Mitochondrial permeability transition pore as a selective target for anti-cancer therapy

Frontiers in Oncology

Volumn 3 MAR, Issue , 2013, Pages

  Suh, Dong H ^a   Kim, Mi Kyung ^a   Kim, Hee S ^a   Chung, Hyun H ^a   Song, Yong S ^a,b  

^a Seoul National University College of Medicine   (South Korea)

^b Seoul National University   (South Korea)

Author keywords

Anti cancer therapy; Apoptosis; Cancer; Mitochondria; Mitochondrial permeability transition pore

Indexed keywords

2 AMINO 6 BROMO 4 (1 CYANO 2 ETHOXY 2 OXOETHYL) 4H CHROMENE 3 CARBOXYLIC ACID ETHYL ESTER; 4 [4 (4' CHLORO 2 BIPHENYLYLMETHYL) 1 PIPERAZINYL] N [4 [3 DIMETHYLAMINO 1 (PHENYLTHIOMETHYL)PROPYLAMINO] 3 NITROBENZENESULFONYL]BENZAMIDE; 6 [3 (1 ADAMANTYL) 4 HYDROXYPHENYL] 2 NAPHTHOIC ACID; ADENINE NUCLEOTIDE TRANSLOCASE; ALPHA TOCOPHEROL SUCCINATE; BERBERINE; BETULIC ACID; BH3 PROTEIN; CLODRONIC ACID; CURCUMIN; CYCLOPHILIN D; CYTOCHROME C; GADOLINIUM TEXAPHYRIN; GLYCOGEN SYNTHASE KINASE 3; GOSSYPOL; HEXOKINASE; HONOKIOL; JASMONIC ACID METHYL ESTER; LONIDAMINE; MITOCHONDRIAL PERMEABILITY TRANSITION PORE; MITOGEN ACTIVATED PROTEIN KINASE; NAVITOCLAX; OBATOCLAX; OBLIMERSEN; PROTEIN BCL 2; PROTEIN KINASE B; RESVERATROL; RETINOIC ACID; UNINDEXED DRUG; VOLTAGE DEPENDENT ANION CHANNEL;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; CANCER CHEMOTHERAPY; CELL PERMEABILIZATION; CYTOTOXICITY; DRUG TARGETING; HUMAN; MITOCHONDRIAL MEMBRANE; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); PROSTATE CANCER; PROTEIN BINDING; REVIEW; SIGNAL TRANSDUCTION;

EID: 84890632015     PISSN: None     EISSN: 2234943X     Source Type: Journal    
DOI: 10.3389/fonc.2013.00041     Document Type: Review

References (113)

1. Arora, S., Singh, S., Piazza, G. A., Contreras, C. M., Panyam, J., and Singh, A. P. (2012). Honokiol: a novel natural agent for cancer prevention and therapy. Curr. Mol. Med. 12, 1244-1252.
2. Azmi, A. S., and Mohammad, R. M. (2009). Non-peptidic small molecule inhibitors against Bcl-2 for cancer therapy. J. Cell Physiol. 218, 13-21.
3. Baggstrom, M. Q., Qi, Y., Koczywas, M., Argiris, A., Johnson, E. A., Millward, M. J., et al. (2011). A phase II study of AT-101 (Gossypol) in chemotherapy-sensitive recurrent extensive-stage small cell lung cancer. J. Thorac. Oncol. 6, 1757-1760.
4. Baines, C. P., Kaiser, R. A., Purcell, N. H., Blair, N. S., Osinska, H., Hambleton, M. A., et al. (2005). Loss of cyclophilin D reveals a critical role for mitochondrial permeability transition in cell death. Nature 434, 658-662.
5. Baines, C. P., Kaiser, R. A., Sheiko, T., Craigen, W. J., and Molkentin, J. D. (2007). Voltage-dependent anion channels are dispensable for mitochondrial-dependent cell death. Nat. Cell Biol. 9, 550-555.
6. Barbosa, I. A., Machado, N. G., Skildum, A. J., Scott, P. M., and Oliveira, P. J. (2012). Mitochondrial remodeling in cancer metabolism and survival: potential for new therapies. Biochim. Biophys. Acta 1826, 238-254.
