20 million cells/animal. Tumor xenografts D-54, SWB 33, SWB39, = SWB40,=20 SWB77, and SWB61 had MGMT activities of <10, 56, 10, 45, = 75,=20 and 16-fmol/mg protein, respectively, as determined by the=20 biochemical assay (27)=20 . Respective mitotic indices in xenografts were 5.5, 5.7, = 8.2, 12.1,=20 5.7, and 12.9 m/high powered field (x400).

Drug Doses.
All of the treatments were = administered i.p.=20 BG was dissolved in 40% polyethylene glycol 400/60% PBS. The = pH of=20 the solvent was corrected to 7.0 before the addition of the = drug. TMZ=20 was dissolved in 100% DMSO. MGMT inhibitors were administered = at=20 volumes of 30 ml/m2 and alkylating drugs at 20=20 ml/m2. Drug doses were calculated as = mg/m2=20 using the formula: meters (m) =3D weight (g)2/3 = x K x=20 10-4, where K is 10.5 for mice (28)=20 . In animals of 20 =B1 2 g used in this study, the weight = (kg) of=20 the animal is 3D~=202.6 times the=20 area surface (m2).

Tumor Implantation and Treatment.
Two hundred = =B5L=20 containing 3 x 106 cells = of tumor=20 cells in 5% serum medium were injected at the left flank of=20 6-week-old athymic mice weighing between 18 and 22 g. Visible = tumors=20 appeared in most of the animals within 3 weeks after = implantation.=20 The tumors were subsequently measured with calipers in two=20 perpendicular dimensions, and their volumes were estimated = using the=20 formula (3D{alpha}=202=20 x =DF)/2, where 3D{alpha}=20 = is the=20 shorter and =DF the longer of the two dimensions. Treatment = with TMZ in=20 DMSO was administered i.p. to animals having tumors ranging = between=20 325 and 375 mm3. Animals were killed at 24 and 48 = h after=20 treatment with TMZ; the tumors were excised and processed for = histology. Control animals bearing tumors were treated with = DMSO and=20 were killed at the same time intervals.

Immunohistochemistry and=20 Immunocytochemistry.
Immunoperoxidase staining for = phosphorylated=20 p53 and p21 were performed on formalin-fixed, = paraffin-embedded=20 tissue sections following the standard protocol recommended = by the=20 manufacturer (Cell Signaling Technologies). Briefly, 5-=B5m = tissue=20 sections mounted on Superfrost/Plus slides (Fisher), were=20 deparaffinized, rehydrated, and incubated with 1.0%=20 H2O2 in Tris-buffered saline to block=20 endogenous peroxidase activity. Antigen unmasking was = performed=20 heating samples in sodium citrate buffer (10 mM sodium = citrate, pH=20 6.0) 10 min, 100=B0C. Nonspecific protein binding was blocked = by=20 incubation in 5% horse serum in PBS [(pH 7.2=967.4) 10.4 = mM Na2HPO4, 3.16 mM=20 KH2PO4, and 123 mM NaCl]. = Rabbit=20 polyclonal (for p53) or monoclonal (for p21) IgG were applied = to the=20 sections and incubated (in blocking solution) overnight at = 4=B0C.=20 Serial sections of the tumor without primary antibody were = used=20 as negative control. After washing in PBS, the tumor sections = were incubated in secondary antibody for 30 min at room=20 temperature. The sections were washed again, treated with = Elite ABC=20 (Vectastain), washed, and developed with = 3,3'-diaminobenzidine=20 tetrahydrochloride (50 mg 3,3'-diaminobenzidine in 100 ml PBS = and 150=20 =B5L of 3% H2O2). After rinsing in PBS, = slides=20 were dehydrated in graded alcohols, cleared in xylene, and=20 permanently mounted. For immunocytochemistry, cells were = grown on 1=20 mm coverslides (Corning) and, after drug treatment, fixed = (freshly=20 made 4% paraformaldehyde, 5% sucrose solution, in PBS), = stained,=20 and mounted (DAKO). Standard immunocytochemistry procedures = were=20 used. Briefly, nonspecific binding was blocked in incubating=20 slides, in 5% normal goat serum in Tris buffered saline 0.05% = Tween 20, 60 min at room temperature [50 mM = Tris-HCl=20 (pH 7.2=967.4)], 150 mM NaCl, and = 0.05% Triton=20 X-100]. The slides were then incubated in primary antibody = diluted in=20 blocking serum. A polyclonal (p53) rabbit antibody that = recognizes=20 (Serine-15) phosphorylated p53 (Cell Signaling Technology) = was used=20 to determine activated p53 protein. Alternatively, we also = used a=20 monoclonal rabbit (p21; Santa Cruz Biotech), and mouse (p53, = DO-1;=20 Santa Cruz Biotech) antibody. Cells were washed in TBST and = then=20 incubated with biotinylated secondary antibody for 60 min at = room=20 temperature. Cells were washed, and secondary antibody was = detected=20 using Streptavidin-linked Alexa 488 (Molecular Probes Inc.).=20 Slides were then mounted (DAKO), images captured using a = Nikon=20 Eclipse-800 epifluorescent microscope and a couled monochrome = CCD300T=20 video camera from DAGE-MTI (Michigan City, IN), and analyzed=20 using Metamorph imaging software (Universal Imaging Corp.,=20 Westchester, PA).

