From: Subject: Cannabinoids Induce Glioma Stem-like Cell Differentiation and Inhibit Gliomagenesis -- Aguado et al. 282 (9): 6854 -- Journal of Biological Chemistry Date: Thu, 21 Feb 2008 10:18:49 +0100 MIME-Version: 1.0 Content-Type: multipart/related; type="text/html"; boundary="----=_NextPart_000_0000_01C87473.263B9840" X-MimeOLE: Produced By Microsoft MimeOLE V6.00.2900.3198 This is a multi-part message in MIME format. ------=_NextPart_000_0000_01C87473.263B9840 Content-Type: text/html; charset="Windows-1252" Content-Transfer-Encoding: quoted-printable Content-Location: http://www.jbc.org/cgi/content/full/282/9/6854 Cannabinoids Induce Glioma Stem-like Cell = Differentiation and Inhibit Gliomagenesis -- Aguado et al. 282 (9): 6854 = -- Journal of Biological Chemistry
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Originally=20 published In Press as doi:10.1074= /jbc.M608900200=20 on January 2, 2007=20

J. Biol. Chem., Vol. 282, Issue 9, 6854-6862, March = 2,=20 2007
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Cannabinoids Induce Glioma Stem-like Cell Differentiation and = Inhibit=20 Gliomagenesis*3D"Formula

Tania Aguado3D{ddagger}=201,=20 Arkaitz Carracedo3D{ddagger}=20, = Boris=20 Julien3D{ddagger}2,=20 Guillermo Velasco3D{ddagger}=20, = Garry=20 Milman3D=A7, Raphael Mechoulam3D=A7=20, = Luis=20 Alvarez=B6, Manuel Guzm=E1n3D{ddagger}=20, and = Ismael Galve-Roperh3D{ddagger}=203<= /NOBR>=20

From the 3D{ddagger}=20Department of=20 Biochemistry and Molecular Biology I, School of Biology, Complutense = University,=20 28040 Madrid, Spain, the 3D=A7=20Department of=20 Medicinal Chemistry and Natural Products, School of Pharmacy, Hebrew = University,=20 91120 Jerusalem, Israel, and the =B6Research Unit, = La Paz=20 University Hospital, 28046 Madrid, Spain=20

Received for publication, September 18, 2006 , and in revised form, = December=20 19, 2006.=20


3D"   =20 ABSTRACT
3D"TOP
3D"ABSTRACT
3D"INTRODUCTION
3D"EXPERIMENTAL PROCEDURES
3D"RESULTS
3D"DISCUSSION
3D"REFERENCES
 
G= lioma=20 stem-like cells constitute one of the potential origins of = gliomas,=20 and therefore, their elimination is an essential factor for = the=20 development of efficient therapeutic strategies. Cannabinoids = are=20 known to exert an antitumoral action on gliomas that relies = on at=20 least two mechanisms: induction of apoptosis of transformed = cells and=20 inhibition of tumor angiogenesis. However, whether = cannabinoids=20 target human glioma stem cells and their potential impact in=20 gliomagenesis are unknown. Here, we show that glioma = stem-like cells=20 derived from glioblastoma multiforme biopsies and the glioma = cell=20 lines U87MG and U373MG express cannabinoid type 1 = (CB1)=20 and type 2 (CB2) receptors and other elements of = the=20 endocannabinoid system. In gene array experiments, CB = receptor=20 activation altered the expression of genes involved in the = regulation=20 of stem cell proliferation and differentiation. The = cannabinoid=20 agonists HU-210 and JWH-133 promoted glial differentiation in = a CB=20 receptor-dependent manner as shown by the increased number of = S-1003Dbeta- and glial=20 fibrillary acidic protein-expressing cells. In parallel, = cannabinoids=20 decreased the cell population expressing the neuroepithelial=20 progenitor marker nestin. Moreover, cannabinoid challenge = decreased=20 the efficiency of glioma stem-like cells to initiate glioma = formation=20 in vivo, a finding that correlated with decreased = neurosphere=20 formation and cell proliferation in secondary xenografts. = Gliomas=20 derived from cannabinoid-treated cancer stem-like cells were=20 characterized with a panel of neural markers and evidenced a = more=20 differentiated phenotype and a concomitant decrease in nestin = expression. Overall, our results demonstrate that = cannabinoids target=20 glioma stem-like cells, promote their differentiation, and = inhibit=20 gliomagenesis, thus giving further support to their potential = use in=20 the management of malignant gliomas.


3D"   =20 INTRODUCTION
3D"TOP
3D"ABSTRACT
3D"INTRODUCTION
3D"EXPERIMENTAL PROCEDURES
3D"RESULTS
3D"DISCUSSION
3D"REFERENCES
 
M= alignant=20 gliomas remain the most deadly human brain tumors, with poor=20 prognosis despite years of research in anti-tumoral = therapeutic=20 strategies. A hallmark characteristic of gliomas is their = molecular=20 and cellular heterogeneity (1, 2), = which=20 is considered one of the reasons for their high malignancy = and=20 recurrence. Moreover, even morphologically or histologically=20 related tumors may behave very differently. Neoplastic = transformation=20 of differentiated glial cells was for many years the most = accepted=20 hypothesis to explain the origin of gliomas (1, 2). = However,=20 recent findings support the existence of a stem cell-derived=20 origin for different types of cancers such as gliomas and=20 hematopoietic, breast, and prostate tumors (2, 3). In=20 particular, glioma-derived stem-like cells (GSCs)4 = have been=20 isolated from both human brain tumors (4-8) and = several=20 glioma cell lines (6, 9, 10). = GSCs=20 are crucial for the malignancy of gliomas (8-10) = and may=20 represent the consequence of transformation of the normal = neural=20 stem cell compartment (11). = These=20 findings are in line with the observation that gliomagenesis = is=20 frequently associated with adult brain germinal zones, in = particular=20 the subventricular zone (2, 3).= It=20 is therefore imperative that the development of new therapeutic=20 strategies for the management of gliomas takes into account=20 their cellular diversity and origin. Among those strategies,=20 cannabinoid-based drugs may represent an alternative to other = established chemotherapeutics (12).

The discovery of an endogenous cannabinoid system (13),=20 together with the great improvement in our understanding of = the=20 signaling mechanisms responsible for cannabinoid actions (12, 13), = has=20 fostered the interest in the potential therapeutic = applications=20 of cannabinoids (14). = Several=20 studies have demonstrated a significant antitumoral action of = cannabinoid ligands in animal models (12).=20 Thus, cannabinoid administration to nude mice curbs the = growth=20 of different tumors, including gliomas, lung adenocarcinomas, = thyroid epitheliomas, lymphomas, and skin carcinomas (12). = The=20 antitumoral action on gliomas relies on at least two = mechanisms:=20 induction of apoptosis of tumor cells (15, 16) = and=20 inhibition of tumor angiogenesis (17). = Besides=20 their wide distribution in tumor cells, cannabinoid receptors = are=20 expressed and functionally active in neural progenitors, in = which=20 they regulate cell proliferation and differentiation (18, 19). = This=20 background prompted us to investigate the actions of = cannabinoids on=20 human GSCs and their impact in gliomagenesis. Our results = show that=20 GSCs express cannabinoid receptors and that cannabinoid = stimulation=20 reduces glioma initiation in vivo, a finding that = correlates=20 with increased cell differentiation. These findings provide = further=20 support for cannabinoid-based antitumoral therapies that are = able=20 to target the brain tumor stem cell compartment.