7. Belzacq, A. S., El Hamel, C., Vieira, H. L., Cohen, I., Haouzi, D., Metivier, D., et al. (2001). Adenine nucleotide translocator mediates the mitochondrial membrane permeabilization induced by lonidamine, arsenite and CD437. Oncogene 20, 7579-7587.
8. Bray, K., Chen, H. Y., Karp, C. M., May, M., Ganesan, S., Karantza-Wadsworth, V., et al. (2009). Bcl-2 modulation to activate apoptosis in prostate cancer. Mol. Cancer Res. 7, 1487-1496.
9. Carroll, R. E., Benya, R. V., Turgeon, D. K., Vareed, S., Neuman, M., Rodriguez, L., et al. (2011). Phase IIa clinical trial of curcumin for the prevention of colorectal neoplasia. Cancer Prev. Res. (Phila.) 4, 354-364.
10. Certo, M., Del Gaizo Moore, V., Nishino, M., Wei, G., Korsmeyer, S., Armstrong, S. A., et al. (2006). Mitochondria primed by death signals determine cellular addiction to antiapoptotic BCL-2 family members. Cancer Cell 9, 351-365.
11. Chen, Z., Zhang, H., Lu, W., and Huang, P. (2009). Role of mitochondria-associated hexokinase II in cancer cell death induced by 3-bromopyruvate. Biochim. Biophys. Acta 1787, 553-560.
12. Cheng, E. H., Sheiko, T. V., Fisher, J. K., Craigen, W. J., and Korsmeyer, S. J. (2003). VDAC2 inhibits BAK activation and mitochondrial apoptosis. Science 301, 513-517.
13. Chevrollier, A., Loiseau, D., Chabi, B., Renier, G., Douay, O., Malthiery, Y., et al. (2005). ANT2 isoform required for cancer cell glycolysis. J. Bioenerg. Biomembr. 37, 307-316.
14. Chiara, F., Castellaro, D., Marin, O., Petronilli, V., Brusilow, W. S., Juhaszova, M., et al. (2008). Hexokinase II detachment from mitochondria triggers apoptosis through the permeability transition pore independent of voltage-dependent anion channels. PLoS ONE 3:e1852. doi: 10.1371/journal.pone.0001852
15. Cohen, S., and Flescher, E. (2009). Methyl jasmonate: a plant stress hormone as an anti-cancer drug. Phytochemistry 70, 1600-1609.
16. Costantini, P., Belzacq, A. S., Vieira, H. L., Larochette, N., De Pablo, M. A., Zamzami, N., et al. (2000). Oxidation of a critical thiol residue of the adenine nucleotide translocator enforces Bcl-2-independent permeability transition pore opening and apoptosis. Oncogene 19, 307-314.
17. Dejean, L. M., Ryu, S. Y., Martinez-Caballero, S., Teijido, O., Peixoto, P. M., and Kinnally, K. W. (2010). MAC and Bcl-2 family proteins conspire in a deadly plot. Biochim. Biophys. Acta 1797, 1231-1238.
18. Di Cosimo, S., Ferretti, G., Papaldo, P., Carlini, P., Fabi, A., and Cognetti, F. (2003). Lonidamine: efficacy and safety in clinical trials for the treatment of solid tumors. Drugs Today (Barc.) 39, 157-174.
19. Diel, I. J., Jaschke, A., Solomayer, E. F., Gollan, C., Bastert, G., Sohn, C., et al. (2008). Adjuvant oral clodronate improves the overall survival of primary breast cancer patients with micrometastases to the bone marrow: a long-term follow-up. Ann. Oncol. 19, 2007-2011.
20. Di Lisa, F., Canton, M., Menabo, R., Kaludercic, N., and Bernardi, P. (2007). Mitochondria and cardioprotection. Heart Fail. Rev. 12, 249-260.
21. Divya, C. S., and Pillai, M. R. (2006). Antitumor action of curcumin in human papillomavirus associated cells involves downregulation of viral oncogenes, prevention of NFkB and AP-1 translocation, and modulation of apoptosis. Mol. Carcinog. 45, 320-332.
