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Neuro-Oncology Advance Access published online on = October=20 15, 2009
Neuro-Oncology,=20 doi:10.1093/neuonc/nop005
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Autophagy induced by valproic acid is associated with oxidative = stress in=20 glioma cell lines

Jun Fu, Cui-Jie=20 Shao, Fu-Rong Chen, Ho-Keung Ng and=20 Zhong-Ping Chen

State Key Laboratory for Cancer Research in Southern = China,=20 Department of Neurosurgery/Neuro-Oncology, Cancer Center, Sun Yat-Sen=20 University, Guangzhou, People's Republic of China (J.F., C.-J.S., = F.-R.C.,=20 Z.-P.C.); Department of Anatomical & Cellular Pathology, The Chinese = University of Hong Kong, Hong Kong, People's Republic of China (H.-K.N.) =

Corresponding Author: Zhong-Ping Chen, Cancer = Center,=20 Sun Yat-Sen University Guangzhou, Guangdong 510060, People's Republic of = China=20 (chenzp57{at}mail.sysu.edu.cn ).


3D"   =20 Abstract
Top
3D"Abstract
Patients and Methods
Results
Discussion
Funding
References
 
A= utophagy=20 represents an alternative tumor-suppressing mechanism that = overcomes=20 the dramatic resistance of malignant gliomas to radiotherapy = and=20 proapoptotic-related chemotherapy. This study reports that = valproic=20 acid (VPA), a widely used anti-epilepsy drug, induces = autophagy in=20 glioma cells. Autophagy, crucial for VPA-induced cell death, = is=20 independent of apoptosis, even though apoptotic machinery is=20 proficient. Oxidative stress induced by VPA occurs upstream = of=20 autophagy. Oxidative stress also activates the extracellular=20 signal-regulated kinase 1/2 (ERK1/2) pathway, whereas = blocking this=20 pathway inhibits autophagy and induces apoptosis. VPA-induced = autophagy cannot be alleviated by inositol, suggesting a = mechanism=20 different from that for lithium. Moreover, VPA potentiates = autophagic=20 cell death, but not apoptosis, when combined with other = autophagy=20 inducers such as rapamycin, Ly294002,=20 and temozolomide in glioma cells both in vitro and in vivo,=20 which may warrant further investigation toward possible = clinical=20 application in patients with malignant gliomas.

Keywords: autophagy, glioma, oxidative stress, valproic acid

Received July 30, 2008; Accepted June 9,=20 2009

Malignant gliomas account for = approximately 50%=20 of primary tumors in the brain. Even when a combination of = surgery,=20 chemotherapy, and radiotherapy is used, the median survival = time of=20 patients with glioblastoma multiforme (GBM), the most = malignant=20 type of glioma, is still <1 year from diagnosis.1=20 Resistance to apoptosis, a characteristic of many cancers, = especially=20 malignant glioma, underlies not only tumorigenesis but also = the=20 inherent resistance of cancer cells to radiotherapy and=20 chemotherapy.2=20 Therefore, novel strategies are essential to improve = prognosis=20 of the patients.

Increasing evidence obtained in many model systems, both in = vitro=20 and in vivo, supports the hypothesis that a variety of cell = death=20 programs may be triggered in distinct circumstances. = Autophagy, also=20 known as programmed cell death type II, represents an = alternative=20 tumor-suppressing mechanism to overcome, at least partly, the = dramatic resistance of many cancers to radiotherapy and=20 proapoptotic-related chemotherapy.2=20 Unlike apoptosis, which is a caspase-dependent process = characterized=20 by nuclear condensation and fragmentation but without major=20 ultrastructural changes in cytoplasmic organelles, autophagy = is a=20 caspase-independent process characterized by the accumulation = of=20 autophagic vacuoles in the cytoplasm accompanied by extensive = degradation of organelles, such as mitochondrias and = polyribosomes,=20 and the endoplasmic reticulum, which precedes the destruction = of the=20 nucleus.3=20 However, autophagy may also be important in the regulation of = cancer development as well as progression and in determining = the=20 response of tumor cells to anticancer therapy. Therefore, the = role=20 of autophagy is complicated and may, depending on the=20 circumstances, have diametrically opposite consequences for = the=20 tumor.4=20

Manipulation of autophagy could have the potential to improve=20 anticancer therapeutics. A number of studies have reported = that=20 autophagy, or autophagic cell death, can be activated in = gliomas,=20 in response to various anticancer therapies. Temozolomide = (TMZ),=20 a DNA-alkylating agent, can induce autophagy, but not = apoptosis,=20 in malignant glioma cells,5=20 and has demonstrated real therapeutic benefits in = apoptosis-resistant=20 GBM patients.6=20 Rapamycin, an inhibitor of the mammalian target of rapamycin = (mTOR),=20 can induce autophagy in, as well as suppress the = proliferation of,=20 malignant glioma cells.7=20 Thus, novel successes in the fight against glioblastomas = might be=20 achieved by a combination of proautophagic drugs, such as = TMZ, with=20 inhibitors of mTOR, class I PI3K, or Akt as adjuvant=20 chemotherapies.

Valproic acid (2-propylpentanoic acid, [VPA]) is a branched=20 short-chain fatty acid and has widely been used in the = management=20 of various types of epilepsy for decades. VPA has been = identified=20 as a potent selective histone deacetylase inhibitor, which = induces=20 cellular differentiation, growth arrest, and apoptosis in = gliomas=20 and other types of cancers.8=20 Other studies reported that VPA induces growth arrest, = apoptosis, and=20 senescence in medulloblastoma and glioma cell lines by = increasing=20 histone hyperacetylation and regulating expression of = p21Cip1, CDK4,=20 and c-Myc.9=9611=20 Although proapoptotic machinery was reported to be activated=20 after exposure to VPA, other mechanisms may also be involved. = Schwartz et al.12=20 reported that VPA induces nonapoptotic cell death in multiple = myeloma=20 cell lines. Nevertheless, VPA was also proven to exert = cytoprotection=20 functions and suppress apoptosis in human SY5Y neuroblastoma=20 cells.13=20 Michaelis et al.14=20 showed that VPA induces extracellular signal=96regulated = kinase=20 1/2 (ERK 1/2) activation and inhibits apoptosis in = endothelial=20 cells. However, the mechanisms underlying these effects of = VPA=20 in malignant gliomas remain poorly understood.

In this study, we investigated the role of autophagy in = VPA-induced=20 cytotoxicity and examined possible mechanisms of VPA-induced=20 autophagy in glioma cell lines.