3D"   =20 EXPERIMENTAL PROCEDURES
3D"TOP
3D"ABSTRACT
3D"INTRODUCTION
3D"EXPERIMENTAL PROCEDURES
3D"RESULTS
3D"DISCUSSION
3D"REFERENCES
 
<= I>Materials=97The=20 following materials were kindly donated as indicated: = SR141716=20 and SR144528=20 (Sanofi-Aventis, Montpellier, France), JWH-133 (J. Huffman),=20 anti-mouse cannabinoid type 1 (CB1) receptor = polyclonal=20 antibody (K. Mackie), and anti-trimethyl-histone H3 = (Lys9)=20 polyclonal antibody (Upstate;= I.=20 Flores). Mouse anti-human nestin monoclonal antibody and=20 anti-Musashi-1 polyclonal antibody were from Chemicon, and = rabbit=20 anti-Ki-67 monoclonal antibody (clone SP6) was from Lab = Vision Corp.=20 Anti-cannabinoid type 2 (CB2) receptor polyclonal = antibody=20 was from Affinity BioReagents, and anti-S-1003Dbeta=20 antibody was from = Swant.=20 Recombinant human epidermal growth factor (EGF) and = fibroblast growth=20 factor 2 (FGF-2) were from R&D Systems. Mouse anti-3Dbeta=20-tubulin III = monoclonal=20 antibody was from Covance = Inc., and=20 anti-glial fibrillary acidic protein (GFAP), = anti-MAP2=20 (microtubule-associated protein 2), and = anti--tubulin=20 antibodies were from Sigma. Glioblastoma multiforme (World = Health=20 Organization grade IV astrocytoma) samples were provided by = the=20 Tissue Bank Network of the Molecular Pathology Program of the = Spanish=20 National Cancer Centre.

GSC Culture and Gliomagenesis in Vivo=97GSCs were = obtained=20 from human brain tumor biopsies digested with collagenase = (type=20 Ia, Sigma) in Dulbecco's modified Eagle's medium at 37 =B0C = for=20 90 min (17)=20 and grown under non-adherent conditions (19)=20 in neural stem cell culture medium composed of Dulbecco's = modified=20 Eagle's and Ham's F-12 media supplemented with B-27 = (Invitrogen),=20 50 mM Hepes, 2 =B5g/ml heparin, 20 ng/ml = EGF, 20 ng/ml=20 FGF-2, and 20 ng/ml leukemia inhibitory factor. Of eight = biopsies=20 employed, five rendered cells that fulfilled stem-like cell = criteria=20 (3).= =20 Representative results are shown for one of these GSC lines = and=20 were also extended to GSCs derived from classical human = glioma U87MG=20 and U373MG cell lines. Cell lines were grown as described (15, 17) = and=20 inoculated in vivo, and after tumor digestion, GSCs = were=20 cultured. Clonal neurospheres were grown at 1000 cells/ml and = analyzed by flow cytometry for the expression of different = stem cell=20 markers, including CD133, the stem cell factor receptor = c-Kit, and=20 their ability to exclude Hoechst 33342 (side population = analysis).=20 Differentiation experiments were performed in polyornithine-coated=20 plates, and adherent GSCs were grown in neural stem cell = culture=20 medium without growth factors. GSCs were cultured in the = presence=20 of the indicated stimuli after overnight growth factor = deprivation.=20

Differentiation experiments with at least three independent=20 cultures were performed by quantification of the percentage = of=20 total cells that expressed the indicated neural antigens or = that were=20 highly positive for histone H3 trimethylated at = Lys9. A=20 minimum of 10 fields were scored in a double-blinded manner = to=20 minimize subjective interpretations. Quantified fields were = selected=20 randomly by visualizing total cells with a microscope Hoechst = filter.=20 Stock solutions of cellular effectors were prepared in=20 Me2SO, and the concentrations employed were selected = based=20 on previous studies on cannabinoid regulation of neural = progenitors=20 (19).=20 No significant influence of Me2SO on any of the = parameters=20 determined was observed at the final concentration used = (0.1%,=20 v/v). Control incubations included the corresponding vehicle=20 content. Gliomagenesis was induced by subcutaneous flank = inoculation=20 into athymic nude mice of U87MG-GSCs or glioblastoma = multiforme=20 (GBM) GSCs in 100 =B5l of phosphate-buffered saline = supplemented=20 with 0.1% glucose (16). = In some=20 experiments, 1.5 mg/kg JWH-133 or the corresponding vehicle = was=20 administered daily to subcutaneous gliomas. Tumor growth was = measured=20 with an external caliper, and volume was calculated as (43D{pi}/3) x (width/2)2x (length/2).

Fluorescence-activated Cell Sorter Analysis=97GSCs were=20 dissociated with Accutase (Innovative Cell Technologies Inc., = San Diego, CA) following the manufacturer's instructions; = cells=20 (0.5 x = 106/condition) were=20 fixed in 2% paraformaldehyde at 4 =B0C in phosphate-buffered = saline;=20 and nonspecific binding was blocked using 2% goat serum in=20 phosphate-buffered saline. Antibodies and their corresponding = controls were incubated for 30 min at 4 =B0C in 2% goat=20 serum/phosphate-buffered saline, and cells (10,000/recording) = were=20 analyzed using a FACSCalibur flow cytometer. = Phycoerythrin-conjugated=20 anti-CD133 (Miltenyi Biotec, Bergisch Gladbach, Germany) and=20 phycoerythrin/Cy5-conjugated anti-CD117 (c-Kit; BD = Biosciences)=20 antibodies were employed following the manufacturer's=20 instructions.

mRNA Detection and Quantification=97mRNA was obtained = with an=20 RNeasy Protect kit (Qiagen Inc., Valencia, CA) using an RNase-free=20 DNase kit. cDNA was subsequently obtained using a SuperScript = first-strand cDNA synthesis kit (Roche Applied Science), and=20 amplification of cDNA was performed with the following = primers:=20 human CB1, CGT GGG CAG CCT GTT CCT CA (sense) and CAT = GCG=20 GGC TTG GTC TGG (antisense; 403-bp product); human = CB2,=20 CGC CGG AAG CCC TCA TAC C (sense) and CCT CAT TCG GGC CAT TCC = TG=20 (antisense; 502-bp product); human fatty acid amide = hydrolase, TGG=20 GAA AGG CCT GGG AAG TGA ACA (sense) and GCC GCA GAT GCC GCA = GAA=20 GGA G (antisense; 458-bp product); human monoacylglycerol=20 lipase, ACC CTG GGC TTC CTG TCT TCC TTC (sense) and TTC CTG = CCG=20 TGG CTG TCC TTT GAG (antisense; 564-bp product); human = TRPV1=20 (transient receptor potential cation = channel,=20 subfamily V, member 1), CGC CGC CAG CAC CGA GAA = (sense) and=20 ACC GAG TCC CTG GCG CTG ATG TC (antisense; 546-bp product); = human=20 glyceraldehyde-3-phosphate dehydrogenase, GGG AAG CTC ACT GGC = ATG GCC=20 TTC C (sense) and CAT GTG GGC CAT GAG GTC CAC CAC (antisense; = 318-bp=20 product); human Musashi-1, GAT GGT CAC TCG GAC GAA GAA = (sense) and=20 CAA ACC CTC TGT GCC TGT TG (antisense; 149-bp product); human = nestin, GAG AGG GAG GAC AAA GTC CC (sense) and TCC CTC AGA = GAC TAG=20 CGC AT (antisense; 128-bp product); human NOTCH1, GCC GCC TTT = GTG CTT CTG TTC (sense) and CCG GTG GTC TGT CTG GTC GTC=20 (antisense; 251-bp product); human OCT4, GAC AAC AAT GAA AAT = CTT CAG=20 GAG A (sense) and TTC TGG CGC CGG TTA CAG AAC CA (antisense;=20 217-bp product); and human SOX2, GCA CAT GAA CGG CTG GAG CAA = CG=20 (sense) and TGC TGC GAG TAG GAC ATG CTG TAG G (antisense; = 206-bp=20 product). CB1 and CB2 receptor PCR=20 amplifications were performed under the following conditions: = 93 =B0C=20 for 1 min; two rounds at 59 =B0C for 30 s, 72 =B0C for 1 min, = and 93 =B0C=20 for 30 s; two rounds at 57 =B0C for 30 s, 72 =B0C for 1 min, = and=20 93 =B0C for 30 s; and 35 cycles at 55 =B0C for 30 s, 72 = =B0C for 1=20 min, and 93 =B0C for 30 s. Finally, after a final extension = step at 72=20 =B0C for 5 min, PCR products were separated on 1.5% agarose = gels.=20 Real-time quantitative PCR was performed with TaqMan probes = (Applied=20 Biosystems, Foster City, CA). Amplifications were run in a = 7700=20 real-time PCR system, and the values obtained were adjusted = using 18=20 S RNA levels as a reference.

