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Science 290 (5493): 989-992

Copyright © 2000 by the American Association for the Advancement of Science

Role of BAX in the Apoptotic Response to Anticancer Agents

Lin Zhang, Jian Yu, Ben Ho Park, Kenneth W. Kinzler, Bert Vogelstein*

To assess the role of BAX in drug-induced apoptosis in human colorectal cancer cells, we generated cells that lack functional BAX genes. Such cells were partially resistant to the apoptotic effects of the chemotherapeutic agent 5-fluorouracil, but apoptosis was not abolished. In contrast, the absence of BAX completely abolished the apoptotic response to the chemopreventive agent sulindac and other nonsteroidal anti-inflammatory drugs (NSAIDs). NSAIDs inhibited the expression of the antiapoptotic protein Bcl-XL, resulting in an altered ratio of BAX to Bcl-XL and subsequent mitochondria-mediated cell death. These results establish an unambiguous role for BAX in apoptotic processes in human epithelial cancers and may have implications for cancer chemoprevention strategies.

Howard Hughes Medical Institute, Oncology Center, and Program in Human Genetics, Johns Hopkins University School of Medicine, Baltimore, MD 21231, USA.
*   To whom correspondence should be addressed. E-mail: vogelbe{at}

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Hsp90 Inhibitors Promote p53-Dependent Apoptosis through PUMA and Bax.
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   Abstract »    Full Text »    PDF »
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Neem oil limonoids induces p53-independent apoptosis and autophagy.
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UV irradiation resistance-associated gene suppresses apoptosis by interfering with BAX activation.
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   Abstract »    Full Text »    PDF »
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p53-mediated apoptosis requires inositol hexakisphosphate kinase-2.
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   Abstract »    Full Text »    PDF »
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Mol. Cancer Res. 7, 1268-1284
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A novel agonistic antibody to human death receptor 4 induces apoptotic cell death in various tumor cells without cytotoxicity in hepatocytes.
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Mol. Cancer Ther. 8, 2036-2045
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Determinants for the efficiency of anticancer drugs targeting either Aurora-A or Aurora-B kinases in human colon carcinoma cells.
P. Kaestner, A. Stolz, and H. Bastians (2009)
Mol. Cancer Ther. 8, 2046-2056
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PUMA Suppresses Intestinal Tumorigenesis in Mice.
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Cancer Res. 69, 4999-5006
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p53 Acetylation Is Crucial for Its Transcription-independent Proapoptotic Functions.
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Death Receptor-Induced Activation of the Chk2- and Histone H2AX-Associated DNA Damage Response Pathways.
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Mol. Cell. Biol. 29, 68-82
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An intracellular wave of cytochrome c propagates and precedes Bax redistribution during apoptosis.
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J. Cell Sci. 121, 3515-3523
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Nonsteroidal Anti-Inflammatory Drugs Induced Endothelial Apoptosis by Perturbing Peroxisome Proliferator-Activated Receptor-{delta} Transcriptional Pathway.
J.-Y. Liou, C.-C. Wu, B.-R. Chen, L. B. Yen, and K. K. Wu (2008)
Mol. Pharmacol. 74, 1399-1406
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Effects of Celecoxib and Nimesulide on the Proliferation of Ectopic Endometrial Stromal Cells in vitro.
B. Kong, Y. Tian, W. Zhu, S. Su, and Y. Kan (2008)
Journal of International Medical Research 36, 1032-1038
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Topoisomerase I Requirement for Death Receptor-induced Apoptotic Nuclear Fission.
O. Sordet, A. Goldman, C. Redon, S. Solier, V. A. Rao, and Y. Pommier (2008)
J. Biol. Chem. 283, 23200-23208
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Transcriptional role of p53 in interferon-mediated antiviral immunity.
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J. Exp. Med. 205, 1929-1938
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Severe acute respiratory syndrome coronavirus 3a protein activates the mitochondrial death pathway through p38 MAP kinase activation.
K. Padhan, R. Minakshi, M. A. B. Towheed, and S. Jameel (2008)
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Anti-cancer Effects of JKA97 Are Associated with Its Induction of Cell Apoptosis via a Bax-dependent and p53-independent Pathway.