3D"   =20 Patients and Methods
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Abstract
3D"Patients and Methods
Results
Discussion
Funding
References
 
<= A=20 name=3DS2A>Glioma Cell Lines
Human = glioma=20 cell lines such as U87MG, SF295, and T98G were used in this = study.=20 The cells were cultured in Dulbecco's modified Eagle's medium = supplemented with 10% fetal bovine serum (Hyclone, Logan, UT, = USA), 4=20 mM glutamine, 100 U/mL penicillin, and 100 =B5g/mL = streptomycin.=20

Reagents
Valproic = acid,=20 dansyl monocadaverin (MDC), propidium iodide (PI),=20 N-acetylcysteine (NAC), pan-caspase inhibitor Z-VAD-fmk=20 (zVAD), rapamycin, Ly294002, MEK1 inhibitor PD98059,=20 H2O2, inositol, and 3-methyladenosine = (3-MA)=20 were purchased from Sigma Chemical Co. (St. Louis, MO). JC-1, = 2',7'-dichlorodihydrofluorescein diacetate = (H2DCF), and=20 mitotracker red CMXRos (MTR) were purchased from Molecular = Probe=20 (Eugene, OR, USA). Microtubule-associated protein 1=96light = chain 3=20 (MAP1-LC3), Beclin 1, and cleaved caspase-3 (p17) antibodies = were=20 obtained from Santa Cruz Biotechnology (Santa Cruz, CA, USA). = ERK1/2=20 and phospho-ERK1/2 monoclonal antibodies were obtained from = Cell=20 Signaling Technology (Danvers, MA, USA).

Plasmid and = Transfection
The=20 vector pEGFP-hLC3 was constructed by inserting human MAP1-LC3 = in=20 pEGFP plasmid as described previously.15=20 The plasmid was purchased from ADDGENE plasmid sharing = service=20 (Cambridge, MA, USA). Transfection of glioma cells with = pEGFP-hLC3=20 was performed using FuGene 6 transfection reagent (Roche = Applied=20 Science, Mannheim, Germany) according to the manufacturer's=20 instruction. To quantify autophagic cells after drug = treatment, we=20 counted the number of autophagic cells demonstrated by = GFP-LC3=20 dots (3D≥=2010=20 dots/cell) among 200 GFP-positive cells.

Cytotoxicity = Assay
The=20 cytotoxic effect of VPA on glioma cell lines was determined = using a=20 Trypan blue dye-exclusion assay as described previously.5=20 Tumor cells were seeded at 5 x = 103 cells/well (0.5 mL) in 24-well flat-bottomed = plates=20 and incubated overnight. After exposure to VPA in various=20 concentrations for 96 h, the cells were trypsinized and the = number of=20 viable cells was counted. The viability of untreated cells = was=20 regarded as 100%. For coincubation with TMZ, a single = concentration=20 of VPA (0.5, 1.0, or 1.5 mM) and different concentrations of = TMZ=20 ranging from 6.25 to 400 =B5M were added to cells and = incubations=20 carried out for 96 h. The IC50 value was = calculated with=20 SPSS 10.0 statistical software.

Cell Cycle = Analysis
Cell=20 cycle analysis was performed as described previously.5=20 Briefly, after serum deprivation for 36 h, glioma cells were=20 treated with or without 1.0 mM VPA for another 96 h. Cells = were=20 trypsinized, fixed by 70% ethanol overnight, and stained by=20 Cellular DNA Flow Cytometric Analysis Reagent Set (Becton = Dickinson,=20 San Jose, CA, USA). DNA content was analyzed by the FACScans. = Data were analyzed by Cell Quest software (Becton Dickinson). =

Electron Microscopy=20 Observation
To morphologically demonstrate the induction of=20 autophagy in treated tumor cells, we performed an = ultrastructural=20 analysis as described previously.5=20 Glioma cells treated with or without 1.0 mM VPA for 96 h were = fixed=20 with ice-cold glutaraldehyde (2% in 0.1 M cacodylate buffer, = pH 7.4)=20 for 30 min. After fixation, the samples were postfixed in 1%=20 OsO4 in the same buffer for 1 h and then subjected = to the=20 electron microscopic analysis. Representative areas were = chosen for=20 ultrathin sectioning and viewed with a Philips EM 400 = transmission=20 electron microscope at an accelerating voltage of 80 kV. =

MDC Incorporation=20 Assay
Dansyl monocadaverin incorporation was quantified = using=20 procedures previously described.16=20 Cells were incubated with 0.05 mM MDC in phosphate-buffered = saline=20 (PBS) at 37=B0C for 10 min. After incubation, cells were = washed four=20 times with PBS and collected in 10 mM Tris=96HCl, pH 8.0, = containing=20 0.1% Triton X-100. Intracellular MDC was measured (excitation = wavelength 380 nm, emission filter 525 =B1 20 nm) in a = CytoFluor plate=20 reader. To normalize the measurements to the number of cells=20 present in each well, a solution of ethidium bromide was = added to=20 a final concentration of 0.2 mM and DNA fluorescence was=20 measured (excitation wavelength 530 nm, emission filter 590 = =B1=20 40 nm). The MDC incorporated was expressed as specific = activities=20 (fold to control). MDC-staining autophagic vacuoles were = visualized=20 under a Leica DMIRE2 inverted confocal microscope.

Apoptosis Detection=20 Assay
Apoptosis of VPA-treated tumor cells was detected = using an=20 annexin V-FITC kit (Biovision, Inc., California, USA), = according=20 to the manufacturer's instructions. Briefly, cells were = plated=20 on poly-lysine=96coated cover slides and treated by VPA = alone or=20 in combination. After treatment, the inverted phosphatidylserine = in=20 the outer membrane of apoptotic cells was labeled with a = fluorescent=20 isothiocyanate (FITC)-labeled annexin V. After fixing with 4% = paraformalin and counterstaining with DAPI, the cells were = examined=20 under an Olympus BX61 fluorescence microscope. Pictures were = scanned=20 with a DP71 CCD digital camera. Five hundred cells were = analyzed for=20 each sample. Each experiment was repeated three times. =

Mitochondrial Membrane = Potential=20 Assay
Mitochondrial membrane potential (MMP) was measured = using=20 the mitochondrial-specific dual-fluorescence probe, JC-1, = based=20 on the method described previously.17=20 Glioma cells were treated with VPA at different = concentrations for 96=20 h. After treatment, the medium was removed and replaced with = 10 =B5g/mL=20 of JC-1 in culture media for 10 min followed by two washes = with=20 PBS. A CytoFluor plate reader (excitation wavelength 485 nm,=20 slit width 20 nm) was used to monitor the fluorescence=20 intensities for the monomer and the aggregated JC-1 molecules = (emission wavelengths 520 nm, slit width of 25 nm, 580 nm = slit width=20 of 30 nm, respectively). Results were expressed as = fluorescence=20 ratio (580/530 nm).