cDNA Arrays=97Total RNA was extracted from vehicle- or=20 HU-210-treated GBM-GSCs cells, and poly(A)+ RNA = was=20 isolated with Oligotex resin (Qiagen Inc.) and = reverse-transcribed=20 with Moloney murine leukemia virus reverse transcriptase in = the=20 presence of 50 =B5Ci of [3D{alpha}=20-33P]dATP for the=20 generation of radiolabeled cDNA probes. Purified radiolabeled = probes=20 were hybridized to stem gene array membranes (GEArray Q = series,=20 SuperArray Bioscience Corp., Frederick, MD) according to the=20 manufacturer's instructions.5=20 Hybridization signals were detected using a PhosphorImager = and=20 analyzed using Phoretix housekeeping genes on the blots as = internal=20 controls for normalization. The selection criteria were set=20 conservatively throughout the process, and the genes selected = were=20 required to exhibit at least a 50% change in expression. =

Western Blotting=97Western blot analysis was performed as = described previously (19). = Cleared=20 cell extracts were subjected to SDS-PAGE and transferred to=20 polyvinylidene difluoride membranes. Following incubation = with=20 primary antibodies, blots were developed with horseradish=20 peroxidase-coupled secondary antibodies using an enhanced=20 chemiluminescence detection kit. Loading controls were = performed with=20 anti-3D{alpha}-tubulin=20 antibody. Densitometric quantification of the luminograms was = performed using a GS-700 imaging densitometer (Bio-Rad) and=20 MultiAnalyst software.

Identification of Endocannabinoids in GSCs=97Samples were = dissolved in 1 volume of high pressure liquid = chromatography-grade=20 methanol and precipitated with 1 volume of acetone, and = non-miscible=20 material was filtered. The supernatant was evaporated, and = the=20 residue was partitioned between chloroform and water. A = preparative=20 TLC plate (Silica Gel 60 F24, 1 mm) was pre-developed = with=20 chloroform/methanol (1:1, v/v). Then, the residue of the = chloroform=20 layer was redissolved and applied to a Finnigan LCQ MS = detector.=20 Detection was performed using the electrospray ionization = technique=20 with the full-scan mass spectrometric mode, providing a full = spectrum=20 of samples between m/z 100 and 550. The rest of = the=20 mixture was loaded onto a TLC plate (40:6:1 (v/v)=20 chloroform/petroleum ether/methanol) with synthetic = anandamide and=20 2-arachidonoylglycerol as references. The plate was scrapped, = and=20 after methanol extraction, filtrates were analyzed by gas=20 chromatography-mass spectrometry with an electron impact = detector=20 (Hewlett-Packard G1800 GCD HP-5971) after derivatization with = the=20 silylating agent N,O-bis(trimethylsilyl)trifluoroacetamide = to=20 form trimethylsilyl ethers at free hydroxyl groups.

Immunofluorescence and Confocal = Microscopy=97Immunofluorescence=20 was performed in 10-=B5m tumor sections or in cultured cells = as=20 described previously (17, 18). = Samples=20 were incubated with the indicated antibodies and their = corresponding=20 secondary antibodies, either anti-rabbit or anti-mouse = antibody=20 highly cross-adsorbed with Alexa Fluor 488 (Molecular = Probes). CB=20 receptor expression was determined with anti-rabbit secondary = antibody highly cross-adsorbed with Alexa Fluor 594. The = number of=20 positive cells was normalized to the total cell number = identified by=20 counterstaining with TOTO-3 iodide or Hoechst 33342. GSC=20 differentiation was determined in a minimum of five tumor = sections.=20 The human origin of the cells immunostained with the = different neural=20 markers was confirmed by double labeling with anti-human = nucleus=20 antibody (Chemicon). Tumor section CD133 staining was = performed with=20 non-conjugated antibody (Miltenyi Biotec) as described (7) and = for in=20 vitro cells after 50 mM = ClNH4=20 incubation for autofluorescence treatment. Preparations were = examined=20 using Leica software and a Leica SP2 acoustical optical beam = splitter=20 microscope with two passes with a Kalman filter and a = 1024X1024=20 collection box.

Statistical Analysis=97The results shown represent the = means=20 =B1 S.E. of the number of experiments indicated in every = case.=20 Statistical analysis was performed by analysis of variance, = and post=20 hoc analysis was performing using Student's t test.


3D"   =20 RESULTS
3D"TOP
3D"ABSTRACT
3D"INTRODUCTION
3D"EXPERIMENTAL PROCEDURES
3D"RESULTS
3D"DISCUSSION
3D"REFERENCES
 
<= I>Glioma-derived=20 Stem Cells Express CB Receptors=97To investigate the = potential=20 effects of cannabinoids on GSCs, we first analyzed whether = these=20 cells express CB receptors. GSCs derived from GBM biopsies = and human=20 glioma U87MG and U373MG cell lines were cultured and = generated=20 neurosphere structures equivalent to those formed by normal = neural=20 stem cells (Fig.=20 1A). Clonal GSC cultures were subjected to = subsequent=20 neurosphere passages and showed unlimited self-renewal = ability=20 (supplemental Fig.=20 1A). Thus, we characterized in detail their = stem-like cell=20 characteristics. Immunostaining evidenced a high expression = of the=20 neural stem cell markers Musashi-1 and nestin (Fig. = 1A),=20 with many cells coexpressing both proteins (supplemental Fig. = 1B). In addition, flow cytometry analysis showed a=20 CD133-positive cell population (supplemental Fig. 1C), = the=20 size of which depended on the tumor of origin. The = CB1 and=20 CB2 receptors were shown by double immunofluorescence = to=20 colocalize in nestin-positive cells both in vitro (Fig.=20 1A) and in glioma xenografts (Fig. = 1B);=20 the CB1 and CB2 receptors were present = in 49 =B1=20 5 and 31 =B1 7% of the nestin-positive cells, respectively. = Western=20 blotting of GSC cultures was also used to analyze the = presence of CB=20 receptors (Fig.=20 1C). Reverse transcription PCR analysis confirmed = the=20 expression of stemness markers, including CD133, nestin, = Musashi-1,=20 SOX2, and NOTCH1, and the pluripotency embryonic stem cell = marker=20 OCT4 in GSCs (Fig. = 1D).=20 These findings correlated with enhanced CB receptor = expression of=20 GBM- and U87MG-GSC populations compared with their respective = differentiated counterparts. In particular, GSCs were = significantly=20 enriched in CB2 receptors at both the transcript = and=20 protein levels, in line with the correlation between astrocytoma=20 malignancy and CB2 receptor expression (16). = Other=20 elements of the endocannabinoid (eCB) signaling system were = also=20 present in GSCs, including TRPV1 and the hydrolases=20 monoacylglycerol lipase and fatty acid amide hydrolase, = enzymes=20 responsible for eCB degradation (Fig. = 1D).=20 Finally, GSCs were evaluated for their ability to produce = endogenous=20 cannabinoid ligands upon incubation with the calcium = ionophore A23187=20 [GenBank]=20 (5 =B5M, 2 min) and = subsequent=20 identification by LCQ mass spectrometry (supplemental Table = 1).=20 Several major species of 2-monoacylglycerols were detected,=20 specifically palmitoylglycerol and stearoylglycerol. In = addition,=20 2-arachidonoylglycerol and N-arachidonoylglycine, a = metabolite=20 of anandamide, were present in the samples at trace levels. = Gas=20 chromatography-mass spectrometry analysis after = derivatization with=20 N,O-bis(trimethylsilyl)trifluoroacetamide confirmed = the data=20 obtained by LCQ mass spectrometry (supplemental Table = 1).