W. Luo, J. Liu, J. Li, D. Zhang, M. Liu, J. K. Addo, S. Patil, L. Zhang, J. Yu, J. K. Buolamwini, et al. (2008)
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PINCH-1 Regulates the ERK-Bim Pathway and Contributes to Apoptosis Resistance in Cancer Cells.
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SMAC Mimetics Sensitize Nonsteroidal Anti-inflammatory Drug Induced Apoptosis by Promoting Caspase-3 Mediated Cytochrome c Release.
A. Bank, P. Wang, C. Du, J. Yu, and L. Zhang (2008)
Cancer Res. 68, 276-284
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Screening for Compounds That Induce Apoptosis of Cancer Cells Grown as Multicellular Spheroids.
R. Herrmann, W. Fayad, S. Schwarz, M. Berndtsson, and S. Linder (2008)
J Biomol Screen 13, 1-8
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High Mobility Group Protein B1 Is an Activator of Apoptotic Response to Antimetabolite Drugs.
N. Krynetskaia, H. Xie, S. Vucetic, Z. Obradovic, and E. Krynetskiy (2008)
Mol. Pharmacol. 73, 260-269
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Mcl-1 determines the Bax dependency of Nbk/Bik-induced apoptosis.
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J. Cell Biol. 179, 701-715
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Cell Cycle Dependent and Schedule-Dependent Antitumor Effects of Sorafenib Combined with Radiation.
J. P. Plastaras, S.-H. Kim, Y. Y. Liu, D. T. Dicker, J. F. Dorsey, J. McDonough, G. Cerniglia, R. R. Rajendran, A. Gupta, A. K. Rustgi, et al. (2007)
Cancer Res. 67, 9443-9454
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Resveratrol induces cell death in colorectal cancer cells by a novel pathway involving lysosomal cathepsin D.
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Carcinogenesis 28, 922-931
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p53 and p21 Determine the Sensitivity of Noscapine-Induced Apoptosis in Colon Cancer Cells.
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Cancer Res. 67, 3862-3870
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Nonsteroidal Anti-inflammatory Drugs Induce Colorectal Cancer Cell Apoptosis by Suppressing 14-3-3{varepsilon}.
J.-Y. Liou, D. Ghelani, S. Yeh, and K. K. Wu (2007)
Cancer Res. 67, 3185-3191
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A coordinated action of Bax, PUMA, and p53 promotes MG132-induced mitochondria activation and apoptosis in colon cancer cells.
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Mol. Cancer Ther. 6, 1062-1069
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Differential Effects of Endoplasmic Reticulum Stress-induced Autophagy on Cell Survival.
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J. Biol. Chem. 282, 4702-4710
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Targeting of multiple signalling pathways by heat shock protein 90 molecular chaperone inhibitors.
M. V Powers and P. Workman (2006)
Endocr. Relat. Cancer 13, S125-S135
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Inhibition of 5-lipoxygenase by MK886 augments the antitumor activity of celecoxib in human colon cancer cells..
F. Cianchi, C. Cortesini, L. Magnelli, E. Fanti, L. Papucci, N. Schiavone, L. Messerini, A. Vannacci, S. Capaccioli, F. Perna, et al. (2006)
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Aspirin Induces Apoptosis through the Inhibition of Proteasome Function.
P. Dikshit, M. Chatterjee, A. Goswami, A. Mishra, and N. R. Jana (2006)
J. Biol. Chem. 281, 29228-29235
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Cytopathic effects of the cytomegalovirus-encoded apoptosis inhibitory protein vMIA.
D. Poncet, A.-L. Pauleau, G. Szabadkai, A. Vozza, S. R. Scholz, M. Le Bras, J.-J. Briere, A. Jalil, R. Le Moigne, C. Brenner, et al. (2006)
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Caspase-2 Triggers Bax-Bak-dependent and -independent Cell Death in Colon Cancer Cells Treated with Resveratrol.
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Vinblastine-induced Apoptosis Is Mediated by Discrete Alterations in Subcellular Location, Oligomeric Structure, and Activation Status of Specific Bcl-2 Family Members.