Detection of Intracellular = Reactive=20 Oxygen Species
Intracellular reactive oxygen species (ROS) = was=20 detected by means of an oxidation-sensitive fluorescent probe = (H2DCF) as described previously.17=20 After drug treatment for 96 h, the cells were washed twice in = PBS and=20 then intracellular fluorescence was measured (excitation = wavelength=20 485 nm, emission filter 530 nm) in a CytoFluor plate reader. = DCF=20 fluorescence was defined as an arbitrary unit.

Immunofluorescence=20 Staining
Cells were cultured on the coverslips precoated = with=20 poly-lysine. After various treatment with drugs, the cells = were fixed=20 in 4% paraformaldehyde, permeated with 0.25% Triton X-100,=20 blocked with 3% normal goat serum, stained with first = antibody=20 overnight, and labeled with a goat anti-mouse or goat = anti-rabbit IgG=20 conjugated with FITC (Santa Cruz, CA, USA). The cells were=20 counterstained with Vectashield sealant containing=20 4',6-diamidino-2-phenylindole (DAPI) (Vector Laboratories,=20 California, USA) and examined under an Olympus BX61 = fluorescence=20 microscope. Pictures were scanned with a DP71 CCD digital=20 camera.

Western Blot = Analysis
Cells=20 were washed in cold PBS and lysed in a radioimmuno precipitation=20 assay (RIPA) buffer containing 50 mM Tris=96HCl, pH 7.4, = 150 mM=20 NaCl, 1 mM Phenylmethanesulfonyl fluoride (PMSF), 1 mM=20 Ethylenediamine tetra-acetic acid (EDTA), 5 =B5g/mL = aprotinin, 5=20 =B5g/mL leupeptin, 1% Triton X-100, 1% sodium deoxycholate, = and 0.1%=20 sodium dodecyl sulfate (SDS). The cell extract with 50 =B5g = protein was=20 loaded on a 10% or 15% SDS=96polyacrylamide gel and then = transferred to=20 a nitrocellulose membrane. The membrane was incubated for 1 h = in=20 PBS=96Tween 20 buffer containing 5% skim milk. After blotting = with=20 primary antibody, the protein expression was revealed with = the=20 appropriate horseradish peroxidase=96labeled secondary = antibody, which=20 was detected using LumiGLO chemiluminescent substrate (Cell=20 Signaling). Mouse anti-human β-tubulin was used as = internal reference=20 to ensure equal loadings.

In Vivo Treatment of = Intracerebellar=20 Xenografts with VPA
Balb/c nude (nu/nu) mice were obtained = from the=20 breeding facility at the animal center of Sun Yat-Sen = University. All=20 animal studies were performed in accordance with the = institutional=20 ethical guidelines for experimental animal care in the Cancer = Center of Sun Yat-Sen University. To establish = intracerebellar=20 xenograft models, 4-week-old mice were anesthetized with = sodium=20 pentobarbital (50 mg/kg), after which a small skin incision = (1 mm)=20 was made and a burr hole (0.7 mm in diameter) was created = with a=20 microsurgical drill. U87MG cells (105) were = suspended in 2=20 =B5l of culture medium and injected slowly through the burr = hole into=20 the right cerebellar hemisphere (1 mm to the right of the = midline, 1=20 mm posterior to the coronal suture, and 3 mm deep). The = incision=20 was closed with wound clips and removed 3 days after surgery. =

Valproic acid was dissolved in 0.9% sodium chloride solution = to a=20 final concentration of 600 mg/mL. Valproic acid solution (400 = mg/kg=20 per day for 14 days) was administered by intraperitoneal=20 injection.9=20 TMZ was administered at a dose of 40 mg/kg per day = (equivalent to 200=20 mg/m2 in humans) for 5 days by oral gavage.18=20 PBS was used as negative control. Both treatments were = started=20 on Day 3 after the implantation of tumor cells. At the end of = treatment, all mice were sacrificed. The mouse brains were = removed=20 and stored in liquid nitrogen overnight, then sectioned at = 5-=B5m=20 thickness on a MicromHM200 cryotome (Eryostar). For=20 immunohistochemical (IHC) analysis, mouse brain sections were = fixed=20 in 4% paraformaldehyde for 20 min, then permeated by 0.25% = Triton=20 X-100, and later immersed with the primary antibodies against = MAP1-LC3 (1:200) overnight at 4=B0C. IHC was performed using = the DAKO=20 ABC System (Dako, Denmark). MAP1-LC3-positive cells were = counted=20 under 10 x 40 high-power = fields and=20 expressed as percentage of total cells counted as described=20 previously.19=20

Statistical = Analysis
The=20 data were expressed as mean =B1 SD. Statistical analysis was = performed=20 using Student's t-test (two-tailed). The criterion for = statistical significance was taken as P < .05.


3D"   =20 Results
Top
Abstract
Patients and Methods
3D"Results
Discussion
Funding
References
 
<= A=20 name=3DS3A>Effect of VPA on Malignant Glioma=20 Cells
To examine the cytotoxicity of VPA on malignant glioma = cells, we treated three malignant glioma cell lines (U87MG, = T98G,=20 and SF295) with VPA at concentrations ranging from 0.25 to 10 = mM=20 for 96 h. As shown in Fig. 1A,=20 VPA increased cell death in all three cell lines in a = dose-dependent=20 manner, but their responses varied. IC50 values = for T98G,=20 U87MG, and SF295 were 3.85 =B1 0.58, 2.15 =B1 0.38, and 6.16 = =B1 0.84=20 mM, respectively. To investigate whether cell cycle arrest is = induced in glioma cells by VPA, we performed DNA flow = cytometric=20 analyses. As shown in Fig. 1B,=20 VPA treatment (1.0 mM, 96 h) increased the population at the=20 G0/G1 phase and decreased the = population at the=20 S phase in all three tested glioma cell lines. These results = indicate=20 that VPA induces G0/G1 arrest in = malignant=20 glioma cell lines. The percentage of the sub-G1=20 population, which is indicative of apoptosis, increased after = treatment with VPA in T98G, U87MG, and SF295 cells: from 0.3% = to 2.8% in T98G, from 0.4% to 7% in U87MG, and from 0.2% to = 5%=20 in SF295 cell lines, respectively.