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  = 		FIGURE 1.
Glioma stem-like = cells=20 express CB receptors. A, immunofluorescence of = GBM- and=20 U87MG-GSCs reveals the expression of Musashi-1 (Msh1) = and=20 nestin (green) together with the presence of = CB1=20 and CB2 receptors (red). Scale bars = =3D 40=20 =B5m. B, shown is CB receptor and nestin expression = in glioma=20 xenografts. Scale bar =3D 20 =B5m. C, GBM-, = U87MG-, and=20 U373MG-GSCs express human (h) CB1 and=20 CB2 receptors as shown by Western blotting. -tub, 3D{alpha}=20-tubulin. D,=20 reverse transcription PCR analysis determined the expression = of=20 transcripts for the following components of the eCB system: = the=20 CB1 and CB2 receptors, TRPV1, fatty = acid amide=20 hydrolase (FAAH), and monoacylglycerol lipase = (MAGL).=20 The indicated stem cell-related gene transcripts were = analyzed in=20 GSCs and their differentiated counterparts. GAPDH,=20 glyceraldehyde-3-phosphate dehydrogenase. =

 = ;
CB=20 Receptor Activation Contributes to the Regulation of Glioma = Stem Cell=20 Gene Expression=97To identify the potential action of = cannabinoids=20 on GSCs, we investigated the changes in gene expression = induced by=20 the synthetic cannabinoid agonist HU-210 (30 nM)=20 in GBM-GSCs. HU-210 significantly altered the expression of = 11 genes=20 (Fig.=20 2A) of the 266 genes analyzed. Among them, seven = genes=20 involved in regulation of the cell cycle and cell = proliferation=20 (CDK4 (cyclin-dependent kinase 4),=20 CDKN1B (cyclin-dependent kinase=20 inhibitor 1B), FGFR1 (FGF receptor = 1),=20 FGFR3 (FGF receptor-3), EGF = receptor,=20 EGF, and integrin 3D{alpha}4) were down-regulated by cannabinoid stimulation. = In=20 addition, the transcript levels of neuronal MAP2 and = the tumor=20 suppressor RBL1 (retinoblastoma-like = 1)=20 were increased. These results were confirmed by real-time=20 quantitative PCR analysis of three transcripts (Fig. = 2B)=20 and suggest that CB receptor activation regulates essential = GSC=20 functions such as cell proliferation and differentiation. = However,=20 GSC proliferation and self-renewal were not affected by = cannabinoid=20 stimulation during several neurosphere passages (data not = shown). The=20 impact of CB receptor activation on differentiation-related = genes=20 was therefore determined by quantitative PCR analysis. HU-210 = treatment increased the mRNA levels of the glia-specific = markers=20 GFAP and S-1003Dbeta inaCB1 receptor-dependent manner as evidenced by = SR141716=20 antagonism (Fig. 3, = A and=20 B, respectively). In addition, CB1 = receptor=20 activation resulted in increased expression of the early = neuronal=20 marker 3Dbeta-tubulin=20 III (Fig.=20 3C).

Cannabinoids Promote Neural Differentiation of Glioma Stem=20 Cells=97On the basis of the results of cannabinoid = regulation of=20 differentiation-related genes, we next analyzed the = regulation of=20 GBM-GSC differentiation by the CB1 and = CB2=20 receptor agonists HU-210 and JWH-133 alone or in combination = with the=20 receptor antagonists SR141716,=20 SR144528,=20 and capsazepine. Activation of the CB1 and = CB2=20 receptors, as demonstrated by the use of their respective=20 antagonists, decreased the nestin-positive cell population = (Fig. = 4A)=20 and increased the more differentiated cell population = expressing the=20 glial markers GFAP and S-1003Dbeta=20 (Fig. 4, = B and=20 C, respectively) or the neuronal marker 3Dbeta=20-tubulin III (Fig. = 4D).=20 Capsazepine did not modify the cannabinoid-induced decrease = in=20 nestin-positive cells and the induction of GFAP- and 3Dbeta=20-tubulin = III-positive=20 cells, although it counteracted the S-1003Dbeta=20-positive cell = increase=20 (supplemental Fig. 2). Histone methylation status has been = shown to=20 correlate with changes in neural progenitor cell = differentiation (20),=20 and thus, methylation of histone H3 at Lys9 was = monitored.=20 HU-210 and JWH-133 increased the number of trimethyl-histone = H3=20 (Lys9)-labeled cells in a CB receptor-dependent = manner as=20 evidenced by SR141716=20 and SR144528=20 antagonism (Table=20 1). In summary, these experiments confirmed the neural = progenitor=20 ability of GSC cultures that, under differentiation = conditions,=20 attach and recapitulate their endogenous differentiation = program.=20 Aberrant GSC differentiation was observed, as previously = reported (5, 6, 21).=20 Similarly, cannabinoids induce both neuronal (3Dbeta-tubulin III) and = glial=20 (GFAP) gene expression (Fig. = 3). Many=20 cells were observed to coexpress both glial and neuronal = markers=20 (supplemental Fig. 1D), which, in the case of normal = neural=20 stem-derived cells, segregate in different cell = compartments.=20


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  = 		TABLE 1
Cannabinoid = regulation of histone H3 methylation

Methylation of histone H3 at Lys9 (meK9-H3) = was=20 determined in GSCs after differentiation in the presence of = vehicle=20 (Control), 30 nM HU-210 alone or with = 2 =B5M=20 SR141716, 2 =B5M SR141716 alone, 30 nM JWH-133=20 alone or with 2 =B5M SR144528, or 2 =B5M SR144528 alone. =

 = ;



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  = 		FIGURE 2.
Gene expression = changes in=20 cannabinoid-treated glioma stem-like cells. A,=20 HU-210-induced changes in GBM-GSCs were analyzed by stem = gene array.=20 Selected changes in gene expression were significantly = different=20 (p < 0.01 versus control cells). B,=20 cannabinoid regulation of the EGF receptor (EGFR),=20 FGFR1, and FGFR3 transcripts was confirmed by=20 quantitative PCR. Results correspond to three independent=20 experiments. **, p < 0.01. C, = control. =

 = ;



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  = 		FIGURE 3.
Cannabinoid = regulation of=20 glioma stem-like cell gene expression in vitro.=20 A-C, real-time PCR analysis of GFAP, S-1003Dbeta=20, = and3Dbeta=20-tubulin = III (-tubIII) expression, respectively, in GSCs = treated=20 with 30 nM HU-210, 2 =B5M=20 SR141716 (SR1), or both and normalized to 18 S RNA = transcript=20 levels. Results correspond to three independent experiments. = **, p < 0.01 versus the control=20 (C). =

 = ;
Cannabinoids=20 Inhibit Gliomagenesis Initiated by Glioma Stem = Cells=97Stem-like=20 cells are considered to be the initiating cell population of=20 tumorigenesis. Thus, when injected in nude mice, U87MG- and = GBM-GSCs=20 induced tumor formation at cell numbers that were 30- and = 10-fold=20 lower, respectively, than their differentiated counterparts = (0.25=20 x 106 U87MG-GSCs and 1 = x 106 GBM-GSCs were = injected=20 to initiate tumor formation). As cannabinoid receptor = activation=20 regulates GSCs, we sought to determine their impact on the = ability of=20 GSCs to initiate glioma generation in vivo. U87MG-GSCs = previously cultured in the presence of 30 nM = HU-210=20 or JWH-133 were less efficient as tumor-initiating cells (Table = 2).=20 Moreover, cannabinoid-treated GSCs generated tumors with a = lower=20 growth rate, resulting in smaller tumor size compared with=20 vehicle-treated cells (Fig. = 5A=20 and Table = 2).=20 Similarly, HU-210- and JWH-133-treated GBM-GSCs were less = efficient=20 in initiating gliomagenesis (Fig.=20 5B and Table = 2). In=20 particular, HU-210 notably reduced tumor growth, whereas in = the case=20 of JWH-133, tumors were visible only 2 months after the rest = of the=20 animals had been killed (Fig. = 5B=20 and data not shown). Samples of GSC-derived gliomas were = obtained,=20 and their ability to form primary spheres was determined. = Tumors=20 generated by cannabinoid-treated GSCs showed decreased=20 neurosphere-forming activity (Fig. = 6A)=20 and reduced cell proliferation (Ki-67-positive cells) (Fig. 6, = B and=20 C). These observations confirm that cannabinoids = inhibit=20 stem-like cell-initiated gliomagenesis.