22. Don, A. S., Kisker, O., Dilda, P., Donoghue, N., Zhao, X., Decollogne, S., et al. (2003). A peptide trivalent arsenical inhibits tumor angiogenesis by perturbing mitochondrial function in angiogenic endothelial cells. Cancer Cell 3, 497-509.
23. Dong, L. F., Low, P., Dyason, J. C., Wang, X. F., Prochazka, L., Witting, P. K., et al. (2008). Alpha-tocopheryl succinate induces apoptosis by targeting ubiquinone-binding sites in mitochondrial respiratory complex II. Oncogene 27, 4324-4335.
24. Dong, L. F., Swettenham, E., Eliasson, J., Wang, X. F., Gold, M., Medunic, Y., et al. (2007). Vitamin E analogues inhibit angiogenesis by selective induction of apoptosis in proliferating endothelial cells: the role of oxidative stress. Cancer Res. 67, 11906-11913.
25. Elstrom, R. L., Bauer, D. E., Buzzai, M., Karnauskas, R., Harris, M. H., Plas, D. R., et al. (2004). Akt stimulates aerobic glycolysis in cancer cells. Cancer Res. 64, 3892-3899.
26. Fried, L. E., and Arbiser, J. L. (2009). Honokiol, a multifunctional antiangiogenic and antitumor agent. Antioxid. Redox Signal. 11, 1139-1148.
27. Fulda, S., Friesen, C., Los, M., Scaffidi, C., Mier, W., Benedict, M., et al. (1997). Betulinic acid triggers CD95 (APO-1/Fas)-and p53-independent apoptosis via activation of caspases in neuroectodermal tumors. Cancer Res. 57, 4956-4964.
28. Fulda, S., Galluzzi, L., and Kroemer, G. (2010). Targeting mitochondria for cancer therapy. Nat. Rev. Drug Discov. 9, 447-464.
29. Ganapathy-Kanniappan, S., Vali, M., Kunjithapatham, R., Buijs, M., Syed, L. H., Rao, P. P., et al. (2010). 3-bromopyruvate: a new targeted antiglycolytic agent and a promise for cancer therapy. Curr. Pharm. Biotechnol. 11, 510-517.
30. Gledhill, J. R., Montgomery, M. G., Leslie, A. G., and Walker, J. E. (2007). Mechanism of inhibition of bovine F1-ATPase by resveratrol and related polyphenols. Proc. Natl. Acad. Sci. U.S.A. 104, 13632-13637.
31. Gogvadze, V., Orrenius, S., and Zhivotovsky, B. (2009a). Mitochondria as targets for cancer chemotherapy. Semin. Cancer Biol. 19, 57-66.
32. Gogvadze, V., Orrenius, S., and Zhivotovsky, B. (2009b). Mitochondria as targets for chemotherapy. Apoptosis 14, 624-640.
33. Goldin, N., Arzoine, L., Heyfets, A., Israelson, A., Zaslavsky, Z., Bravman, T., et al. (2008). Methyl jasmonate binds to and detaches mitochondria-bound hexokinase. Oncogene 27, 4636-4643.
34. Halestrap, A. P., Clarke, S. J., and Javadov, S. A. (2004). Mitochondrial permeability transition pore opening during myocardial reperfusion-a target for cardioprotection. Cardiovasc. Res. 61, 372-385.
35. Hann, C. L., Daniel, V. C., Sugar, E. A., Dobromilskaya, I., Murphy, S. C., Cope, L., et al. (2008). Therapeutic efficacy of ABT-737, a selective inhibitor of BCL-2, in small cell lung cancer. Cancer Res. 68, 2321-2328.
36. Jeong, S. H., Jo, W. S., Song, S., Suh, H., Seol, S. Y., Leem, S. H., et al. (2009). A novel resveratrol derivative, HS1793, overcomes the resistance conferred by Bcl-2 in human leukemic U937 cells. Biochem. Pharmacol. 77, 1337-1347.
37. Kim, H. J., Yang, K. M., Park, Y. S., Choi, Y. J., Yun, J. H., Son, C. H., et al. (2012). The novel resveratrol analogue HS-1793 induces apoptosis via the mitochondrial pathway in murine breast cancer cells. Int. J. Oncol. 41, 1628-1634.