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  		Fig. 1. Effect of VPA on = malignant glioma=20 cells. (A) Cytotoxic effect of VPA on U87MG, SF295, and T98G = glioma=20 cells for 96 h. The viability of the untreated cells was = regarded as=20 100%. Points, mean of three independent experiments; bars, = SD. (B)=20 Effect of VPA on cell cycle in three glioma cell lines. = After serum=20 deprivation for 36 h, malignant glioma cells treated with or = without=20 VPA (1.0 mM) for 96 h were collected and stained with = propidium=20 iodide and analyzed in the FACScan. The percentage of cells = in=20 different phases of the cell cycle was determined using Cell = Quest=20 software. =

 = ;
VPA Induces Autophagy in Glioma=20 Cells
To confirm the hypothesis that VPA can induce = autophagy in=20 glioma cells, we performed several analyses. Electron = microscopic=20 (EM) and GFP-LC3-labeling analyses showed that autophagic=20 vacuoles increased in the U87MG cell line treated with 1.0 mM = VPA=20 for 96 h (Fig. 2A,=20 B, and D). Most of the autophagosomes contained lamellar = structures=20 or residual digested components, whereas untreated tumor = cells=20 exhibited few such features (Fig. 2Aa=20 and Ac).



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  		Fig. 2. (A) Ultrastructural = features of=20 VPA-induced autophagy in glioma cells. The cells treated = with (1.0=20 mM) or without VPA for 96 h were harvested and fixed, and = the=20 electron microscopic observation was performed. GFP-LC3 = plasmid was=20 transfected into glioma cells 24 h before VPA treatment. (a = and c)=20 Untreated U87MG cells and (b and d) VPA-treated U87MG cells. = N=20 indicates nucleus. The arrowhead indicates autophagosome = including=20 residual digested material. Bar, a, b, 2.5 =B5m; c, d, 10 = =B5m. (B)=20 Representative Western blot showing MAP1-LC3 and Beclin-1 in = U87MG=20 cells before or after VPA exposure for dose (96 h) or for = time study=20 (1.0 mM). (C and D) MDC staining in glioma cells before or = after VPA=20 exposure for dose (96 h) or for time study (1.0 mM VPA). = *P=20 < .05, as compared to noVPA control. (E) MDC-specific = activities=20 induced by VPA (1.0 mM, 96 h) can be suppressed by autophagy = inhibitor 3-MA. *P < .05, when compared with = VPA-treated=20 group. (F) The percentage of GFP-LC3=96labeled cells in VPA = group (1.0=20 mM, 96 h) can be reduced by autophagy inhibitor 3-MA. = *P <=20 .05, when compared with VPA-treated group. Results shown are = the=20 means =B1 SD of three independent experiments. =

 = ;
To=20 quantify the incidence of VPA-induced autophagy, we used MDC=20 staining. All three glioma cell lines showed enhanced MDC-specific=20 activities that increased after treatment with VPA in either = a=20 dose- or time-dependent manner (Fig. 2C=20 and D). Moreover, addition of 3-MA inhibited the MDC = incorporation=20 after treatment with VPA (Fig. 2F).=20

In addition, we examined the expression of two MAP1-LC3 forms,=20 LC3-I and LC3-II, using Western blot analysis, since LC3-II = is=20 closely associated with the membrane of autophagosomes.15=20 Expression of LC3-II increased in U87MG cell lines treated = with=20 VPA in a dose- or time-dependent manner (Fig. 2B).=20 Similar results can also be observed for Beclin-1. GFP-LC3=20 staining also showed that addition of 3-MA decreased=20 GFP-LC3-labeling cells after treatment with VPA (Fig. 2F).=20 Combined with results revealed above, our data indicated that = VPA=20 induced autophagy in glioma cell lines.

Autophagy Is Crucial for = VPA-Induced=20 Cell Death
To further examine the role of autophagy in = VPA-induced=20 cell death, we performed Trypan blue exclusion assay and = annexin=20 V-FITC staining. The pan-caspase inhibitor Z-VAD-fmk did not=20 prevent cell death, indicating that caspase-independent death = mechanisms might be triggered by VPA in these glioma cell = lines.=20 Cell death induced by VPA can be significantly alleviated by=20 autophagy inhibitor 3-MA (2.5 mM), whereas it was only = slightly=20 affected by Z-VAD-fmk, suggesting that autophagy, rather than = apoptosis, is a crucial mechanism in the tumoricidal effect = of=20 VPA (Fig. 3A).=20 Treatment with VPA (1.0 mM, 96 h) did not dramatically = increase the=20 percentage of annexin V-FITC=96positive cells (Fig. 3B).=20 Even in apoptosis-proficient U87MG cells that harbor = wild-type p53=20 and functional caspase-3, the apoptosis rate was relatively = low (2.2=20 =B1 1.1%). In contrast, treatment with 5 =B5M cisplatin for = 48 h induced=20 apoptosis in 17.7 =B1 2.6%, 13.5 =B1 2.8%, and 22.6 =B1 3.1% = of=20 T98G, SF295, and U87MG cells, respectively. Apoptosis induced = by VPA can be neutralized by caspase inhibitor Z-VAD-fmk, = while=20 not by autophagy inhibitor 3-MA, suggesting that apoptosis is = independent of autophagy. Caspase-3 analysis showed similar=20 results (Fig. 3C).=20 Caspase-3 study also revealed that activation of caspase-3 = induced by=20 VPA can be considerably enhanced by ERK1/2 inhibitor = PD98059.=20



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  		Fig. 3. Autophagy is crucial for = VPA-induced cell death. Cells were seeded in 12-well plates = at 2=20 x 104 per mL. = At 48 h=20 after exposure to VPA (1.0 mM), 3-MA (2.5 mM), zVAD (100 = =B5M), and=20 PD98059 (10 =B5M) were added and the cells were cultured for = an=20 additional 48 h. (A) Quantification of cell death after = exposure to=20 VPA alone or in combination. Cell death was determined by = Trypan=20 blue exclusion assay. *P < .05, as compared to = noVPA=20 group, **P < .05, when compared with VPA-treated = group.=20 #P > .05, when compared with = VPA-treated group.=20 (B) Apoptosis detection in glioma cells treated with VPA = alone or in=20 combination with various drugs. After treatment, cells were = labeled=20 with annexin V-FITC, and counterstained with DAPI. Five = hundred=20 cells were analyzed for each sample. Cisplatin (5 =B5M) was = used as=20 drug control for apoptosis. *P < .05, when = compared with=20 VPA-treated group. Results were the mean =B1 SD of three = independent=20 experiments. (C) Representative Western blot showing cleaved = caspase-3 (p17) in U87MG cells following exposure to 1.0 mM = VPA=20 alone or in combination with various drugs for 96 h. = β-Tubulin was=20 used as loading control. =