Clonogenic Survival Assays.
Exponentially growing = cells=20 were seeded at a density of 250 to 300 cells/60-mm dish and = left to=20 attach for 24 h; then the cells were either pretreated with = BG at 20=20 =B5M, TMZ (at specified = concentrations), or=20 mock-treated. For the BG colony-forming assays, cells were = incubated=20 for 2 h in serum containing medium with BG and then changed = to serum=20 free, TMZ containing medium for 30 min, then switched back to = serum=20 and BG containing medium. Twenty-four h afterward the cells = were=20 changed to BG free, serum-containing medium and left for 2 = weeks to=20 grow colonies, after which they were fixed and stained with a = crystal=20 violet/formalin solution, and counted. Cell survival is = estimated=20 from the number of colonies (defined as a cluster of >50 = cells)=20 formed and expressed as a percentage of the number of = colonies in the=20 control. Assays were set up in quadruplicate, and SDs were = used in=20 the calculations instead of SEs.

TUNEL Assays and Apoptotic Indices.
Briefly, the = cells=20 were treated with TMZ, resuspended, fixed, and labeled (TUNEL = assay;=20 Boehringer Mannheim) according to the manufacturer=92s = protocols at=20 either 24 or 48 h after treatment with TMZ (100 =B5M). Apoptotic indexes were calculated = scoring five=20 randomly selected fields (number of cells counted over 400) = and=20 extrapolating the results to the number of apoptotic cells in = 1000=20 cells.

Western Blots.
Cells were lysed as described = earlier (29)=20 , and protein concentration was determined using the Bradford = Reagent=20 (Bio-Rad); 20=9630 =B5g protein was run on SDS-PAGE (10% for = MMR proteins=20 and 12% acrylamide for all of the others; acrylamide). = Protein=20 was then electroblotted to nitrocellulose membranes (40 V=20 overnight at 4=B0C) in transfer buffer containing 25 mM Tris-HCl, 129 mM = glycine, and=20 20% methanol. Membranes were blocked in 5% milk in TBST, = incubated in=20 primary antibody (in TBST, 5% milk for 1 h at room = temperature),=20 rinsed, and incubated in horseradish peroxidase-conjugated = secondary=20 antibody (Amersham). Western blots were visualized using = enhanced=20 chemiluminescence (Amersham). Antibodies to p53 (DO-1),=20 phosphorylated p53 (Cell Signal Technologies), p21 (Santa = Cruz=20 Biotechnologies), and =DF-actin (Sigma) were used at optimal=20 titrations.

TG Assays.
Clonogenic survival assays were set up = with=20 LoVo and glioma cell lines for TG (0.001=963 =B5g/ml). = Briefly,=20 cells were plated at low density (300 cells/60-mm dish) and=20 allowed to attach for 24 h, then the cells were switched to = medium=20 containing the required amount of TG. The medium was changed = every=20 3=964 days to replenish the treatments. Cells were harvested = after=20 2 weeks, fixed, and stained with a crystal violet/formalin = solution,=20 and counted. Cell survival was estimated from the number of=20 colonies formed, expressed as a percentage of the number of=20 colonies in the control dishes. Assays were set up in = quadruplicate,=20 and SDs used instead of standard errors.

Sequencing of p53 Gene in Tumor=20 Lines.
Total RNA was isolated from 70=9680% confluent cells = with=20 RNAzol B (Tel-Test Inc.), and reverse-transcription PCR = (GeneAmp=20 RNA PCR kit; Perking Elmer) was performed using the following = conditions (for cDNA: room temperature for 10 min, 37=B0C = for 1=20 h, 90=B0C for 3 min, and 4=B0C for 5 min; PCR: 95=B0C for 2 = min, 94=B0C for=20 30 s, 58=B0C for 50 s, and 72=B0C for 45 s, 37 cycles. Final = elongation=20 was done for 10 min at 72=B0C). Three sets of overlapping = regions were=20 sequenced (forward and reverse sequences); primers used are=20 described in Table 1 .