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Inhibition of Glutathione Synthesis Overcomes Bcl-2-Mediated Topoisomerase Inhibitor Resistance and Induces Nonapoptotic Cell Death via Mitochondrial-Independent Pathway.
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Cancer Res. 66, 5772-5780
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Free Fatty Acids Induce JNK-dependent Hepatocyte Lipoapoptosis.
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J. Biol. Chem. 281, 12093-12101
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Androgen and Its Receptor Promote Bax-Mediated Apoptosis.
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Carcinogenesis 27, 584-592
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Cancer Res. 66, 1730-1739
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c-Abl-independent p73 stabilization during gemcitabine- or 4'-thio-{beta}-D-arabinofuranosylcytosine-induced apoptosis in wild-type and p53-null colorectal cancer cells..
J. V. Thottassery, L. Westbrook, H. Someya, and W. B. Parker (2006)
Mol. Cancer Ther. 5, 400-410
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Tissue Transglutaminase Serves as an Inhibitor of Apoptosis by Cross-Linking Caspase 3 in Thapsigargin-Treated Cells.
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Mol. Cell. Biol. 26, 569-579
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Gut 55, 115-122
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Sensitization of DNA damage-induced apoptosis by the proteasome inhibitor PS-341 is p53 dependent and involves target proteins 14-3-3{sigma} and survivin.
S. A.J. Vaziri, J. Hill, K. Chikamori, D. R. Grabowski, N. Takigawa, M. Chawla-Sarkar, L. R. Rybicki, A. V. Gudkov, T. Mekhail, R. M. Bukowski, et al. (2005)
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Cancer-Specific Functions of SIRT1 Enable Human Epithelial Cancer Cell Growth and Survival.
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Loss of Bif-1 Suppresses Bax/Bak Conformational Change and Mitochondrial Apoptosis.
Y. Takahashi, M. Karbowski, H. Yamaguchi, A. Kazi, J. Wu, S. M. Sebti, R. J. Youle, and H.-G. Wang (2005)
Mol. Cell. Biol. 25, 9369-9382
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MAP-1 is a mitochondrial effector of Bax.
K. O. Tan, N. Y. Fu, S. K. Sukumaran, S.-L. Chan, J. H. Kang, K. L. Poon, B. S. Chen, and V. C. Yu (2005)
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COX and cancer.
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QJM 98, 711-718
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Pharmacologic Modulation of Glycogen Synthase Kinase-3{beta} Promotes p53-Dependent Apoptosis through a Direct Bax-Mediated Mitochondrial Pathway in Colorectal Cancer Cells.
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Cancer Res. 65, 9012-9020
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Sulindac sulfide-induced apoptosis is enhanced by a small-molecule Bcl-2 inhibitor and by TRAIL in human colon cancer cells overexpressing Bcl-2.
F. A. Sinicrope and R. C. Penington (2005)
Mol. Cancer Ther. 4, 1475-1483
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SDX-101, the R-enantiomer of etodolac, induces cytotoxicity, overcomes drug resistance, and enhances the activity of dexamethasone in multiple myeloma.
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Sulindac Inhibits {beta}-Catenin Expression in Normal-Appearing Colon of Hereditary Nonpolyposis Colorectal Cancer and Familial Adenomatous Polyposis Patients.
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Bax-dependent Regulation of Bak by Voltage-dependent Anion Channel 2.
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14-3-3{sigma} Expression Is an Independent Prognostic Parameter for Poor Survival in Colorectal Carcinoma Patients.
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Human colon cancer cells lacking Bax resist curcumin-induced apoptosis and Bax requirement is dispensable with ectopic expression of Smac or downregulation of Bcl-XL.
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Common Polymorphism G(-248)A in the Promoter Region of the bax Gene Results in Significantly Shorter Survival in Patients With Chronic Lymphocytic Leukemia Once Treatment Is Initiated.
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Bcl-XL small interfering RNA suppresses the proliferation of 5-fluorouracil-resistant human colon cancer cells.
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Bcl-XL specifically activates Bak to induce swelling and restructuring of the endoplasmic reticulum.
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{Delta}Np63{alpha} Up-Regulates the Hsp70 Gene in Human Cancer.