38. Kim, W., Yoon, J. H., Jeong, J. M., Cheon, G. J., Lee, T. S., Yang, J. I., et al. (2007). Apoptosis-inducing antitumor efficacy of hexokinase II inhibitor in hepatocellular carcinoma. Mol. Cancer Ther. 6, 2554-2562.
39. Kinnally, K. W., and Antonsson, B. (2007). A tale of two mitochondrial channels, MAC and PTP, in apoptosis. Apoptosis 12, 857-868.
40. Kokoszka, J. E., Waymire, K. G., Levy, S. E., Sligh, J. E., Cai, J., Jones, D. P., et al. (2004). The ADP/ATP translocator is not essential for the mitochondrial permeability transition pore. Nature 427, 461-465.
41. Kroemer, G., Galluzzi, L., and Brenner, C. (2007). Mitochondrial membrane permeabilization in cell death. Physiol. Rev. 87, 99-163.
42. Kutuk, O., and Letai, A. (2008). Alteration of the mitochondrial apoptotic pathway is key to acquired paclitaxel resistance and can be reversed by ABT-737. Cancer Res. 68, 7985-7994.
43. Larochette, N., Decaudin, D., Jacotot, E., Brenner, C., Marzo, I., Susin, S. A., et al. (1999). Arsenite induces apoptosis via a direct effect on the mitochondrial permeability transition pore. Exp. Cell Res. 249, 413-421.
44. Lehenkari, P. P., Kellinsalmi, M., Napankangas, J. P., Ylitalo, K. V., Monkkonen, J., Rogers, M. J., et al. (2002). Further insight into mechanism of action of clodronate: inhibition of mitochondrial ADP/ATP translocase by a nonhydrolyzable, adenine-containing metabolite. Mol. Pharmacol. 61, 1255-1262.
45. Li, L., Han, W., Gu, Y., Qiu, S., Lu, Q., Jin, J., et al. (2007). Honokiol induces a necrotic cell death through the mitochondrial permeability transition pore. Cancer Res. 67, 4894-4903.
46. Lifson, J. D., Rossio, J. L., Piatak, M. Jr., Bess, J. Jr., Chertova, E., Schneider, D. K., et al. (2004). Evaluation of the safety, immunogenicity, and protective efficacy of whole inactivated simian immunodeficiency virus (SIV) vaccines with conformationally and functionally intact envelope glycoproteins. AIDS Res. Hum. Retroviruses 20, 772-787.
47. Lin, D. T., and Lechleiter, J. D. (2002). Mitochondrial targeted cyclophilin D protects cells from cell death by peptidyl prolyl isomerization. J. Biol. Chem. 277, 31134-31141.
48. Liu, G., Kelly, W. K., Wilding, G., Leopold, L., Brill, K., and Somer, B. (2009). An open-label, multicenter, phase I/II study of single-agent AT-101 in men with castrate-resistant prostate cancer. Clin. Cancer Res. 15, 3172-3176.
49. Machida, K., Ohta, Y., and Osada, H. (2006). Suppression of apoptosis by cyclophilin D via stabilization of hexokinase II mitochondrial binding in cancer cells. J. Biol. Chem. 281, 14314-14320.
50. Madden, K., Flowers, L., Salani, R., Horowitz, I., Logan, S., Kowalski, K., et al. (2009). Proteomics-based approach to elucidate the mechanism of antitumor effect of curcumin in cervical cancer. Prostaglandins Leukot. Essent. Fatty Acids 80, 9-18.
51. Magda, D., and Miller, R. A. (2006). Motexafin gadolinium: a novel redox active drug for cancer therapy. Semin. Cancer Biol. 16, 466-476.
52. Manero, F., Gautier, F., Gallenne, T., Cauquil, N., Gree, D., Cartron, P. F., et al. (2006). The small organic compound HA14-1 prevents Bcl-2 interaction with Bax to sensitize malignant glioma cells to induction of cell death. Cancer Res. 66, 2757-2764.
53. Marchetti, P., Zamzami, N., Joseph, B., Schraen-Maschke, S., Mereau-Richard, C., Costantini, P., et al. (1999). The novel retinoid 6-[3-(1-adamantyl)-4-hydroxyphenyl]-2-naphtalene car-boxylic acid can trigger apoptosis through a mitochondrial pathway independent of the nucleus. Cancer Res. 59, 6257-6266.