View = this=20 table:
[in this=20 window]
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  = 		TABLE 2
Cannabinoid = regulation of glioma stem-like cell-initiated = gliomagenesis

HU-210- and JWH-133-treated cells were injected = subcutaneously=20 into mice, and the efficiency of tumorigenesis (number of = mice that=20 generated tumors relative to total injected mice and the=20 corresponding percentages), relative tumor growth, and tumor = weight=20 at the end of the experiment were evaluated. =

 = ;



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  = 		FIGURE 4.
Cannabinoid = regulation of=20 glioma stem-like cell differentiation in vitro. = Left=20 panels, quantification of nestin-positive (A),=20 GFAP-positive (B), S-1003Dbeta=20-positive=20 (C), and 3Dbeta-tubulin III (3Dbeta=20-tubIII)-positive (D) cells = (green)=20 versus total cells. Cannabinoid-induced = differentiation was=20 analyzed after a 4-day differentiation period of GBM-GSCs in = the=20 presence of vehicle (control (C)), 30 nM=20 HU-210 alone or with 2 =B5M SR141716=20 (SR1), and 30 nM JWH-133 alone = or with 2=20 =B5M SR144528 (SR2). Each = antagonist was=20 also tested alone. Results correspond to three independent=20 experiments. *, p < 0.05 versus = the=20 control; **, p < 0.01. Right = panels,=20 representative immunofluorescence images of vehicle- and=20 cannabinoid-treated cells. Cell nuclei are shown in blue. = Scale=20 bar =3D 55 =B5m. =

 = ;
To=20 analyze cannabinoid regulation of the differentiation status = of=20 GSC-derived tumors, progenitor markers were analyzed by = immunofluorescence.=20 Tumors derived from cannabinoid-treated cells showed = decreased=20 nestin immunoreactivity (Fig. = 7A),=20 a finding that was also observed in gliomas treated in = vivo=20 with JWH-133 (54 =B1 7% relative immunoreactivity = versus 100 =B1=20 8% in vehicle-treated tumors). In addition, the expression of = vimentin, a progenitor marker that has been correlated with = glioma=20 malignancy (22, 23), = was=20 also decreased (48 =B1 5% relative immunoreactivity in=20 JWH-133-treated tumors versus 100 =B1 9% in = vehicle-treated=20 tumors). Next, we analyzed the expression of differentiated=20 markers in cannabinoid-treated derived gliomas. CB receptor=20 activation increased the expression of the neuronal markers=20 MAP2 and 3Dbeta-tubulin III (Fig. 7, = B and=20 C) and increased S-1003Dbeta=20 glial=20 immunoreactivity (Fig. = 7D).=20 In agreement with a previous report (6), = GFAP=20 immunoreactivity could not be detected, but an increase in = its=20 transcript levels was observed (250 =B1 55% upon HU-210 = treatment and=20 160 =B1 20% upon JWH-133 treatment versus 100 =B1 10% = upon vehicle=20 treatment).


3D"   =20 DISCUSSION
3D"TOP
3D"ABSTRACT
3D"INTRODUCTION
3D"EXPERIMENTAL PROCEDURES
3D"RESULTS
3D"DISCUSSION
3D"REFERENCES
 
T= he recent=20 discovery of brain cancer stem cells has important = implications both=20 for the development of new therapeutic strategies for glioma=20 management and for the evaluation of potential pitfalls and = benefits=20 of currently available treatments (1-3). = Here,=20 we show that GSCs express different elements of the eCB = system,=20 including G protein-coupled receptors (CB1 and = CB2),=20 the ionotropic receptor TRPV1, and eCB-degrading enzymes = (fatty acid=20 amide hydrolase and monoacylglycerol lipase), and that=20 cannabinoid agonists target the stem-like cell compartment of = brain=20 tumors, promote GSC differentiation in a receptor-dependent=20 manner, and reduce gliomagenesis in vivo. Although no = overt=20 differences between CB1 and CB2=20 receptor-mediated actions in GSCs were evident in this study, = potential variations in their molecular mechanisms of action = may=20 occur. For instance, it is known that the CB1 = receptor=20 (but not the CB2 receptor) is coupled to the modulation = of=20 various Ca2+ and K+ channels (13) = and that=20 CB1 receptor activation is selectively regulated = by=20 cholesterol-enriched membrane microdomains (24). = In=20 addition, the different molecular species of eCBs differ in = their=20 affinity for the two CB receptor types. Thus, = 2-arachidonoylglycerol=20 rather than anandamide has been proposed as the preferential=20 ligand for CB2 receptors (25).=20 Furthermore, CB2 receptor-selective enrichment in = GSCs=20 might help to explain the observed correlation between = CB2=20 receptor expression and glioma cell malignancy (16).=20 On the other hand, capsazepine was able to prevent some of = the=20 cannabinoid actions on GSC differentiation, suggesting that=20 these ligands may also affect TRPV1 function by as yet = unknown=20 mechanisms. Altogether, these observations support that the=20 coexpression of different CB receptors in GSCs would allow = these=20 cells not only to be pharmacologically targeted by CB2=20 receptor-selective non-psychotropic ligands (14), = but also to=20 respond differentially depending on the molecular composition = of the=20 eCB tone present in the tumor niche. Those eCB molecules may = be=20 produced by GSCs and surrounding cells of neuronal and glial = origin=20 (13). = In=20 this respect, altered levels of eCBs have been reported in = human=20 GBM biopsies compared with normal brain tissue, suggesting = that=20 this family of extracellular lipid cues may be involved in = the=20 endogenous antitumoral response (26, 27).



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  = 		FIGURE 5.
Cannabinoids = inhibit=20 glioma stem cell-initiated gliomagenesis. A and = B,=20 tumor growth of U87MG- and GBM-GSCs, respectively, treated = with=20 vehicle (control (C); 3Dbullet=20), 30 = nM HU-210 (3D{circ}=20), or = JWH-133 ()=20 and injected subcutaneously into immunodeficient mice.=20 Representative images of dissected tumors are shown below. = Scale=20 bars =3D 0.5 (A) and 0.3 (B) cm. = *,=20 p < 0.05 versus the control; **, = p < 0.01. =

 = ;



View = larger=20 version (26K):
[in this=20 window]
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  = 		FIGURE 6.
Cannabinoid = inhibition of=20 tumor-derived neurosphere formation and in vivo cell=20 proliferation. A, shown is the primary sphere = formation=20 from the indicated tumor biopsies. B, cell = proliferation was=20 quantified by Ki-67 immunoreactivity in U87MG-derived = (black=20 bars) and GBM-derived (stripped bars) tumors = obtained=20 from cannabinoid- and vehicle (control (C))-treated = GSCs.=20 **, p < 0.01 versus the control. = C, representative pictures are shown for each = condition.=20 Ki-67 is shown in red, and cell nuclei are shown in = green.=20 Scale bar =3D 90 =B5m. Results correspond to three = independent=20 experiments. =

