Mediation of the antiapoptotic activity of Bcl-xL protein upon interaction with VDAC1 protein

Journal of Biological Chemistry

Volumn 287, Issue 27, 2012, Pages 23152-23161

  Arbel, Nir ^a   Ben Hail, Danya ^a   Shoshan Barmatz, Varda ^a  

^a BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

ANTI-APOPTOTIC PROTEIN; ANTIAPOPTOTIC ACTIVITIES; CANCER CELLS; CHANNEL CONDUCTANCE; CHANNEL CONDUCTIVITY; CHEMOTHERAPEUTIC AGENTS; DIRECT INTERACTIONS; MICRO-SCALES; MITOCHONDRIAL PROTEIN; N-TERMINAL DOMAINS; OVER-EXPRESSION; SYNTHETIC PEPTIDE; TERMINAL REGIONS; TIME-DEPENDENT; TUMOR CELLS; VOLTAGE-DEPENDENT ANION CHANNELS;

CELL DEATH; MITOCHONDRIA; PEPTIDES; PLANTS (BOTANY);

RECOMBINANT PROTEINS;

PROTEIN BCL XL; STAUROSPORINE; SYNTHETIC PEPTIDE; VOLTAGE DEPENDENT ANION CHANNEL 1;

AMINO TERMINAL SEQUENCE; APOPTOSIS; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL PROTECTION; CELL SURVIVAL; CHANNEL GATING; CONCENTRATION RESPONSE; CONTROLLED STUDY; GENE MUTATION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; INHIBITION KINETICS; MITOCHONDRION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN PURIFICATION; SURFACE PLASMON RESONANCE; TIME; TUMOR CELL;

APOPTOSIS; BCL-X PROTEIN; DRUG RESISTANCE, NEOPLASM; HEK293 CELLS; HUMANS; MITOCHONDRIA; NEOPLASMS; PEPTIDE FRAGMENTS; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN STRUCTURE, TERTIARY; RNA, SMALL INTERFERING; SURFACE PLASMON RESONANCE; VOLTAGE-DEPENDENT ANION CHANNEL 1;

EID: 84863316405     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.345918     Document Type: Article

References (60)