54. Martel, C., Huynh Le, H., Garnier, A., Ventura-Clapier, R., and Brenner, C. (2012). Inhibition of the mitochondrial permeability transition for cytoprotection: direct versus indirect mechanisms. Biochem. Res. Int. 2012:213403. doi: 10.1155/2012/213403
55. Masgras, I., Rasola, A., and Bernardi, P. (2012). Induction of the permeability transition pore in cells depleted of mitochondrial DNA. Biochim. Biophys. Acta 1817, 1860-1866.
56. Mason, K. D., Vandenberg, C. J., Scott, C. L., Wei, A. H., Cory, S., Huang, D. C., et al. (2008). In vivo efficacy of the Bcl-2 antagonist ABT-737 against aggressive Myc-driven lymphomas. Proc. Natl. Acad. Sci. U.S.A. 105, 17961-17966.
57. Mathupala, S. P., Ko, Y. H., and Pedersen, P. L. (2006). Hexokinase II: cancer's double-edged sword acting as both facilitator and gatekeeper of malignancy when bound to mitochondria. Oncogene 25, 4777-4786.
58. McCommis, K. S., and Baines, C. P. (2012). The role of VDAC in cell death: friend or foe? Biochim. Biophys. Acta 1818, 1444-1450.
59. Mehta, M. P., Shapiro, W. R., Phan, S. C., Gervais, R., Carrie, C., Chabot, P., et al. (2009). Motexafin gadolinium combined with prompt whole brain radiotherapy prolongs time to neurologic progression in non-small-cell lung cancer patients with brain metastases: results of a phase III trial. Int. J. Radiat. Oncol. Biol. Phys. 73, 1069-1076.
60. Monick, M. M., Powers, L. S., Barrett, C. W., Hinde, S., Ashare, A., Groskreutz, D. J., et al. (2008). Constitutive ERK MAPK activity regulates macrophage ATP production and mitochondrial integrity. J. Immunol. 180, 7485-7496.
61. Nakagawa, T., Shimizu, S., Watanabe, T., Yamaguchi, O., Otsu, K., Yamagata, H., et al. (2005). Cyclophilin D-dependent mitochondrial permeability transition regulates some necrotic but not apoptotic cell death. Nature 434, 652-658.
62. Neuzil, J., Wang, X. F., Dong, L. F., Low, P., and Ralph, S. J. (2006). Molecular mechanism of 'mitocan'-induced apoptosis in cancer cells epitomizes the multiple roles of reactive oxygen species and Bcl-2 family proteins. FEBS Lett. 580, 5125-5129.
63. Neuzil, J., Weber, T., Schroder, A., Lu, M., Ostermann, G., Gellert, N., et al. (2001). Induction of cancer cell apoptosis by alpha-tocopheryl succinate: molecular pathways and structural requirements. FASEB J. 15, 403-415.
64. Nguyen, M., Marcellus, R. C., Roulston, A., Watson, M., Serfass, L., Murthy Madiraju, S. R., et al. (2007). Small molecule obatoclax (GX15-070) antagonizes MCL-1 and overcomes MCL-1-mediated resistance to apoptosis. Proc. Natl. Acad. Sci. U.S.A. 104, 19512-19517.
65. Notario, B., Zamora, M., Vinas, O., and Mampel, T. (2003). All-trans-retinoic acid binds to and inhibits adenine nucleotide translocase and induces mitochondrial permeability transition. Mol. Pharmacol. 63, 224-231.
66. O'Brien, S., Moore, J. O., Boyd, T. E., Larratt, L. M., Skotnicki, A., Koziner, B., et al. (2007). Randomized phase III trial of fludarabine plus cyclophosphamide with or without oblimersen sodium (Bcl-2 antisense) in patients with relapsed or refractory chronic lymphocytic leukemia. J. Clin. Oncol. 25, 1114-1120.
67. O'Brien, S. M., Claxton, D. F., Crump, M., Faderl, S., Kipps, T., Keating, M. J., et al. (2009). Phase I study of obatoclax mesylate (GX15-070), a small molecule pan-Bcl-2 family antagonist, in patients with advanced chronic lymphocytic leukemia. Blood 113, 299-305.