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  		Table 1 p53 reverse = transcription-PCR=20 primer sequence and description =

 = ;
Genetic=20 Analysis.
Presence and extent of allelic loss and = microsatellite=20 instability were assessed by a broad panel of polymorphic=20 microsatellites situated at the following genomic loci: 1p = (D1S407,=20 D1S1193, and MYCL), 9p21 (D9S251 and D9S254), 10q23 (D10S520 = and=20 D10S1173), 17p13 (D17S974, D17S1289, D17S1303, and TP53), and = 19q=20 (D19S400 and D19S559). DNA extracts from the xenografts used, = under=20 various treatment conditions, and also from human = nonpolyposis=20 colorectal cancers displaying microsatellite instability = (positive=20 controls), were PCR amplified across each microsatellite = using=20 flanking oligonucleotide primers bearing fluorescent labels = for=20 quantitative detection (GeneScan; Applied Biosystems). = Nucleic acid=20 amplification was performed according to manufacturer=92s=20 instructions (GeneAmp kit; Perkin-Elmer-Cetus). The PCR = products=20 underwent capillary electrophoresis (ABI 310; Applied = Biosystems)=20 with quantitative determination of polymorphic alleles.=20 Non-neoplastic tissue from the source of the cells was not = available.=20 Instead, the untreated cell line served as the starting point = of=20 the analysis with all of the microsatellites manifesting = single=20 alleles classified as noninformative for this analysis. = Allelic=20 balance was determined to be present when the peak height = ratio=20 formed by dividing the longer allele by the shorter allele = fell=20 into the numerical range from 0.66 to 1.50. Low-level allelic = loss was said to be present when the ratio was between 0.50 = and=20 0.66 or 1.5 and 2.0. High-level allelic loss was assessed as = being=20 present when the allelic ratio fell below 0.50 or above 2.0. = The=20 closer the values approach 0 or infinity, the greater the = degree of=20 allelic imbalance. All of the analyses were performed in = triplicate=20 with the average taken for the three readings. Under these=20 conditions, at least 50% of the cells contributing DNA to = individual=20 analyses would be required to have hemizygous loss for = high-level=20 allelic loss to be detected.


3D"   =20 RESULTS
Top
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
3D"RESULTS
DISCUSSION
REFERENCES
 
T= he=20 resistance of glioma cell lines to TMZ and its correlation = with=20 levels of expression of MGMT is shown on Table 2 . Unlike BCNU, the cytotoxicity of which = closely=20 parallels MGMT activity (30)=20 , there was not a clear correlation between MGMT activity and = response to TMZ at the range of MGMT expressed by these cell = lines=20 and xenografts. For example, SWB77 was markedly more = resistant than=20 SWB95 despite a lower level of MGMT activity. Similarly, = SWB33 and=20 SWB40 showed different sensitivity to TMZ despite comparable = levels=20 of MGMT activity, and SWB39 was quite resistant despite a low = level=20 of MGMT activity.


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  		Table 2 The resistance of glioma = cell=20 lines to TMZ depends on MGMT =

 = ;
TMZ=20 itself is quite effective in reducing MGMT activity levels = below 10=20 fmol/mg protein (Fig. 1) , so that moderate levels of MGMT activity in = a tumor=20 (<70 fmol/mg protein) are not playing an active role in = the=20 resistance of tumors to this agent (30)=20 . Clearly other resistance mechanisms are in play.



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  		Fig. 1. Time course of depletion = of MGMT=20 activity in SWB40 tumor xenografts after treatment with 240=20 mg/m2 TMZ (3D{circ}=20),=20 180 mg/m2 BG (=95), or 250 mg/m2 dBG = (). Mean of three determination; bars, = =B1SD. =

 = ;
Table=20 3 shows the p53 status of the glial tumors used in = this=20 study. Three of the tumors had wtp53 sequence (SWB61, SWB40,=20 and D54), whereas the other 4 had mutated p53 (SWB95, SWB77,=20 SWB39, and SWB33). Although the susceptibility of SWB40 and=20 SWB61, and the resistance of SWB77 and SWB39 to TMZ = correlated=20 with their p53 status, the mutational status in p53 alone did = not determine the resistance of tumors to TMZ by itself. For=20 example, the relative resistance of D-54 as compared with = either=20 SWB40 or SWB61 to TMZ was unexpected, because this tumor had = no=20 detectable MGMT and expressed wtp53. Its resistance could be=20 associated to inefficient p21 induction after treatment with = TMZ. In=20 comparison, the sensitive tumor lines SWB61 and SWB40 showed = a robust=20 p21 induction in response to TMZ treatment (Fig. 2) . Unlike tumors having wt p53, those with mutated p53 = did=20 not induce a higher level of p21 protein in response to TMZ=20 treatment.


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  		Table 3 p53 status of human = glioma cell=20 lines =

 = ;


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  		Fig. 2. Effect of TMZ on the = expression of=20 p21 in glioma cell lines. Glioma cell lines were exposed to = TMZ (100=20 =B5M) for 1 h in serum-free = conditions, after=20 which cells were lysed, and proteins both in the nuclear and = cytosolic fractions separated by SDS-PAGE and probed for = expression=20 of p21 as described in "Materials and Methods." Each lane = was loaded=20 with 30 =B5g protein. Blots were subsequently stripped and = reprobed=20 for =DF-actin to ensure equal loading and transfer. Values = represent=20 the means for three independent experiments performed in = triplicate;=20 bars, =B1SD. =