 = ;
VPA-Induced Accumulation of = Mitochondrial ROS,=20 Loss of Membrane Potential, and Mitochondrial Injuries
To = confirm=20 the oxidative stress induced by VPA, we assessed the = accumulation of=20 ROS. Similar to other cell systems,17=20 VPA treatment for 96 h increased DCF fluorescence in all = three=20 cell lines (Fig. 4A).=20 This effect can be suppressed by NAC, but not autophagy = inhibitor=20 3-MA, indicating that ROS production occurs upstream of = autophagy. In=20 addition to being able to generate ROS, mitochondria are = susceptible=20 to damage by ROS. As shown in Fig. 4C=20 and D, normal mitochondria existed in a cell as = interconnected=20 tubular networks that appear as a reticulum or as multiple = individual=20 punctate organelles, while after VPA treatment (96 h), = mitochondria=20 exhibited swelling morphology, the reticular pattern was = disrupted,=20 and the number of cristae was also markedly reduced. All = these=20 results suggested that mitochondrial ROS induced by VPA might = result=20 in mitochondrial injury.



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  		Fig. 4. Oxidative stress is an = early event=20 after exposure to VPA. (A) After pretreatment with NAC (5 = mM) or=20 3-MA (2.5 mM) for 24 h in U87MG cells, VPA (1.0 mM) was = added and=20 cells were cultured for an additional 96 h.=20 H2O2 (100 =B5M, 6 h) was used as = positive=20 control. Intracellular oxidative stress was measured with = DCF=20 fluorescence intensity. *P < .05, as compared to = noVPA=20 group. **P < .05, when compared with VPA-treated = group.=20 #P > .05, when compared with = VPA-treated group.=20 Data are presented as the mean =B1 SD of three independent=20 experiments. (B) Effects of VPA on MMP assessed by the JC-1=20 fluorescent probe. U87MG cells were treated with VPA (0.25, = 0.5,=20 1.0, 1.5 mM) for up to 96 h valinomycin (10 mM) was used as = positive=20 control. NAC (5 mM) was added 24 h before VPA (1.0 mM) = treatment.=20 *P < .05, when compared with the nonVPA group. = **P=20 < .05, when compared with VPA-treated group (1.0 mM). = Values are=20 expressed as mean =B1 SD of three independent experiments. = (C)=20 Mitochondrial ROS generation in glioma cells after exposure = to VPA.=20 Representative fluorescent staining showing ROS visualized = by DCF=20 fluorescence (green), and mitochondria labeled by = mitotracker red=20 CMXRos (red) in U87MG cells yellow color indicates the=20 colocalization between ROS and mitochondria. Bar, 10 =B5m. = (D) VPA=20 treatment resulted in mitochondrial injuries. After exposure = to VPA,=20 U87MG cells were stained by mitotracker red CMXRos (MTR) or=20 collected for electron microscopic analysis. Upper panel, = bar, 1 =B5m;=20 lower panel, bar, 10 =B5m. =

 = ;
To=20 examine the effect of VPA on mitochondrial function, the = glioma cells=20 were treated with JC-1. A loss in MMP has been indicated by a = decrease in the red/green fluorescence intensity ratio. = Valproic acid=20 affected the MMP in all cell lines in a dose-dependent manner = (0.25=961.5 mM) as compared to untreated controls = (Fig. 4B).=20 The positive control, potassium ionophore valinomycin, = resulted in=20 MMP depolarization as indicated by a 50%=9660% decrease in = the=20 fluorescence intensity ratio following 15 min of treatment. A = recovery in MMP was also observed in the cells treated with 5 = mM NAC.=20 Our data confirmed the role of mitochondrial ROS in = VPA-induced=20 mitochondrial dysfunction.

Autophagy Induced by VPA Is = Regulated by=20 Oxidative Stress
To confirm the hypothesis that autophagy = induced by=20 VPA is regulated by oxidative stress, we performed several = analyses.=20 As shown in Fig. 5A,=20 cell death induced by VPA can be significantly alleviated by = ROS=20 scavenger NAC (5 mM), suggesting that oxidative stress is = crucial for=20 the tumoricidal effect of VPA. Similarly, NAC inhibited the = increase=20 of GFP-LC3 labeling cells after exposure to VPA. The addition = of=20 apoptosis inhibitor zVAD actually mildly enhanced autophagy = induced=20 by VPA, whereas inositol had no effect on VPA-induced = autophagy,=20 suggesting that autophagy is independent of apoptosis = (Fig. 5B).=20 Moreover, upregulation of LC3-II can be inhibited by NAC, = 3-MA, and=20 PD98059 in U87MG cell lines (Fig. 5D).=20 MDC staining in all cell lines showed that addition of 3-MA, = PD98059,=20 and NAC inhibited the MDC incorporation after treatment with = VPA=20 (Fig. 5C),=20 whereas inositol had no effect. Our data indicated that VPA = induced=20 autophagy in glioma cells, which was regulated by oxidative=20 stress.



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  		Fig. 5. VPA promotes autophagy = through=20 induction of oxidative stress. Cells were seeded in 12-well = plates=20 at 2 x 104 = per mL. At=20 48 h after exposure to VPA (1.0 mM), 3-MA (2.5 mM), NAC (5 = mM), zVAD=20 (100 =B5M), PD98059 (10 =B5M), or inositol (1 mM) was added = and cells=20 were cultured for an additional 48 h. (A) Quantification of = cell=20 death after exposure to VPA alone or in combination. Cell = death was=20 determined by trypan blue exclusion assay. *P < = .05, as=20 compared to the VPA-treated group. (B) Quantification of = cells=20 expressing LC3 aggregation after VPA treatment. The = percentage of=20 LC3 aggregated cells was quantitated by counting the number = of the=20 cells showing the punctate pattern of GFP-LC3 in 200 = GFP-positive=20 cells. Results shown are the means =B1 SD of three = independent=20 experiments. *P < .05, **P > .05, when = compared=20 with the VPA-treated group. (C) MDC staining in U87MG cells. = Autophagosome was labeled by MDC (green punctuate), = Magnification=20 400x. (D) Representative = Western=20 blot showing MAP1-LC3 in U87MG cells following exposure to = 1.0 mM=20 VPA alone or in combination with various drugs for 96 h. = β-Tubulin=20 was used as a loading control. =

 = ;
Role of the ERK Pathway in = VPA-Induced=20 Autophagy
Because the ERK pathway positively regulates = autophagy in=20 cancer cells,20=20 we also examined this pathway. As examined by Western blot = analysis,=20 treatment with VPA for 24=9696 h increased phosphorylated = ERK1/2=20 (p-ERK1/2) in U87MG glioma cells (Fig. 6A).=20 Immunofluorescence assay showed increased ERK 1/2 = phosphorylation=20 in the cells following VPA treatment for 96 h (Fig. 6D).=20 The activation of ERK1/2 can be inhibited by PD98059 and NAC, = suggesting the role of oxidative stress in its signaling = regulation=20 (Fig. 6A=20 and D).