68. Oudard, S., Carpentier, A., Banu, E., Fauchon, F., Celerier, D., Poupon, M. F., et al. (2003). Phase II study of lonidamine and diazepam in the treatment of recurrent glioblastoma multiforme. J. Neurooncol. 63, 81-86.
69. Palmeira, C. M., and Wallace, K. B. (1997). Benzoquinone inhibits the voltage-dependent induction of the mitochondrial permeability transition caused by redox-cycling naphthoquinones. Toxicol. Appl. Pharmacol. 143, 338-347.
70. Parikh, S. A., Kantarjian, H., Schimmer, A., Walsh, W., Asatiani, E., El-Shami, K., et al. (2010). Phase II study of obatoclax mesylate (GX15-070), a small-molecule BCL-2 family antagonist, for patients with myelofibrosis. Clin. Lymphoma Myeloma Leuk. 10, 285-289.
71. Pastorino, J. G., and Hoek, J. B. (2008). Regulation of hexokinase binding to VDAC. J. Bioenerg. Biomembr. 40, 171-182.
72. Pastorino, J. G., Hoek, J. B., and Shulga, N. (2005). Activation of glycogen synthase kinase 3beta disrupts the binding of hexokinase II to mitochondria by phosphorylating voltage-dependent anion channel and potentiates chemotherapy-induced cytotoxicity. Cancer Res. 65, 10545-10554.
73. Pastorino, J. G., Shulga, N., and Hoek, J. B. (2002). Mitochondrial binding of hexokinase II inhibits Bax-induced cytochrome c release and apoptosis. J. Biol. Chem. 277, 7610-7618.
74. Pathania, D., Millard, M., and Neamati, N. (2009). Opportunities in discovery and delivery of anticancer drugs targeting mitochondria and cancer cell metabolism. Adv. Drug Deliv. Rev. 61, 1250-1275.
75. Pavlov, E. V., Priault, M., Pietkiewicz, D., Cheng, E. H., Antonsson, B., Manon, S., et al. (2001). A novel, high conductance channel of mitochondria linked to apoptosis in mammalian cells and Bax expression in yeast. J. Cell Biol. 155, 725-731.
76. Pereira, C. V., Machado, N. G., and Oliveira, P. J. (2008). Mechanisms of berberine (natural yellow 18)-induced mitochondrial dysfunction: interaction with the adenine nucleotide translocator. Toxicol. Sci. 105, 408-417.
77. Pinlaor, S., Yongvanit, P., Prakobwong, S., Kaewsamut, B., Khoontawad, J., Pinlaor, P., et al. (2009). Curcumin reduces oxidative and nitrative DNA damage through balancing of oxidant-antioxidant status in hamsters infected with Opisthorchis viverrini. Mol. Nutr. Food Res. 53, 1316-1328.
78. Powell, B. L., Moser, B., Stock, W., Gallagher, R. E., Willman, C. L., Stone, R. M., et al. (2010). Arsenic trioxide improves event-free and overall survival for adults with acute promyelocytic leukemia: North American Leukemia Intergroup Study C9710. Blood 116, 3751-3757.
79. Prochazka, L., Dong, L. F., Valis, K., Freeman, R., Ralph, S. J., Turanek, J., et al. (2010). alpha-Tocopheryl succinate causes mitochondrial permeabilization by preferential formation of Bak channels. Apoptosis 15, 782-794.
80. Ralph, S. J., and Neuzil, J. (2009). Mitochondria as targets for cancer therapy. Mol. Nutr. Food Res. 53, 9-28.
81. Ramos, J., Sirisawad, M., Miller, R., and Naumovski, L. (2006). Motexafin gadolinium modulates levels of phosphorylated Akt and synergizes with inhibitors of Akt phosphorylation. Mol. Cancer Ther. 5, 1176-1182.
82. Rasola, A., Sciacovelli, M., Chiara, F., Pantic, B., Brusilow, W. S., and Bernardi, P. (2010). Activation of mitochondrial ERK protects cancer cells from death through inhibition of the permeability transition. Proc. Natl. Acad. Sci. U.S.A. 107, 726-731.