 = ;
The=20 malignancy of human brain tumors inversely correlates with = their=20 degree of differentiation as shown by increased nestin, = Musashi-1,=20 and doublecortin expression (28-30), = whereas=20 their mitotic activity is inversely correlated with their=20 increased expression of mature glial and neuronal markers (22, 23, 31).=20 Thus, compared with GBM, low-grade astrocytomas, = oligodendrogliomas,=20 and neuroblastomas have a better prognosis and much more = efficient=20 therapeutic management (1, 2). = Genetic=20 modeling of glioma origin has shown that, in addition to=20 differentiated astrocytes (32),=20 neural stem cells constitute a potential niche for malignant=20 transformation that may be more permissive for malignization=20 (11, 33). = These=20 findings were followed by the identification of brain=20 tumor-initiating cells through their selective expression of = CD133=20 (7, = 8) or = their=20 ability to exclude Hoechst 33342 (9, = 10). = The=20 existence of a brain tumor-initiating cell phenotype with = stem cell=20 features may lead in the future to potential therapeutic = strategies=20 based on enforced stem cell differentiation aimed at = decreasing brain=20 tumor-initiating ability (8, 34).=20 In this context, a strong correlation between poor glioma = prognosis=20 and the expression of a signature of neurogenesis-related = genes=20 has been reported recently (23). = Similarly,=20 radial glial progenitor cells constitute the putative origin = for=20 ependymoma (35), = and=20 neural stem cells may cause cerebellar tumors (34).=20 Finally, brain stem-like cells have been shown to reproduce a = brain=20 tumor phenotype in a more reliable manner compared with=20 differentiated transformed cells (36). = However, it=20 should be kept in mind that, in addition to much evidence = supporting=20 a role for stem-like cells in gliomagenesis and tumor biology = (3), new = studies=20 are required to provide definitive proof of the concept (37). = In=20 particular, a better understanding of the molecular = mechanisms=20 responsible for the transformation of normal neural stem = cells=20 (38, 39) = and=20 dedifferentiation of neural cells (32, 33) = and=20 of the alternative origins of GSCs (40) is = required.



View = larger=20 version (65K):
[in this=20 window]
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  = 		FIGURE 7.
Cannabinoid = regulation of=20 glioma stem-like cell differentiation in vivo. = Left=20 panels, quantification of nestin (A), MAP2 = (B),=20 3Dbeta-tubulin III (3Dbeta=20-tub = III;=20 C), and S-1003Dbeta=20 = immunoreactivity=20 (D) in HU-210- and JWH-133-treated U87MG-GSC-derived = tumors.=20 *, p < 0.05 versus the control=20 (C); **, p < 0.01. Right = panels,=20 neural markers are shown in green, and cell nuclei = are shown=20 in red. Representative immunofluorescence images of=20 cannabinoid-treated tumors are shown. Results correspond to = three=20 independent experiments. Scale bar =3D 80 =B5m. =

 = ;
Cannabinoids=20 are known to exert an antitumoral action against gliomas (15-17), = an effect=20 that has been extended to a variety of tumors of different = origins=20 (12). = Our new=20 data support that, in addition to inducing apoptosis of=20 differentiated transformed cells (12),=20 cannabinoids promote differentiation of GSCs and inhibit = tumor=20 initiation. These observations are in line with recent = findings=20 demonstrating that cannabinoid stimulation promotes = differentiation=20 of non-transformed adult neural progenitors (18, 41). = Moreover,=20 the expression of CB receptors by brain tumor-initiating = cells may=20 reflect their normal developmentally regulated expression = pattern by=20 non-transformed neural stem cells such as subventricular zone = progenitors (42) = and=20 cortical radial progenitors and hippocampal nestin type I = cells (19,=20 41).=20 These findings are thus related to the link between the = normal neural=20 stem cell compartment and tumor development (2, = 3). In=20 conclusion, our results demonstrate the action of cannabinoids = on=20 glioma stem-like cells and thus may open new avenues for=20 cannabinoid-based antitumoral strategies.


3D"   =20 FOOTNOTES
 
* This work was = supported in=20 part by Ministerio de Educaci=F3n y Ciencia Grant = SAF2006-00918,=20 Santander/Universidad Complutense Madrid Grant PR27/05-13988, = Comunidad Aut=F3noma de Madrid Grants GR/SAL589-04 and = S-SAL/0261/2006,=20 and the Fundaci=F3n Cient=EDfica de la Asociaci=F3n = Espa=F1ola Contra=20 el C=E1ncer. The costs of publication of this article were=20 defrayed in part by the payment of page charges. This article = must therefore be hereby marked "advertisement" in = accordance=20 with 18 U.S.C. Section 1734 solely to indicate this fact. = 3DBack

3D"Formula The on-line version of this article (available = at http://www.jbc.org/) = contains=20 supplemental Figs. 1 and 2 and Table 1. 3DBack

1 Supported by = the=20 Comunidad Aut=F3noma de Madrid. 3DBack

2 Supported by a = postdoctoral fellowship from the Association pour la = Recherche sur le=20 Cancer (France). 3DBack

3 Supported by = the Ram=F3n=20 y Cajal Program of the Ministerio de Educaci=F3n y Ciencia. To whom = correspondence=20 should be addressed: Dept. of Biochemistry and Molecular Biology I, = School of=20 Biology, Complutense University, c/Jos=E9 Antonio Novais s/n, 28040 = Madrid, Spain.=20 Tel.: 34-91-394-4668; Fax: 34-91-394-4672; E-mail: igr{at}quim.ucm.es .=20

4 The = abbreviations used=20 are: GSCs, glioma-derived stem-like cells; CB1,=20 cannabinoid receptor type 1; CB2, cannabinoid receptor=20 type 2; EGF, epidermal growth factor; FGF-2, fibroblast = growth=20 factor 2; GFAP, glial fibrillary acidic protein; GBM, = glioblastoma=20 multiforme; eCB, endocannabinoid. 3DBack

5 See http://www.superarray.com/ for a = detailed=20 list of the genes analyzed. 3DBack


3D"   =20 ACKNOWLEDGMENTS
 
We are = indebted to=20 our laboratory colleagues for encouragement and support; to = A. Egu=EDa,=20 J. Palazuelos, and L. Uriguen for experimental assistance; = and to M.=20 Lorente for providing samples of U87MG-derived gliomas. =