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  		Fig. 6. Role of the ERK pathway = in=20 VPA-induced autophagy. (A) Representative Western blot = showing ERK=20 1/2 phosphorylation in U87MG cells after treatment without = (control)=20 or with VPA (1.0 mM) alone for 24=9696 h or with PD98059 (10 = =B5M) or=20 NAC (5 mM). (B) Apoptosis measured using annexin V-FITC = staining.=20 Cells were treated with 1.0 mM VPA alone or with 10 =B5M = PD98059 for=20 96 h. Data were the mean of triplicate experiments; error = bars, SD=20 *P < .05, as compared to the VPA-treated group. = (C)=20 Quantitation of cells with GFP-LC3 dots among cells treated = with 1.0=20 mM VPA alone or 1.0 mM VPA and 10 =B5M PD98059. Cells were = transiently=20 transfected with the GFP-LC3 plasmid for 24 h and then = treated for=20 96 h as described. The number of cells with GFP-LC3 dots was = counted, and their percentage among the total number of = cells=20 expressing GFP was determined. Data were the mean of = triplicate=20 experiments; error bars, SD *P < .05, when = compared with=20 the VPA-treated group. (D) Representative immunostaining of = p-ERK1/2=20 in U87MG cells with VPA (1.0 mM) alone or with PD98059 (10 = =B5M) and=20 NAC (5 mM) for 96 h. Bar, 10 =B5m. =

 = ;
To=20 determine whether activation of the ERK pathway is involved = in=20 VPA-induced autophagy, we used an MEK1 inhibitor, PD98059. = Expression=20 of LC3-II increased in the cells treated with VPA but = decreased in=20 the cells pretreated with PD98059 and then treated with VPA = for 96 h=20 (Fig. 5D).=20 We then determined the extent of the inhibitory effect of = PD98059 on=20 VPA-induced autophagy in glioma cell lines by examining = GFP-LC3=20 localization. The percentage of cells with GFP-LC3 dots = decreased=20 significantly in the cells treated with PD98059 and VPA = compared with=20 VPA alone (Fig. 6C).=20 The ERK pathway is known as an antiapoptosis pathway.21=20 Its inhibition by PD98059 enhanced apoptosis in VPA-treated = cells=20 (Figs. 3C=20 and 6B). These results indicated that blocking the ERK = pathway has a=20 negative effect on the VPA effect, which suggests that the = ERK=20 pathway is involved in VPA-induced autophagy in glioma cells. = ERK1/2=20 activation might constitute a mechanism through which = oxidative=20 stress regulates autophagy.

VPA Sensitized Glioma Cells to = Phosphatidylinositol 3-Kinase or mTOR Inhibitor via Augmentation of=20 Autophagy
Autophagy is activated mainly through the = disruption of=20 the PI3K/Akt/mTOR signaling pathway.7=20 Ly294002,=20 rapamycin, and TMZ are known inducers for autophagy in glioma = cells.7=20 We determined the sensitivity of malignant glioma cells to = these=20 drugs alone or in combination with VPA based on cell = viability=20 (Fig. 7A).=20 Our data showed that Ly294002,=20 rapamycin, and TMZ combined with VPA increased cell death = more than=20 they did alone. To confirm that the combinatory interactions = of these=20 drugs with VPA could be attributed to the augmentation of = autophagy,=20 we performed MDC staining and annexin V-FITC staining. As = shown in=20 Fig. 7C,=20 in U87MG, T98G, and SF295 cell lines, the combination = treatment=20 significantly increased MDC incorporation when compared with=20 the single-agent treatment. However, VPA did not = significantly=20 enhance apoptotic cell death when combined with other = autophagy=20 inducers (Fig. 7B).=20



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  		Fig. 7. VPA potentiates = autophagic cell=20 death when combined with other autophagy inducers. VPA = potentiates=20 autophagic cell death when combined with TMZ, rapamycin = (RPA), or=20 Ly294002=20 (Ly). Cells were treated with 1.0 mM VPA alone or in = combination=20 with TMZ (25 =B5M), RPA (10 nM), or Ly294002=20 (1 =B5M) for 96 h. (A) Trypan blue exclusion assay was used = to=20 evaluate cell death after drug treatment. *P < = .05, as=20 compared to TMZ, RPA, or Ly alone. (B) Apoptosis detection = in U87MG=20 and T98G glioma cells treated with VPA alone or in = combination with=20 TMZ, RPA, or Ly294002. After annexin V-FITC staining, 500 = cells were=20 analyzed for each sample. *P > .05, when compared = with=20 TMZ, RPA, or Ly294002=20 alone. (C) Quantitation of autophagic cells with MDC = incorporation=20 among cells treated with 1.0 mM VPA alone or in combination = with=20 TMZ, RPA, or Ly294002=20 for 96 h. *P < .05, when compared with TMZ, RPA, = or=20 Ly294002=20 alone. (D) VPA enhances TMZ-induced cytotoxicity. For = coincubation=20 experiments, a single concentration of VPA (0.5, 1.0, or 1.5 = mM) and=20 different concentrations of TMZ were added to cells and = incubations=20 carried out for 96 h. The viability of untreated cells was = regarded=20 as 100%. The IC50 value was calculated with SPSS = 10.0=20 statistical software. Data are the mean of triplicate = experiments;=20 error bars, SD *P < .05, when compared with TMZ = alone (no=20 VPA). =

 = ;
As=20 shown in Fig. 7D,=20 VPA enhanced TMZ-induced cytotoxicity in tested glioma cell = lines. In=20 T98G cells, IC50 of TMZ plus VPA (1.0 or 1.5 mM)=20 suppressed cell viability to <50% of that of TMZ alone. = Kanzawa et=20 al.5=20 reported that TMZ is an inducer for autophagy rather than for = apoptosis in glioma cells. Therefore, our data may reflect = the fact=20 that the combined effects might depend on the stimulation of=20 autophagic cell death.