83. Ready, N., Karaseva, N. A., Orlov, S. V., Luft, A. V., Popovych, O., Holmlund, J. T., et al. (2011). Double-blind, placebo-controlled, randomized phase 2 study of the proapoptotic agent AT-101 plus docetaxel, in second-line non-small cell lung cancer. J. Thorac. Oncol. 6, 781-785.
84. Rostovtseva, T. K., Antonsson, B., Suzuki, M., Youle, R. J., Colombini, M., and Bezrukov, S. M. (2004). Bid, but not Bax, regulates VDAC channels. J. Biol. Chem. 279, 13575-13583.
85. Rostovtseva, T. K., Tan, W., and Colombini, M. (2005). On the role of VDAC in apoptosis: fact and fiction. J. Bioenerg. Biomembr. 37, 129-142.
86. Roy, S. S., Madesh, M., Davies, E., Antonsson, B., Danial, N., and Hajnoczky, G. (2009). Bad targets the permeability transition pore independent of Bax or Bak to switch between Ca2+-dependent cell survival and death. Mol. Cell 33, 377-388.
87. Rudin, C. M., Hann, C. L., Garon, E. B., Ribeiro De Oliveira, M., Bonomi, P. D., Camidge, D. R., et al. (2012). Phase II study of single-agent navitoclax (ABT-263) and biomarker correlates in patients with relapsed small cell lung cancer. Clin. Cancer Res. 18, 3163-3169.
88. Schubert, A., and Grimm, S. (2004). Cyclophilin, D, a component of the permeability transition-pore, is an apoptosis repressor. Cancer Res. 64, 85-93.
89. Selzer, E., Thallinger, C., Hoeller, C., Oberkleiner, P., Wacheck, V., Pehamberger, H., et al. (2002). Betulinic acid-induced Mcl-1 expression in human melanoma-mode of action and functional significance. Mol. Med. 8, 877-884.
90. Shehzad, A., Wahid, F., and Lee, Y. S. (2010). Curcumin in cancer chemoprevention: molecular targets, pharmacokinetics, bioavailability, and clinical trials. Arch. Pharm. (Weinheim) 343, 489-499.
91. Shimizu, S., Ide, T., Yanagida, T., and Tsujimoto, Y. (2000). Electrophysiological study of a novel large pore formed by Bax and the voltage-dependent anion channel that is permeable to cytochrome c. J. Biol. Chem. 275, 12321-12325.
92. Shoshan-Barmatz, V., and Ben-Hail, D. (2012). VDAC, a multi-functional mitochondrial protein as a pharmacological target. Mitochondrion 12, 24-34.
93. Shulga, N., Wilson-Smith, R., and Pastorino, J. G. (2009). Hexokinase II detachment from the mitochondria potentiates cisplatin induced cytotoxicity through a caspase-2 dependent mechanism. Cell Cycle 8, 3355-3364.
94. Simamura, E., Hirai, K., Shimada, H., Koyama, J., Niwa, Y., and Shimizu, S. (2006). Furanonaphthoquinones cause apoptosis of cancer cells by inducing the production of reactive oxygen species by the mitochondrial voltage-dependent anion channel. Cancer Biol. Ther. 5, 1523-1529.
95. Simonin, K., Brotin, E., Dufort, S., Dutoit, S., Goux, D., N'Diaye, M., et al. (2009). Mcl-1 is an important determinant of the apoptotic response to the BH3-mimetic molecule HA14-1 in cisplatin-resistant ovarian carcinoma cells. Mol. Cancer Ther. 8, 3162-3170.
96. Singh, S., and Khar, A. (2006). Biological effects of curcumin and its role in cancer chemoprevention and therapy. Anticancer Agents Med. Chem. 6, 259-270.
97. Slack, J. L., and Rusiniak, M. E. (2000). Current issues in the management of acute promyelocytic leukemia. Ann. Hematol. 79, 227-238.
98. Szabo, I., De Pinto, V., and Zoratti, M. (1993). The mitochondrial permeability transition pore may comprise VDAC molecules. II. The electrophysiological properties of VDAC are compatible with those of the mitochondrial megachannel. FEBS Lett. 330, 206-210.
99. Tan, W., Loke, Y. H., Stein, C. A., Miller, P., and Colombini, M. (2007). Phosphorothioate oligonucleotides block the VDAC channel. Biophys. J. 93, 1184-1191.