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3D"TOP
3D"ABSTRACT
3D"INTRODUCTION
3D"EXPERIMENTAL PROCEDURES
3D"RESULTS
3D"DISCUSSION
3D"REFERENCES
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Content-Location: http://www.jbc.org/javascript/ajax/xmlhttprequest.js /*=0A= =0A= Cross-Browser XMLHttpRequest v1.2=0A= =3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D= =3D=3D=3D=3D=3D=3D=3D=3D=0A= =0A= Emulate Gecko 'XMLHttpRequest()' functionality in IE and Opera. Opera = requires=0A= the Sun Java Runtime Environment .=0A= =0A= by Andrew Gregory=0A= http://www.scss.com.au/family/andrew/webdesign/xmlhttprequest/=0A= =0A= This work is licensed under the Creative Commons Attribution License. To = view a=0A= copy of this license, visit = http://creativecommons.org/licenses/by-sa/2.5/ or=0A= send a letter to Creative Commons, 559 Nathan Abbott Way, Stanford, = California=0A= 94305, USA.=0A= =0A= Attribution: Leave my name and web address in this script intact.=0A= =0A= Not Supported in Opera=0A= ----------------------=0A= * user/password authentication=0A= * responseXML data member=0A= =0A= Not Fully Supported in Opera=0A= ----------------------------=0A= * async requests=0A= * abort()=0A= * getAllResponseHeaders(), getAllResponseHeader(header)=0A= =0A= */=0A= // IE support=0A= if (window.ActiveXObject && !window.XMLHttpRequest) {=0A= window.XMLHttpRequest =3D function() {=0A= var msxmls =3D new Array(=0A= 'Msxml2.XMLHTTP.5.0',=0A= 'Msxml2.XMLHTTP.4.0',=0A= 'Msxml2.XMLHTTP.3.0',=0A= 'Msxml2.XMLHTTP',=0A= 'Microsoft.XMLHTTP');=0A= for (var i =3D 0; i < msxmls.length; i++) {=0A= try {=0A= return new ActiveXObject(msxmls[i]);=0A= } catch (e) {=0A= }=0A= }=0A= return null;=0A= };=0A= }=0A= // Gecko support=0A= /* ;-) */=0A= // Opera support=0A= if (window.opera && !window.XMLHttpRequest) {=0A= window.XMLHttpRequest =3D function() {=0A= this.readyState =3D 0; // = 0=3Duninitialized,1=3Dloading,2=3Dloaded,3=3Dinteractive,4=3Dcomplete=0A= this.status =3D 0; // HTTP status codes=0A= this.statusText =3D '';=0A= this._headers =3D [];=0A= this._aborted =3D false;=0A= this._async =3D true;=0A= this._defaultCharset =3D 'ISO-8859-1';=0A= this._getCharset =3D function() {=0A= var charset =3D _defaultCharset;=0A= var contentType =3D = this.getResponseHeader('Content-type').toUpperCase();=0A= val =3D contentType.indexOf('CHARSET=3D');=0A= if (val !=3D -1) {=0A= charset =3D contentType.substring(val);=0A= }=0A= val =3D charset.indexOf(';');=0A= if (val !=3D -1) {=0A= charset =3D charset.substring(0, val);=0A= }=0A= val =3D charset.indexOf(',');=0A= if (val !=3D -1) {=0A= charset =3D charset.substring(0, val);=0A= }=0A= return charset;=0A= };=0A= this.abort =3D function() {=0A= this._aborted =3D true;=0A= };=0A= this.getAllResponseHeaders =3D function() {=0A= return this.getAllResponseHeader('*');=0A= };=0A= this.getAllResponseHeader =3D function(header) {=0A= var ret =3D '';=0A= for (var i =3D 0; i < this._headers.length; i++) {=0A= if (header =3D=3D '*' || this._headers[i].h =3D=3D header) {=0A= ret +=3D this._headers[i].h + ': ' + this._headers[i].v + '\n';=0A= }=0A= }=0A= return ret;=0A= };=0A= this.getResponseHeader =3D function(header) {=0A= var ret =3D getAllResponseHeader(header);=0A= var i =3D ret.indexOf('\n');=0A= if (i !=3D -1) {=0A= ret =3D ret.substring(0, i);=0A= }=0A= return ret;=0A= };=0A= this.setRequestHeader =3D function(header, value) {=0A= this._headers[this._headers.length] =3D {h:header, v:value};=0A= };=0A= this.open =3D function(method, url, async, user, password) {=0A= this.method =3D method;=0A= this.url =3D url;=0A= this._async =3D true;=0A= this._aborted =3D false;=0A= this._headers =3D [];=0A= if (arguments.length >=3D 3) {=0A= this._async =3D async;=0A= }=0A= if (arguments.length > 3) {=0A= opera.postError('XMLHttpRequest.open() - user/password not = supported');=0A= }=0A= this.readyState =3D 1;=0A= if (this.onreadystatechange) {=0A= this.onreadystatechange();=0A= }=0A= };=0A= this.send =3D function(data) {=0A= if (!navigator.javaEnabled()) {=0A= alert("XMLHttpRequest.send() - Java must be installed and = enabled.");=0A= return;=0A= }=0A= if (this._async) {=0A= setTimeout(this._sendasync, 0, this, data);=0A= // this is not really asynchronous and won't execute until the = current=0A= // execution context ends=0A= } else {=0A= this._sendsync(data);=0A= }=0A= }=0A= this._sendasync =3D function(req, data) {=0A= if (!req._aborted) {=0A= req._sendsync(data);=0A= }=0A= };=0A= this._sendsync =3D function(data) {=0A= this.readyState =3D 2;=0A= if (this.onreadystatechange) {=0A= this.onreadystatechange();=0A= }=0A= // open connection=0A= var url =3D new java.net.URL(new = java.net.URL(window.location.href), this.url);=0A= var conn =3D url.openConnection();=0A= for (var i =3D 0; i < this._headers.length; i++) {=0A= conn.setRequestProperty(this._headers[i].h, this._headers[i].v);=0A= }=0A= this._headers =3D [];=0A= if (this.method =3D=3D 'POST') {=0A= // POST data=0A= conn.setDoOutput(true);=0A= var wr =3D new = java.io.OutputStreamWriter(conn.getOutputStream(), this._getCharset());=0A= wr.write(data);=0A= wr.flush();=0A= wr.close();=0A= }=0A= // read response headers=0A= // NOTE: the getHeaderField() methods always return nulls for me :(=0A= var gotContentEncoding =3D false;=0A= var gotContentLength =3D false;=0A= var gotContentType =3D false;=0A= var gotDate =3D false;=0A= var gotExpiration =3D false;=0A= var gotLastModified =3D false;=0A= for (var i =3D 0; ; i++) {=0A= var hdrName =3D conn.getHeaderFieldKey(i);=0A= var hdrValue =3D conn.getHeaderField(i);=0A= if (hdrName =3D=3D null && hdrValue =3D=3D null) {=0A= break;=0A= }=0A= if (hdrName !=3D null) {=0A= this._headers[this._headers.length] =3D {h:hdrName, = v:hdrValue};=0A= switch (hdrName.toLowerCase()) {=0A= case 'content-encoding': gotContentEncoding =3D true; break;=0A= case 'content-length' : gotContentLength =3D true; break;=0A= case 'content-type' : gotContentType =3D true; break;=0A= case 'date' : gotDate =3D true; break;=0A= case 'expires' : gotExpiration =3D true; break;=0A= case 'last-modified' : gotLastModified =3D true; break;=0A= }=0A= }=0A= }=0A= // try to fill in any missing header information=0A= var val;=0A= val =3D conn.getContentEncoding();=0A= if (val !=3D null && !gotContentEncoding) = this._headers[this._headers.length] =3D {h:'Content-encoding', v:val};=0A= val =3D conn.getContentLength();=0A= if (val !=3D -1 && !gotContentLength) = this._headers[this._headers.length] =3D {h:'Content-length', v:val};=0A= val =3D conn.getContentType();=0A= if (val !=3D null && !gotContentType) = this._headers[this._headers.length] =3D {h:'Content-type', v:val};=0A= val =3D conn.getDate();=0A= if (val !=3D 0 && !gotDate) this._headers[this._headers.length] = =3D {h:'Date', v:(new Date(val)).toUTCString()};=0A= val =3D conn.getExpiration();=0A= if (val !