 = ;
Expression=20 of p21 succeeded the translocation of phosphorylated p53 to = the=20 nucleus. Nuclear translocation of p53 was robust in SWB61, = SWB40, and=20 to a lesser extent in D-54, whereas there was only marginal = response=20 in lines with mutated p53 sequences (Fig. 3) . In SWB95, which had a mutated p53 sequence, the = p53=20 was phosphorylated but did not show significant nuclear=20 translocation. Despite the failure of p53-mutated tumors to=20 phosphorylate p53, trigger induction of p21 protein level, = and induce=20 G1-S arrest, the TMZ-induced DNA damage caused = significant=20 perturbations of cell cycle populations in all of the p53 = mutant=20 lines tested with the exception of SWB77 (Fig. 4) . Although these perturbations were less = persistent or=20 pronounced than those seen in cells expressing wtp53, such as = SWB61=20 and SWB40 (Fig. 4) , it was evident that persistent cell cycle = checkpoint=20 arrests were also induced by mechanisms that were = p53-independent in=20 glial tumors.



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  		Fig. 3. Effect of TMZ on the = expression=20 and nuclear translocation of phosphorylated p53 in glioma = cell=20 lines. Glioma cell lines exposed to TMZ (100 =B5M) for 1 h in serum-free conditions, after = which=20 cells were lysed, proteins in the nuclear and cytosolic = fraction=20 separated by SDS-PAGE, and probed for expression of = phosphorylated=20 p53 as described in "Materials and Methods." Each lane was = loaded=20 with 30 =B5g protein. Blots were subsequently stripped and = reprobed=20 for =DF-actin to ensure equal loading and transfer. Values = represent=20 the means for three independent experiments performed in = triplicate;=20 bars, =B1SD. =

 = ;


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  		Fig. 4. Cell cycle distribution = of glioma=20 cell cultures treated with TMZ. Glioma cells were grown to = 70%=20 confluence treated with BG (20 =B5M) = and TMZ (100=20 =B5M) harvested at the times = indicated, stained=20 for propidium iodide, and analyzed by flow cytometry. The = results=20 were analyzed by MODFIT LT statistics program (Verity Inc.,=20 Burlington, MA). The distribution of nuclei in = G1, S, and=20 G2 with various DNA contents is shown for SWB77, = SWB39=20 (not responding, mut-p53), SWB33, SWB95 (responding, = mut-p53),=20 SWB40, and SWB61 (responding, wt-p53). =

 = ;
The=20 importance of cell cycle arrest in the effectiveness of = treatment of=20 glial tumors to TMZ is demonstrated in Table 4 . The extent of TMZ-induced apoptosis during=20 exponential growth of glial cells in culture was directly = related to=20 the extent of cell cycle arrest. The larger apoptotic indices = were=20 observed in SWB40 and SWB61, and SWB95 followed by SWB33. = SWB77 and=20 SWB 39 did not show significant apoptotic responses after=20 exposure to TMZ whereas marked responses were observed in the = p53-deficient lines SWB33 and SWB95 (Fig. 5) . Thus, apoptosis was not necessarily = associated with a=20 wtp53 sequence in glial tumors but rather with a = functional=20 mechanism to arrest the cell cycle in response to TMZ induced = damage.


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  		Table 4 Effect of cell cycle = arrest on=20 apoptosis in glial cell tumor cells (in vitro) =

 = ;


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  		Fig. 5. Effect of TMZ on = apoptosis in=20 glial cell cultures. Immunocytochemical staining of = apoptotic cells=20 in mocked (B), SWB40 (D), SWB 95 (F), = SWB 39=20 (H), D-54 (J), and SWB 77 (L) 48 h = after=20 treatment with 100 =B5M TMZ, = respectively.=20 Left panels show transmission image of the field = shown on the=20 right. Cells were grown in cover slides to 80% = confluence,=20 fixed, and stained for TUNEL as described in "Materials and=20 Methods." Controls treated similarly but without primary = antibody=20 were run in parallel to ensure staining specificity. = Bar, 100=20 =B5m. =

 = ;
Correlations=20 between the expression of p53/p21, cell cycle arrest, and = apoptosis=20 similar to those observed in culture also applied in = xenografts 48 h=20 after their treatment with TMZ. Expression of phosphorylated = p53 and=20 p21 was evident in SWB40, SWB61, and D-54, but not SWB77, 95, = or 39=20 after a single injection of 400 mg/m2 TMZ in mice = bearing=20 these tumor xenografts (Fig. 6) . The correlation between apoptosis and glial = tumor=20 cells that undergo cell cycle arrest is also evident in = comparisons=20 between SWB95 and SWB77 (Table 5) .