100. Tikunov, A., Johnson, C. B., Pediaditakis, P., Markevich, N., Macdonald, J. M., Lemasters, J. J., et al. (2010). Closure of VDAC causes oxidative stress and accelerates the Ca(2+)-induced mitochondrial permeability transition in rat liver mitochondria. Arch. Biochem. Biophys. 495, 174-181.
101. Traba, J., Del Arco, A., Duchen, M. R., Szabadkai, G., and Satrustegui, J. (2012). SCaMC-1 promotes cancer cell survival by desensitizing mitochondrial permeability transition via ATP/ADP-mediated matrix Ca(2+) buffering. Cell Death Differ. 19, 650-660.
102. Van Delft, M. F., Wei, A. H., Mason, K. D., Vandenberg, C. J., Chen, L., Czabotar, P. E., et al. (2006). The BH3 mimetic ABT-737 targets selective Bcl-2 proteins and efficiently induces apoptosis via Bak/Bax if Mcl-1 is neutralized. Cancer Cell 10, 389-399.
103. Vander Heiden, M. G., Li, X. X., Gottleib, E., Hill, R. B., Thompson, C. B., and Colombini, M. (2001). Bcl-xL promotes the open configuration of the voltage-dependent anion channel and metabolite passage through the outer mitochondrial membrane. J. Biol. Chem. 276, 19414-19419.
104. Van Poznak, C., Seidman, A. D., Reidenberg, M. M., Moasser, M. M., Sklarin, N., Van Zee, K., et al. (2001). Oral gossypol in the treatment of patients with refractory metastatic breast cancer: a phase I/II clinical trial. Breast Cancer Res. Treat. 66, 239-248.
105. Vyssokikh, M. Y., and Brdiczka, D. (2003). The function of complexes between the outer mitochondrial membrane pore (VDAC) and the adenine nucleotide translocase in regulation of energy metabolism and apoptosis. Acta Biochim. Pol. 50, 389-404.
106. Wang, J. L., Liu, D., Zhang, Z. J., Shan, S., Han, X., Srinivasula, S. M., et al. (2000). Structure-based discovery of an organic compound that binds Bcl-2 protein and induces apoptosis of tumor cells. Proc. Natl. Acad. Sci. U.S.A. 97, 7124-7129.
107. Wenner, C. E. (2012). Targeting mitochondria as a therapeutic target in cancer. J. Cell Physiol. 227, 450-456.
108. Willis, S. N., Chen, L., Dewson, G., Wei, A., Naik, E., Fletcher, J. I., et al. (2005). Proapoptotic Bak is sequestered by Mcl-1 and Bcl-xL, but not Bcl-2, until displaced by BH3-only proteins. Genes Dev. 19, 1294-1305.
109. Wilson, W. H., O'Connor, O. A., Czuczman, M. S., Lacasce, A. S., Gerecitano, J. F., Leonard, J. P., et al. (2010). Navitoclax, a targeted high-affinity inhibitor of BCL-2, in lymphoid malignancies: a phase 1 dose-escalation study of safety, pharmacokinetics, pharmacodynamics, and antitumour activity. Lancet Oncol. 11, 1149-1159.
110. Youle, R. J., and Strasser, A. (2008). The BCL-2 protein family: opposing activities that mediate cell death. Nat. Rev. Mol. Cell Biol. 9, 47-59.
111. Zalk, R., Israelson, A., Garty, E. S., Azoulay-Zohar, H., and Shoshan-Barmatz, V. (2005). Oligomeric states of the voltage-dependent anion channel and cytochrome c release from mitochondria. Biochem. J. 386, 73-83.
112. Zhang, S., Li, G., Ma, X., Wang, Y., Liu, G., Feng, L., et al. (2012). Norcantharidin enhances ABT-737-induced apoptosis in hepatocellular carcinoma cells by transcriptional repression of Mcl-1. Cell. Signal. 24, 1803-1809.
113. Zheng, Y., Shi, Y., Tian, C., Jiang, C., Jin, H., Chen, J., et al. (2004). Essential role of the voltage-dependent anion channel (VDAC) in mitochondrial permeability transition pore opening and cytochrome c release induced by arsenic trioxide. Oncogene 23, 1239-1247.