G. Wu, M. Osada, Z. Guo, A. Fomenkov, S. Begum, M. Zhao, S. Upadhyay, M. Xing, F. Wu, C. Moon, et al. (2005)
Cancer Res. 65, 758-766
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Sulindac enhances adenoviral vector expressing mda-7/IL-24-mediated apoptosis in human lung cancer.
Y. Oida, B. Gopalan, R. Miyahara, S. Inoue, C. D. Branch, A. M. Mhashilkar, E. Lin, B. N. Bekele, J. A. Roth, S. Chada, et al. (2005)
Mol. Cancer Ther. 4, 291-304
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Combination of IFN-{alpha} and 5-Fluorouracil Induces Apoptosis through IFN-{alpha}/{beta} Receptor in Human Hepatocellular Carcinoma Cells.
M. Kondo, H. Nagano, H. Wada, B. Damdinsuren, H. Yamamoto, N. Hiraoka, H. Eguchi, A. Miyamoto, T. Yamamoto, H. Ota, et al. (2005)
Clin. Cancer Res. 11, 1277-1286
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Induction of lysosomal membrane permeabilization by compounds that activate p53-independent apoptosis.
H. Erdal, M. Berndtsson, J. Castro, U. Brunk, M. C. Shoshan, and S. Linder (2005)
PNAS 102, 192-197
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Drugging the Cancer Kinome: Progress and Challenges in Developing Personalized Molecular Cancer Therapeutics.
P. WORKMAN (2005)
Cold Spring Harb Symp Quant Biol 70, 499-515
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Inhibition of Cyclooxygenase (COX)-2 Expression by Tet-Inducible COX-2 Antisense cDNA in Hormone-Refractory Prostate Cancer Significantly Slows Tumor Growth and Improves Efficacy of Chemotherapeutic Drugs.
D. S. Dandekar and B. L. Lokeshwar (2004)
Clin. Cancer Res. 10, 8037-8047
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Organ-selective chemoresistance in metastasis from human breast cancer cells: inhibition of apoptosis, genetic variability and microenvironment at the metastatic focus.
B. Gu, L. Espana, O. Mendez, A. Torregrosa, and A. Sierra (2004)
Carcinogenesis 25, 2293-2301
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SMAC/Diablo-dependent apoptosis induced by nonsteroidal antiinflammatory drugs (NSAIDs) in colon cancer cells.
M. Kohli, J. Yu, C. Seaman, A. Bardelli, K. W. Kinzler, B. Vogelstein, C. Lengauer, and L. Zhang (2004)
PNAS 101, 16897-16902
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Inhibition of Extracellular-signal Regulated Kinases 1/2 Is Required for Apoptosis of Human Colon Cancer Cells In vitro by Sulindac Metabolites.
P. L. Rice, K. S. Beard, L. J. Driggers, and D. J. Ahnen (2004)
Cancer Res. 64, 8148-8151
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Hydrogen Peroxide-Mediated Cytosolic Acidification Is a Signal for Mitochondrial Translocation of Bax during Drug-Induced Apoptosis of Tumor Cells.
K. A. Ahmad, K. B. Iskandar, J. L. Hirpara, M.-V. Clement, and S. Pervaiz (2004)
Cancer Res. 64, 7867-7878
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Apoptosis and colorectal cancer.
A J M Watson (2004)
Gut 53, 1701-1709
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Non-steroidal anti-inflammatory drug activated gene (NAG-1) expression is closely related to death receptor-4 and -5 induction, which may explain sulindac sulfide induced gastric cancer cell apoptosis.
T. J. Jang, H. J. Kang, J. R. Kim, and C. H. Yang (2004)
Carcinogenesis 25, 1853-1858
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Ectopic expression of Bcl-XL or Ku70 protects human colon cancer cells (SW480) against curcumin-induced apoptosis while their down-regulation potentiates it.
R. Rashmi, S. Kumar, and D. Karunagaran (2004)
Carcinogenesis 25, 1867-1877
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Regulation of Bax Activation and Apoptotic Response to Microtubule-damaging Agents by p53 Transcription-dependent and -independent Pathways.
H. Yamaguchi, J. Chen, K. Bhalla, and H.-G. Wang (2004)
J. Biol. Chem. 279, 39431-39437
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