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  		Fig. 6. Effect of TMZ on p53=20 phosphorylation, p53 translocation to the nucleus, and = expression of=20 p21 on glial tumor xenografts. Animals carrying glial tumor=20 xenografts (350 + 25 mm3) were treated = with a=20 single dose of TMZ (400 mg/m2) and killed 24 and = 48 h=20 after treatment (five animals at each time point). Response = to the=20 drug as determined by expression of p21 and phosphorylated = p53 was=20 similar at these two time points, but apoptosis in = responding tumor=20 xenografts was more robust at 48 h after treatment. = Panels=20 1=964 correspond to SWB40, D-54, = SWB77, and=20 SWB95, respectively. A, B, and C are stained = with=20 H&E and for phosphorylated p53 and p21 plus methyl green = counterstain, respectively. Note the robust expression of=20 phosphorylated p53 and p21 in SWB40 (B1 and = C1,=20 respectively) in the nuclei and the intense staining for p53 = and p21=20 in apoptotic cells (arrows). Expression of p53 = (nuclear) and=20 p21 (cytoplasmic) is observed in D-54 = (B2 and C2) but to a much lesser extent than = their=20 respective expression in SWB40. Lack of expression of p53 = and p21 in=20 SWB77 in response to TMZ treatment (B3 and C3) = is in=20 agreement with the absence of apoptotic cells (A3). = Weak=20 staining of cytosol for phosphorylated p53 is observed in = SWB95=20 (B4), but there is no expression of p21 (C4). = Original=20 magnification x400. =

 = ;

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  		Table 5 Apoptotic indices in = glioma=20 xenografts after treatment with TMZ =

 = ;
The=20 apoptotic response of cells to TMZ treatment could be attributed = to=20 differences in MMR among the lines tested and possible greater = MMR=20 effectiveness in cell lines with wtp53 to restrict propagation=20 through the cell cycle as long as=20 O6-methylguanine:thymine mismatches exist. = A=20 defective MMR could explain why the resistance of SWB77 to = TMZ is=20 only partially reversed by MGMT inhibition, as well as its = poor=20 apoptotic response, and the absence of G2 cell cycle=20 blocks to TMZ-induced damage. Thus, MMR was examined by = direct=20 measurement of MMR proteins (Table 6) and by the TG assay (Fig. 7) using LoVo, a MMR-deficient tumor line, as a control. = Our=20 results show the following. First, all of the brain tumor = cell=20 lines we tested, including SWB77, expressed similar levels of = all of the key MMR proteins that characterize functional MMR. = Second, SWB77 was as sensitive as SWB40 or SWB61 to TG and an = order of magnitude less resistant than the MMR-defective = LoVo.=20 Finally, genetic analysis for presence and extent of allelic=20 loss in cell lines assessed by a broad panel of polymorphic=20 microsatellites indicated that treatment with TMZ does not = result=20 in microsatellite sequence slippage.


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  		Table 6 Levels of MMR proteins = in glioma=20 xenografts =

 = ;


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  		Fig. 7. TG toxicity for SWB77, = SWB40, and=20 the control MMR-deficient cell line LoVo (marked by 3D{circ}=20,=20 3D{blacksquare}=20,=20 3D{triangledown}=20,=20 respectively). The graph represents clonogenic efficiency = with=20 increasing concentrations of TG. Assays were set up as = described in=20 "Materials and Methods," and results are shown as number of = colonies=20 formed (as a percentage of the number of colonies in control = plates); bars, =B1SD. Assays were set up in = quadruplicate and=20 repeated in at least three independent runs. =

 = ;
When=20 allelic loss genotyping was performed on a broad panel of 13=20 microsatellites, only 4=965 markers were found to be = informative in any=20 given cell line consistent with a high degree of allelic loss = already=20 present in the untreated glioma lines used in this study. All = of the=20 informative markers in the untreated cell lines showed = allelic=20 balance of polymorphic alleles. After treatment with BG and = TMZ, as=20 reported previously (28)=20 , xenografts exhibited various degrees of allelic loss in = informative=20 markers. Noteworthy in this regard was the finding that all = of the=20 pretreatment informative markers developed various degrees of = allelic=20 imbalance indicating clonal expansion of glioma cells with = greater=20 genomic structural damage. Two patterns of acquired allelic = loss were=20 evident with respect to the manner in which individual cell = lines=20 responded to BG and TMZ treatment. In the first pattern, all = of the=20 informative markers showed only low-level allelic loss. This = was true=20 for the D-54, SWB40, and SWB61, and indicated significant = admixture=20 of nonmutated and mutated glioma cells in the tumors. In the = second=20 pattern of response, a very high degree of allelic imbalance = was=20 noted with near total replacement of pretreated xenografts = with=20 tumors showing allelic loss for all of the remaining markers. = It=20 is noteworthy that SWB77 xenografts regrown in animals = treated=20 with TMZ were entirely mutated (Table 7) .