VPA Induces Autophagic Cell = Death in=20 Intracerebellar Glioblastoma Xenografts
To assess the effect = of VPA=20 on U87MG intracerebellar glioblastoma xenografts, autophagic = effect=20 was examined by immunohistochemical staining of MAP1-LC3. In=20 PBS-treated U87MG tumors, <10% of the tumor cells were = MAP1-LC3=20 positive, and treatment with VPA caused a significant = increase of=20 MAP1-LC3 expression (Fig. 8A;=20 P < .05). In contrast to either VPA or TMZ alone, = treatment=20 with the drug combination significantly increased the = percentage=20 of MAP1-LC3=96expressing cells in U87MG tumors (Fig. 8A;=20 P < .05). Increases in necrotic cell with MAP1-LC3 = staining=20 were observed in all three drug-treated groups, and the = combination=20 of TMZ with VPA exhibited the highest level of = autophagy-related=20 cell death (Fig. 8B).=20 These results suggest that cell death induced by VPA alone or = in=20 combination with TMZ is correlated with the induction of=20 autophagy.



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  		Fig. 8. VPA induces = autophagy-related=20 death in U87MG intracerebellar xenografts.

Mice bearing intracerebellar xenografts were killed at = the end of=20 drug treatment and compared with the untreated group. (A) = The number=20 of cells identified by immunohistochemical staining with = MAP1-LC3=20 were counted in digitally captured images under high-power = (10 x 40) magnification and = graphed as the=20 percentage of total cells. Columns, mean; bars, SE. = *P <=20 .05, as compared to the PBS group (n =3D 4); = **P <=20 .05, when compared with single drug (n =3D 4). (B) = Induction of=20 autophagy in necrotic cells after drug treatment. Necrotic = cells=20 were stained with MAP1-LC3 antibody. Black arrow head = indicates the=20 site of necrotic cells with MAP1-LC3 staining. Bar, 100 = =B5m. =

 = ;

3D"   =20 Discussion
Top
Abstract
Patients and Methods
Results
3D"Discussion
Funding
References
 
V= alproic=20 acid, a commonly used drug for treating epilepsy and bipolar=20 disorders, has emerged as a promising agent for cancer = treatment in=20 recent years.8=20 In addition to clinical assessment, the experimental = examination of=20 VPA as anticancer drug is ongoing, even though many questions = regarding its underlying mechanisms remain poorly understood. = Our=20 present results indicated that VPA can induce autophagy, = which=20 constitutes the main cause of cell death instead of apoptosis = in=20 glioma cell lines. Even in apoptosis-proficient U87MG cells = that=20 harbor wild-type p53 and functional caspase-3, most of the = cell death=20 can be attributed to autophagy. Thus, following VPA = treatment, glioma=20 cells may die from a caspase-independent autophagic process = showing=20 signs of apoptosis, suggesting that cells may choose between = the=20 autophagic and the apoptotic execution pathways. Moreover, = several=20 experiments showed that the limits between apoptosis and = autophagy=20 may be tenuous and suggest either considerable overlap or=20 interdependence of both programs of cell demise.22=20 On a molecular level, this means that the apoptotic and = autophagic=20 response machineries share common pathways that either link = or=20 polarize the cellular responses.22=20

Mitochondria produce low levels of ROS as an inevitable = consequence=20 of oxidative metabolism, thus generating the MMP that drives=20 the synthesis of ATP by the F1F0-ATPase and = almost=20 all other mitochondrial functions.23=20 While under oxidative stress, ROS are generated at higher = levels,=20 inducing cellular damage and cell death.23=20 Cancer cells produce higher levels of ROS than normal cells = because=20 of increased metabolic stress and proliferative capacity, and = thus=20 may be more sensitive to oxidative stress as a result of high = endogenous ROS levels and may provide a selective mechanism = to induce=20 cell death.24=20 In this study, we demonstrated that VPA is capable of = producing=20 elevated levels of mitochondrial ROS in glioma cells. ROS = induced by=20 VPA lead to loss of MMP and mitochondrial injuries in glioma = cells,=20 which cause cytotoxicity and ultimately cell death. =

Several studies implicated mitochondrial ROS in the induction = of=20 autophagy.24,25=20 Cancer cells have an antioxidant system where antioxidant = enzymes=20 such as manganese-superoxide dismutase (SOD), catalase, and=20 glutathione peroxidase eliminate ROS.23=20 Chen et al.24=20 recently reported that oxidative stress induced by=20 H2O2 or SOD inhibitor = 2-methoxyestradiol (2-ME)=20 can cause autophagic cell death in transformed cell line = HEK293, and=20 cancer cell lines U87 and HeLa. Similarly, our data also = indicated=20 that autophagy induced by VPA is dependent on oxidative = stress,=20 suggesting that oxidative stress occurs upstream of = autophagy.=20 Therefore, our results may propose a central role for = mitochondria as=20 the source for redox regulation of autophagy after exposure = to=20 VPA in glioma cells. However, is the regulation of autophagy=20 limited to mitochondria ROS production alone? Scherz-Shouval = et=20 al.26=20 discovered redox as a posttranslational modification that = regulates=20 autophagy through the regulation of autophagy effector Atg4. = In=20 this study, we found that ERK1/2 activation was also regulated = by=20 oxidative stress.

Upregulation of ERK1/2 activity via enhanced activity of the=20 ras/raf-1/MEK/ERK pathway is imperative for induction of=20 autophagy in HT-29 colon cancer cells.27=20 Lee et al.28=20 showed that H2O2 treatment resulted in = marked=20 sustained activation of ERK, which can be prevented by = catalase, the=20 hydrogen peroxide scavenger. ERK2 knockdown by siRNA leads to = collapse of MMP with acute oxidative stress in human lens = epithelial=20 cells.29=20 Some evidence exists that the ERK pathway mediates apoptosis = via the=20 upstream action of mitochondrial cytochrome c release = and=20 caspase-3 activation through upregulation of Bax and = p53.30=20 Our data actually revealed an opposite role of ERK in = VPA-induced=20 apoptosis, since its inhibition by PD98059 led to enhanced = apoptosis.=20 Thus, ERK1/2 activation might play a pivotal role in = switching to=20 oxidative stress=96induced autophagy rather than apoptosis in = glioma cells.

Recently, Sarkar et al.31=20 proposed that lithium induced autophagy via inositol = monophosphatase=20 (IMPase) inhibition, leading to free inositol depletion and = reduced=20 myo-inositol-1,4,5-triphosphate (IP3) levels. This represents = a novel=20 way of regulating mammalian autophagy, independent of the = mTOR.=20 Although inositol depletion is a first event shown to be = common to=20 lithium and VPA, VPA did not demonstrate any direct = stimulation or=20 inhibition on partially purified IMPase preparation derived = from=20 bovine brain, suggesting that reduced IP3 levels might be = caused by=20 other mechanisms.32=20 Nevertheless, our data also showed that addition of inositol = did not=20 attenuate autophagy induced by VPA, suggesting a different = mechanism=20 from that of lithium.