=3D 0 && !gotExpiration) = this._headers[this._headers.length] =3D {h:'Expires', v:(new = Date(val)).toUTCString()};=0A= val =3D conn.getLastModified();=0A= if (val !=3D 0 && !gotLastModified) = this._headers[this._headers.length] =3D {h:'Last-modified', v:(new = Date(val)).toUTCString()};=0A= // read response data=0A= var reqdata =3D '';=0A= var stream =3D conn.getInputStream();=0A= if (stream) {=0A= var reader =3D new java.io.BufferedReader(new = java.io.InputStreamReader(stream, this._getCharset()));=0A= var line;=0A= while ((line =3D reader.readLine()) !=3D null) {=0A= if (this.readyState =3D=3D 2) {=0A= this.readyState =3D 3;=0A= if (this.onreadystatechange) {=0A= this.onreadystatechange();=0A= }=0A= }=0A= reqdata +=3D line + '\n';=0A= }=0A= reader.close();=0A= this.status =3D 200;=0A= this.statusText =3D 'OK';=0A= this.responseText =3D reqdata;=0A= this.readyState =3D 4;=0A= if (this.onreadystatechange) {=0A= this.onreadystatechange();=0A= }=0A= if (this.onload) {=0A= this.onload();=0A= }=0A= } else {=0A= // error=0A= this.status =3D 404;=0A= this.statusText =3D 'Not Found';=0A= this.responseText =3D '';=0A= this.readyState =3D 4;=0A= if (this.onreadystatechange) {=0A= this.onreadystatechange();=0A= }=0A= if (this.onerror) {=0A= this.onerror();=0A= }=0A= }=0A= };=0A= };=0A= }=0A= // ActiveXObject emulation=0A= if (!window.ActiveXObject && window.XMLHttpRequest) {=0A= window.ActiveXObject =3D function(type) {=0A= switch (type.toLowerCase()) {=0A= case 'microsoft.xmlhttp':=0A= case 'msxml2.xmlhttp':=0A= case 'msxml2.xmlhttp.3.0':=0A= case 'msxml2.xmlhttp.4.0':=0A= case 'msxml2.xmlhttp.5.0':=0A= return new XMLHttpRequest();=0A= }=0A= return null;=0A= };=0A= }=0A= ------=_NextPart_000_0000_01C87473.263B9840 Content-Type: application/octet-stream Content-Transfer-Encoding: quoted-printable Content-Location: http://www.jbc.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= e.style.posTop =3D value;=0A= }=0A= else if (name =3D=3D "posWidth") {=0A= e.style.posWidth =3D value;=0A= }=0A= else if (name =3D=3D "right") {=0A= e.style.right =3D value;=0A= }=0A= else if (name =3D=3D "ruby-align") {=0A= e.style.rubyAlign =3D value;=0A= }=0A= else if (name =3D=3D "ruby-overhang") {=0A= e.style.rubyOverhang =3D value;=0A= }=0A= else if (name =3D=3D "ruby-position") {=0A= e.style.rubyPosition =3D value;=0A= }=0A= else if (name =3D=3D "scrollbar-3dlight-color") {=0A= e.style.scrollbar3dLightColor =3D value;=0A= }=0A= else if (name =3D=3D "scrollbar-arrow-color") {=0A= e.style.scrollbarArrowColor =3D value;=0A= }=0A= else if (name =3D=3D "scrollbar-base-color") {=0A= e.style.scrollbarBaseColor =3D value;=0A= }=0A= else if (name =3D=3D "scrollbar-darkshadow-color") {=0A= e.style.scrollbarDarkShadowColor =3D value;=0A= }=0A= else if (name =3D=3D "scrollbar-face-color") {=0A= e.style.scrollbarFaceColor =3D value;=0A= }=0A= else if (name =3D=3D "scrollbar-highlight-color") {=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 "textDecorationNone") {=0A= e.style.textDecorationNone =3D value;=0A= }=0A= else if (name =3D=3D "textDecorationOverline") {=0A= e.style.textDecorationOverline =3D value;=0A= }=0A= else if (name =3D=3D "textDecorationUnderline") {=0A= e.style.textDecorationUnderline =3D value;=0A= }=0A= else if (name =3D=3D "text-indent") {=0A= e.style.textIndent =3D value;=0A= }=0A= else if (name =3D=3D "text-justify") {=0A= e.style.textJustify =3D value;=0A= }=0A= else if (name =3D=3D "text-kashida-space") {=0A= e.style.textKashidaSpace =3D value;=0A= }=0A= else if (name =3D=3D "text-overflow") {=0A= e.style.textOverflow =3D value;=0A= }=0A= else if (name =3D=3D "text-transform") {=0A= e.style.textTransform =3D value;=0A= }=0A= else if (name =3D=3D "text-underline-position") {=0A= e.style.textUnderlinePosition =3D value;=0A= }=0A= else if (name =3D=3D "top") {=0A= e.style.top =3D value;=0A= }=0A= else if (name =3D=3D "unicode-bidi") {=0A= e.style.unicodeBidi =3D value;=0A= }=0A= else if (name =3D=3D "vertical-align") {=0A= e.style.verticalAlign =3D value;=0A= }=0A= else if (name =3D=3D "visibility") {=0A= e.style.visibility =3D value;=0A= }=0A= else if (name =3D=3D "white-space") {=0A= e.style.whiteSpace =3D value;=0A= }=0A= else if (name =3D=3D "width") {=0A= e.style.width =3D value;=0A= }=0A= else if (name =3D=3D "word-break") {=0A= e.style.wordBreak =3D value;=0A= }=0A= else if (name =3D=3D "word-spacing") {=0A= e.style.wordSpacing =3D value;=0A= }=0A= else if (name =3D=3D "word-wrap") {=0A= e.style.wordWrap =3D value;=0A= }=0A= else if (name =3D=3D "writing-mode") {=0A= e.style.writingMode =3D value;=0A= }=0A= else if (name =3D=3D "z-index") {=0A= e.style.zIndex =3D value;=0A= }=0A= else if (name =3D=3D "zoom") {=0A= e.style.zoom =3D value;=0A= }=0A= }=0A= catch (e) {=0A= /* ignore error on attempt to set e.style.[property] */=0A= }=0A= }=0A= }=0A= }=0A= ------=_NextPart_000_0000_01C87473.263B9840 Content-Type: application/octet-stream Content-Transfer-Encoding: quoted-printable Content-Location: http://www.jbc.org/javascript/entrez/callback.js /************************************************************************= *****=0A= * javascript/entrez/callback.js=0A= *=0A= * Entrez Linking callback to populate content box.=0A= *=0A= * Copyright 2006 Board of Trustees of the Leland Stanford Junior = University.=0A= = *************************************************************************= ***/=0A= =0A= /*=0A= * Execute callback to fill content box with Entrez Linking information.=0A= */=0A= function entrez_callback(pmid, callback_url) {=0A= /*=0A= * MSIE 5.5 and below have issues with the JavaScript=0A= * used for Entrez Linking. For now we have to disable=0A= * the callback until we can track down a proper fix=0A= * (or everybody sanely upgrades to version 6 or 7!).=0A= */=0A= if (navigator) {=0A= var appname =3D navigator.appName;=0A= if (appname =3D=3D "Microsoft Internet Explorer") {=0A= var userAgent =3D navigator["userAgent"];=0A= var s =3D "MSIE ";=0A= var n =3D -1; =0A= if ((n =3D userAgent.indexOf(s)) !=3D -1) {=0A= var v =3D parseFloat(userAgent.substring(n+s.length));=0A= if (v < 6) {=0A= return;=0A= }=0A= }=0A= }=0A= }=0A= =0A= /*=0A= * Acquire table row element to update, initiate callback=0A= * to update table with Entrez Links.=0A= */=0A= var tr =3D document.getElementById('entrez_callback_'+pmid);=0A= if (!tr) {=0A= return;=0A= }=0A= var req =3D new XMLHttpRequest();=0A= if (!req) {=0A= return;=0A= }=0A= req.onreadystatechange =3D function() {=0A= if (req.readyState =3D=3D 4 && (req.status =3D=3D 200 || req.status = =3D=3D 304)) {=0A= var src =3D req.responseXML.documentElement;=0A= var dst =3D document.createDocumentFragment();=0A= for (var i =3D 0; i < src.childNodes.length; i++) {=0A= copy_xml_to_html(src.childNodes[i], dst);=0A= }=0A= var tbl =3D tr.parentNode;=0A= tbl.replaceChild(dst, tr);=0A= }=0A= }=0A= req.open('GET', callback_url, true);=0A= req.send(null);=0A= }=0A= ------=_NextPart_000_0000_01C87473.263B9840--