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[in=20 this window]
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  		Table 7 Allelic loss resulting = from=20 treatment of glial tumor xenografts with BG and TMZ =

 = ;

3D"   =20 DISCUSSION
Top
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
3D"DISCUSSION
REFERENCES
 
T= he=20 results presented here indicate that mechanisms of sensitivity = and=20 resistance to TMZ and presumably to other methylating agents = is much=20 more complex than the mechanism involved in the resistance to = BCNU=20 and other bifunctional alkylating agents. The low to moderate = levels=20 of MGMT found in the majority of human glial tumors do not=20 effectively protect against TMZ, because TMZ alone is = effective in=20 suppressing such MGMT levels for up to 24 h.

The most effective mechanism of resistance of glial tumors to = TMZ=20 has been identified here as the loss of the p53-inducible = cell cycle=20 checkpoint. Apoptosis in glial tumors can be associated with = a=20 functional p53 cycle and correlates with a robust and = extensive=20 G1-S cell cycle arrest in response to TMZ-induced = damage.=20 Tumors that had either a mutated p53 sequence or showed a = sluggish=20 response in mobilizing p21, exhibited higher levels of = resistance=20 than tumors with an active p53 response to DNA damage. With = the=20 exception of SWB77, which does not arrest in G1-S = after=20 treatment with up to 200 =B5M TMZ, cell = cycle=20 arrest (in S phase) was observed in all of the treated cell=20 lines regardless of expression of wt- or mut-p53, although = the=20 extent of the arrest correlated with p53 functional status = being=20 most pronounced in wt-p53-expressing cells. Arrest in = G2/M=20 phase was also observed only in mut-p53 cells and not in = wt-p53=20 cells, which is in agreement with a previous report (20)=20 .

An additional mechanism of resistance to methylating agents = is=20 related to deficiencies in MMR repair (20=20 ,=20 30, 31,=20 32)=20 . Despite the expected toxicity by the action of MMR on=20 unrepaired O6-methyl G:T or C pairs, which = are=20 recognized by MSH2 or MLH1, glial tumor xenografts show = variable=20 resistance to methylating drugs that does not correlate with = either=20 their MGMT level nor with their MMR status. The failure of = TMZ to=20 yield a uniform response in the MMR-efficient glial tumor = xenografts=20 used in this study suggests that MMR is not the only factor=20 determining the response of glial tumors to DNA-methylating = drugs,=20 and it may not even be the major one. Because MMR deficiency = is=20 thought to be low among glial tumors (33)=20 , factors that either limit capacity of MMR to kill cells = carrying=20 unrepaired mutations or even factors unrelated to such = mechanism may=20 determine the response of glial tumors to chemotherapy or = radiation=20 in the clinic. That encourages additional search for=20 understanding the limitations of MMR in tumors and also for = seeking=20 alternate pathways of tumor resistance to therapy. =

The question of MGMT control by genes such as p53, which = are=20 already linked to the susceptibility of gliomas to treatment, = clearly deserves additional investigation. For example, = enforced=20 expression of wt-p53 has been reported to curtail = transcription=20 of the MGMT gene in human tumor cells, thus enhancing = their=20 response to alkylating agents (34)=20 . Whether the ectopic expression of p53 modulates resistance = to DNA=20 damage by down-regulating MGMT or enhances the response of = apoptotic=20 pathways remains to be seen. Our results do not demonstrate a = correlation between expression of wt-p53 and MGMT level in = the glial=20 tumors examined. Even more importantly, the response to TMZ = as=20 determined by apoptosis was entirely unrelated to MGMT levels = regardless of the mutational status of p53. A direct = involvement of=20 MGMT in the response of gliomas to TMZ may apply in tumors=20 expressing MGMT levels well above those of the xenografts = used in=20 this study (18)=20 , but such correlation does not seem applicable for the = majority of=20 glial tumors, which express MGMT levels below 100 fmol/mg=20 protein.

Our data also demonstrate that the resistance of tumor cells = that=20 cannot repair O6-methylguanine adducts because of = their=20 low MGMT expression appears not to be related to MMR status, = as=20 it has been suggested previously (18)=20 . The MMR status of the cell lines used in this study was = determined=20 by the TG assay, which indicated similar efficiency of the = overall=20 mismatch-mediated repair in these lines. Microsatellite = analysis=20 after treatment of xenografts with BG and TMZ revealed that = tumors=20 regrown several weeks from treatment had a replication error = negative=20 phenotype, which also indicates MMR efficiency. Finally, = Western=20 analysis for MSH2 (which binds G-T mismatches), MLH1, which = along=20 with MSH2 defines the methylation-sensitive phenotype, and = PMS1=20 showed high levels of expression and movement to the nucleus=20 after DNA damage with TMZ. Although such analysis is = extensive=20 and convincing for a functional MMR system, it is still = possible=20 that methodologies applied here may not be sufficient to = detect=20 subtle differences in MMR response that could had defined the = variable toxicity of the tumors to TMZ treatment.