In summary, in the present study, we have demonstrated, for = the=20 first time, that VPA induced autophagy in malignant glioma = cells=20 through modulating oxidative stress. ERK1/2 activation is = also=20 required for induction of autophagy mediated by oxidative = stress. In=20 addition, a previous study indicated that autophagy failed to = be=20 significantly induced in primary astrocytes under oxidative=20 stress.24=20 Thus, targeting ROS generation could selectively induce = autophagic=20 cell death in cancer cells. This may lead to new strategies = to=20 develop therapeutic drugs that will selectively target cancer = cells=20 to undergo autophagy, inducing cell death independent of = apoptosis.=20 We also found that treatment combining temezolomide or = rapamycin with=20 VPA had a synergistic effect on development of autophagy in = these=20 glioma cell lines, which may provide a promising rationale = for using=20 therapies that combine VPA and other proautophagic drugs for = the=20 treatment of patients with apoptosis-resistant gliomas. = Recently,=20 clinical trials have been conducted to determine the safety,=20 toxicity, and maximum tolerated dose of VPA alone or in = combination=20 in solid tumor malignancies and to define its clinical=20 feasibility.33,34=20 Thus, VPA could be a drug that could eventually be used in=20 combination therapies, with classical cytotoxics, = proautophagic=20 drugs, or radiation, in gliomas.


3D"   =20 Funding
Top
Abstract
Patients and Methods
Results
Discussion
3D"Funding
References
 
T= his=20 research was supported by the National Natural Science = Foundation of=20 China (No. 30772551) and State Key Laboratory for Cancer = Research in=20 Southern China Grant 985-II.

Conflict of interest statement. None declared.


3D"   =20 References
Top
Abstract
Patients and Methods
Results
Discussion
Funding
3D"References
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'none' : 'block' ); } } } function hide( id ) { if( supported ) { if( document.layers && document.layers[id] ) { document.layers[id].display =3D 'none'; } else if( document.getElementById && = document.getElementById(id) ) { document.getElementById(id).style.display =3D 'none'; } else if( document.all && document.all[id] ) { document.all[id].style.display =3D 'none'; } } } function unhide( id, display ) { // Default to display at block level if( ! display ) display =3D 'block'; if( supported ) { // As IE does not support table-row, translate it to block if( navigator.appName =3D=3D 'Microsoft Internet Explorer' && = display =3D=3D 'table-row' ) display =3D 'block'; if( document.layers && document.layers[id] ) { document.layers[id].display =3D display; } else if( document.getElementById && = document.getElementById(id) ) { document.getElementById(id).style.display =3D display; } else if( document.all && document.all[id] ) { document.all[id].style.display =3D display; } } } function visible( id ) { if( supported ) { if( document.layers && document.layers[id] ) { if( document.layers[id].display =3D=3D 'none' ) return 0; } else if( document.getElementById && = document.getElementById(id) ) { if( document.getElementById(id).style.display =3D=3D 'none' = ) return 0; } else if( document.all && document.all[id] ) { if( document.all[id].style.display =3D=3D 'none' ) return = 0; } return 1; } return 0; } function removeSpaces(string) { var tstring =3D ""; string =3D '' + string; splitstring =3D string.split(" "); for(i =3D 0; i < splitstring.length; i++) tstring +=3D = splitstring[i]; return tstring; } var selectItems =3D new Object(); function setOptions( listname, selectedItem, optionList ) { optionList.options.length =3D 0; optionList[0] =3D new Option( "Please select", "", true, false ); if( selectItems[listname][selectedItem] ) { var newList =3D selectItems[listname][selectedItem]; if( selectedItem !=3D "" ) { for( var i =3D 0; i < newList.length; i++ ) { optionList.options[i+1] =3D new Option( newList[i].text, = newList[i].value ? newList[i].value : newList[i].text ); } } } } // Return the absolute Y position of an element on a page (from the top = of the page, NOT visible screen) function findPos(obj) { var curtop =3D 0; var = bodyBorder=3D-document.body.offsetTop||document.body.clientTop; if (navigator.userAgent.indexOf("MSIE")!=3D-1) { curtop-=3D8 }=20 if (obj.offsetParent) { do { curtop +=3D obj.offsetTop; } while (obj =3D obj.offsetParent); } return curtop+bodyBorder; } // Update the floating help window. Leave htext blank to hide again. function help_window(htext,field){ var hw =3D document.getElementById("help_window"); if(hw !=3D undefined ){ if(htext =3D=3D ''){ hw.className=3D"hidden"; } else { hw.innerHTML=3Dhtext; hw.className=3D"help_window"; hw.style.top=3DfindPos(field)+"px"; } } } //Archive list interactivity functions var tick_archive=3Dnew Array("Humanities", "Law", "Medicine", "Science", = "Social Sciences"); var tick_archive_x=3Dnew Array(true, true, true, true, true); var tick_year=3Dnew Array(); var tick_year_x=3Dnew Array(); var tick_status=3Dnew Array("I", "E", "L"); var tick_status_x=3Dnew Array(true, true, true); var line_id=3Dnew Array(); var line_archives=3Dnew Array(); var line_year_joined=3Dnew Array(); var line_status=3Dnew Array(); var year_count=3D-1; var line_count=3D-1; function add_year(year_to_add) { year_count+=3D1; tick_year[year_count]=3Dyear_to_add; tick_year_x[year_count]=3Dtrue; } function filter() { for(var i=3D0; i<=3Dline_count; i++) { var ok=3D""; for(var j=3D0; j.=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_01CA7E49.2B8D3FB0 Content-Type: application/octet-stream Content-Transfer-Encoding: quoted-printable Content-Location: http://neuro-oncology.oxfordjournals.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 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quoted-printable Content-Location: http://neuro-oncology.oxfordjournals.org/javascript/entrez/callback.js /************************************************************************= *****=0A= * javascript/entrez/callback.js=0A= *=0A= * Entrez Linking callback to populate content box.=0A= *=0A= * Copyright 2006 Board of Trustees of the Leland Stanford Junior = University.=0A= = *************************************************************************= ***/=0A= =0A= /*=0A= * Execute callback to fill content box with Entrez Linking information.=0A= */=0A= function entrez_callback(pmid, callback_url) {=0A= /*=0A= * MSIE 5.5 and below have issues with the JavaScript=0A= * used for Entrez Linking. 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