The large extent of mutations allowed in SWB77 after treatment = and=20 regrowth implies that MMR does not always lead to cell death = and that=20 cells escaping the MMR-imposed cell cycle blocks may also = escape=20 scrutiny regarding the integrity of their genome. On the = other hand,=20 the lower incidence of mutations during regrowth of SWB40 and = 61=20 indicates a much stricter control of mismatches by MMR, which = may=20 take place during p53-dependent lengthy cell cycle = checkpoints=20 imposed on these tumors after TMZ treatment. The differences = in the=20 extent of allelic loss between SWB61 and SWB77, the most = responsive=20 and most resistant gliomas to TMZ, respectively, can only = result from=20 differences in cell cycle responses to DNA damage and not = from=20 differences in the capacity to repair of=20 O6-methylguanine adducts, which would have=20 predicted a more rapid repair in SWB77 than in SWB61. In = fact, the=20 capacity of glial xenografts to repair alkylation damage is = severely=20 restricted by the complete suppression of MGMT levels for at = least 24=20 h after TMZ treatment or even 48 h after the combination of = BG and=20 TMZ. Overall, the present study demonstrates a limited MMR=20 involvement in repair of glial tumors, which appear to = possess highly=20 functional MMR systems.

Although p53 status is useful in characterizing individual = tumors=20 and classes of tumors, our data indicate that at least for = glial=20 tumors mutated p53 is not always an accurate predictor of = drug=20 sensitivity and resistance. The fact that data are emerging = to=20 support both positive and negative correlations between p53 = mutations=20 and drug sensitivity supports our observation (35)=20 and suggests a need to account for the discrepancies. Our = data=20 suggest that in brain tumors it is likely that cell cycle=20 checkpoints, most notably those induced by a functional p53 = response,=20 favor apoptosis and reduce the chance of mutations induced by = methylating chemotherapeutic agents.


3D"   =20 FOOTNOTES
 
The costs of publication of this article were = defrayed=20 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.

1 Supported by National = Cancer=20 Institute Grants CA 57725, CA84461, and CA 78561. =

2 To whom requests for = reprints=20 should be addressed, at Department of Pathology, University = of=20 Pittsburgh Cancer Institute, Pittsburgh, PA 15261. Phone: = (418)=20 648-9850; Fax: (412) 383-9822; E-mail: Kokkinakisdm{at}msx.upmc.edu

3 The abbreviations used = are: BCNU,=20 1,3-bis(2-chloroethyl)-1-nitrosourea; MGMT,=20 O6-methylguanine-DNA methyltransferase; BG,=20 O6-benzylguanine; dBG,=20 O6-benzyl-2'-deoxyguanosine; MMR, mismatch repair; = TMZ,=20 temozolomide; wt, wild type; TUNEL, terminal deoxynucleotidyl = transferase (Tdt)-mediated nick end labeling; TG, = thioguanine.=20

Received 10/31/01; revised 4/ 3/02; accepted 4/18/02.


3D"   =20 REFERENCES
Top
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
3D"REFERENCES
&nb= sp;

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J. A. Quinn, A. Desjardins, J. Weingart, H. Brem, M. E. = Dolan, S.=20 M. Delaney, J. Vredenburgh, J. Rich, A. H. Friedman, D. A. = Reardon, et=20 al.
Phase I Trial of Temozolomide Plus = O6-Benzylguanine=20 for Patients With Recurrent or Progressive Malignant = Glioma
J.=20 Clin. Oncol., October 1, 2005; 23(28): 7178 - 7187. =
[Abstrac= t]=20 [Full=20 Text] [PDF] =
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R. N. Trivedi, K. H. Almeida, J. L. Fornsaglio, S. = Schamus, and R.=20 W. Sobol
The Role of Base Excision Repair in the = Sensitivity=20 and Resistance to Temozolomide-Mediated Cell = Death
Cancer=20 Res., July 15, 2005; 65(14): 6394 - 6400.
[Abstract]=20 [F= ull=20 Text] [PDF]=20
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D. M. Kokkinakis, X. Liu, S. Chada, M. M. Ahmed, M. M. = Shareef, U.=20 K. Singha, S. Yang, and J. Luo
Modulation of Gene = Expression in=20 Human Central Nervous System Tumors under Methionine = Deprivation-induced=20 Stress
Cancer Res., October 15, 2004; = 64(20): 7513 -=20 7525.
[Abstract]=20 [F= ull=20 Text] [PDF]=20
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S. C. Schold Jr., D. M. Kokkinakis, S. M. Chang, M. S. = Berger, K.=20 R. Hess, D. Schiff, H. I. Robins, M. P. Mehta, K. L. Fink, R.L. = Davis,=20 et al.
O6-Benzylguanine suppression of=20 O6-alkylguanine-DNA alkyltransferase in anaplastic=20 gliomas
Neuro-oncol, January 1, 2004; 6(1): = 28 - 32.=20
[Abstract]=20 [PDF]<= /A>=20
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K. Vera, L. Djafari, S. Faivre, J.-S. Guillamo, K. = Djazouli, M.=20 Osorio, F. Parker, C. Cioloca, B. Abdulkarim, J.-P. Armand, et = al.
Dose-dense regimen of temozolomide given every = other=20 week in patients with primary central nervous system=20 tumors
Ann. Onc., January 1, 2004; 15(1): = 161 - 171.=20
[= Abstract]=20 [Full= =20 Text] [PDF] =
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D. M. Kokkinakis, M. M. Ahmed, D. Chendil, R. C. = Moschel, and A.=20 E. Pegg
Sensitization of Pancreatic Tumor Xenografts to = Carmustine and Temozolomide by Inactivation of Their = O6-Methylguanine-DNA=20 Methyltransferase with O6-Benzylguanine or=20 O6-Benzyl-2'-Deoxyguanosine
Clin. Cancer Res.,=20 September 1, 2003; 9(10): 3801 - 3807.
[Abstract]=20 [Full=20 Text] [PDF= ]=20
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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; 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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_0031_01C87193.4532D6B0 Content-Type: application/octet-stream Content-Transfer-Encoding: quoted-printable Content-Location: http://clincancerres.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 if (name =3D=3D "margin-right") {=0A= e.style.marginRight =3D value;=0A= }=0A= else if (name =3D=3D "margin-top") {=0A= e.style.marginTop =3D value;=0A= }=0A= else if (name =3D=3D "min-height") {=0A= e.style.minHeight =3D value;=0A= }=0A= else if (name =3D=3D "overflow") {=0A= e.style.overflow =3D value;=0A= }=0A= else if (name =3D=3D "overflow-x") {=0A= e.style.overflowX =3D value;=0A= }=0A= else if (name =3D=3D "overflow-y") {=0A= e.style.overflowY =3D value;=0A= }=0A= else if (name =3D=3D "padding") {=0A= e.style.padding =3D value;=0A= }=0A= else if (name =3D=3D "padding-bottom") {=0A= e.style.paddingBottom =3D value;=0A= }=0A= else if (name =3D=3D "padding-left") {=0A= e.style.paddingLeft =3D value;=0A= }=0A= else if (name =3D=3D "padding-right") {=0A= e.style.paddingRight =3D value;=0A= }=0A= else if (name =3D=3D "padding-top") {=0A= e.style.paddingTop =3D value;=0A= }=0A= else if (name =3D=3D "page-break-after") {=0A= e.style.pageBreakAfter =3D value;=0A= }=0A= else if (name =3D=3D "page-break-before") {=0A= e.style.pageBreakBefore =3D value;=0A= }=0A= else if (name =3D=3D "pixelBottom") {=0A= e.style.pixelBottom =3D value;=0A= }=0A= else if (name =3D=3D "pixelHeight") {=0A= e.style.pixelHeight =3D value;=0A= }=0A= else if (name =3D=3D "pixelLeft") {=0A= e.style.pixelLeft =3D value;=0A= }=0A= else if (name =3D=3D "pixelRight") {=0A= e.style.pixelRight =3D value;=0A= }=0A= else if (name =3D=3D "pixelTop") {=0A= e.style.pixelTop =3D value;=0A= }=0A= else if (name =3D=3D "pixelWidth") {=0A= e.style.pixelWidth =3D value;=0A= }=0A= else if (name =3D=3D "posBottom") {=0A= e.style.posBottom =3D value;=0A= }=0A= else if (name =3D=3D "posHeight") {=0A= e.style.posHeight =3D value;=0A= }=0A= else if (name =3D=3D "position") {=0A= e.style.position =3D value;=0A= }=0A= else if (name =3D=3D "posLeft") {=0A= e.style.posLeft =3D value;=0A= }=0A= else if (name =3D=3D "posRight") {=0A= e.style.posRight =3D value;=0A= }=0A= else if (name =3D=3D "posTop") {=0A= 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{=0A= e.style.scrollbarHighlightColor =3D value;=0A= }=0A= else if (name =3D=3D "scrollbar-shadow-color") {=0A= e.style.scrollbarShadowColor =3D value;=0A= }=0A= else if (name =3D=3D "scrollbar-track-color") {=0A= e.style.scrollbarTrackColor =3D value;=0A= }=0A= else if (name =3D=3D "float") {=0A= e.style.styleFloat =3D value;=0A= }=0A= else if (name =3D=3D "table-layout") {=0A= e.style.tableLayout =3D value;=0A= }=0A= else if (name =3D=3D "text-align") {=0A= e.style.textAlign =3D value;=0A= }=0A= else if (name =3D=3D "text-align-last") {=0A= e.style.textAlignLast =3D value;=0A= }=0A= else if (name =3D=3D "text-autospace") {=0A= e.style.textAutospace =3D value;=0A= }=0A= else if (name =3D=3D "text-decoration") {=0A= e.style.textDecoration =3D value;=0A= }=0A= else if (name =3D=3D "textDecorationBlink") {=0A= e.style.textDecorationBlink =3D value;=0A= }=0A= else if (name =3D=3D "textDecorationLineThrough") {=0A= e.style.textDecorationLineThrough =3D value;=0A= }=0A= else if (name =3D=3D 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