1. Cory, S., and Adams, J. M. (2002) The Bcl2 family: regulators of the cellular life-or-death switch. Nat. Rev. Cancer 2, 647-656 (Pubitemid 37328916)
2. Reed, J. C. (2002) Apoptosis-based therapies. Nat. Rev. Drug Discov. 1, 111-121
3. 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
4. Adams, J. M., and Cory, S. (2007) The Bcl-2 apoptotic switch in cancer development and therapy. Oncogene 26, 1324-1337 (Pubitemid 46328466)
5. Certo, M., Del Gaizo Moore, V., Nishino, M., Wei, G., Korsmeyer, S., Armstrong, S. A., and Letai, A. (2006) Mitochondria primed by death signals determine cellular addiction to antiapoptotic BCL-2 family members. Cancer Cell 9, 351-365 (Pubitemid 43668734)
6. Gross, A., McDonnell, J. M., and Korsmeyer, S. J. (1999) BCL-2 family members and the mitochondria in apoptosis. Genes Dev. 13, 1899-1911 (Pubitemid 29407357)
7. Sentman, C. L., Shutter, J. R., Hockenbery, D., Kanagawa, O., and Korsmeyer, S. J. (1991) bcl-2 inhibits multiple forms of apoptosis but not negative selection in thymocytes. Cell 67, 879-888 (Pubitemid 121001502)
8. Oancea, M., Mani, A., Hussein, M. A., and Almasan, A. (2004) Apoptosis of multiple myeloma. Int. J. Hematol. 80, 224-231 (Pubitemid 39410928)
9. Tsujimoto, Y., Finger, L. R., Yunis, J., Nowell, P. C., and Croce, C. M. (1984) Cloning of the chromosome breakpoint of neoplastic B cells with the t(14;18) chromosome translocation. Science 226, 1097-1099 (Pubitemid 15217831)
10. Scorrano, L., and Korsmeyer, S. J. (2003) Mechanisms of cytochrome c release by proapoptotic BCL-2 family members. Biochem. Biophys. Res. Commun. 304, 437-444 (Pubitemid 36506515)
11. Arbel, N., and Shoshan-Barmatz, V. (2010) Voltage-dependent anion channel 1-based peptides interact with Bcl-2 to prevent antiapoptotic activity. J. Biol. Chem. 285, 6053-6062
12. Malia, T. J., and Wagner, G. (2007) NMR structural investigation of the mitochondrial outer membrane protein VDAC and its interaction with antiapoptotic Bcl-xL. Biochemistry 46, 514-525 (Pubitemid 46105440)
13. Bayrhuber, M., Meins, T., Habeck, M., Becker, S., Giller, K., Villinger, S., Vonrhein, C., Griesinger, C., Zweckstetter, M., and Zeth, K. (2008) Structure of the human voltage-dependent anion channel. Proc. Natl. Acad. Sci. U.S.A. 105, 15370-15375
14. Hiller, S., Garces, R. G., Malia, T. J., Orekhov, V. Y., Colombini, M., and Wagner, G. (2008) Solution structure of the integral human membrane protein VDAC-1 in detergent micelles. Science 321, 1206-1210
15. Ujwal, R., Cascio, D., Colletier, J. P., Faham, S., Zhang, J., Toro, L., Ping, P., and Abramson, J. (2008) The crystal structure of mouse VDAC1 at 2.3 Å resolution reveals mechanistic insights into metabolite gating. Proc. Natl. Acad. Sci. U.S.A. 105, 17742-17747
16. Gincel, D., Silberberg, S. D., and Shoshan-Barmatz, V. (2000) Modulation of the voltage-dependent anion channel (VDAC) by glutamate. J. Bioenerg. Biomembr. 32, 571-583 (Pubitemid 32204234)
17. Colombini, M. (2004) VDAC: the channel at the interface between mitochondria and the cytosol. Mol. Cell. Biochem. 256-257, 107-115
18. Shoshan-Barmatz, V., De Pinto, V., Zweckstetter, M., Raviv, Z., Keinan, N., and Arbel, N. (2010) VDAC, a multifunctional mitochondrial protein regulating cell life and death. Mol. Aspects Med. 31, 227-285
19. Abu-Hamad, S., Arbel, N., Calo, D., Arzoine, L., Israelson, A., Keinan, N., Ben-Romano, R., Friedman, O., and Shoshan-Barmatz, V. (2009) The VDAC1 N terminus is essential both for apoptosis and the protective effect of antiapoptotic proteins. J. Cell Sci. 122, 1906-1916
20. Kroemer, G., Galluzzi, L., and Brenner, C. (2007) Mitochondrial membrane permeabilization in cell death. Physiol. Rev. 87, 99-163 (Pubitemid 46209992)
21. Shimizu, S., Shinohara, Y., and Tsujimoto, Y. (2000) Bax and Bcl-xL independently regulate apoptotic changes of yeast mitochondria that require VDAC but not adenine nucleotide translocator. Oncogene 19, 4309-4318
22. 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 (Pubitemid 38468883)
23. Shimizu, S., Matsuoka, Y., Shinohara, Y., Yoneda, Y., and Tsujimoto, Y. (2001) Essential role of voltage-dependent anion channel in various forms of apoptosis in mammalian cells. J. Cell Biol. 152, 237-250 (Pubitemid 34285595)
24. Shi, Y., Chen, J., Weng, C., Chen, R., Zheng, Y., Chen, Q., and Tang, H. (2003) Identification of the protein-protein contact site and interaction mode of human VDAC1 with Bcl-2 family proteins. Biochem. Biophys. Res. Commun. 305, 989-996 (Pubitemid 36597861)
25. Boise, L. H., González-García, M., Postema, C. E., Ding, L., Lindsten, T., Turka, L. A., Mao, X., Nuñez, G., and Thompson, C. B. (1993) bcl-x, a bcl-2-related gene that functions as a dominant regulator of apoptotic cell death. Cell 74, 597-608 (Pubitemid 23259741)
26. Johnson, B. W., Cepero, E., and Boise, L. H. (2000) Bcl-xL inhibits cytochrome c release but not mitochondrial depolarization during the activation of multiple death pathways by tumor necrosis factor-α. J. Biol. Chem. 275, 31546-31553
27. Zaid, H., Abu-Hamad, S., Israelson, A., Nathan, I., and Shoshan-Barmatz, V. (2005) The voltage-dependent anion channel-1 modulates apoptotic cell death. Cell Death Differ. 12, 751-760 (Pubitemid 40945982)
28. Shoshan-Barmatz, V., and Gincel, D. (2003) The voltage-dependent anion channel: characterization, modulation, and role in mitochondrial function in cell life and death. Cell Biochem. Biophys. 39, 279-292 (Pubitemid 41270796)
29. Gincel, D., Zaid, H., and Shoshan-Barmatz, V. (2001) Calcium binding and translocation by the voltage-dependent anion channel: a possible regulatory mechanism in mitochondrial function. Biochem. J. 358, 147-155 (Pubitemid 32778108)
30. Wienken, C. J., Baaske, P., Rothbauer, U., Braun, D., and Duhr, S. (2010) Protein binding assays in biological liquids using microscale thermophoresis. Nat. Commun. 1, 100
31. Zillner, K., Jerabek-Willemsen, M., Duhr, S., Braun, D., Längst, G., and Baaske, P. (2012) Microscale thermophoresis as a sensitive method to quantify protein: nucleic acid interactions in solution. Methods Mol. Biol. 815, 241-252
32. Arzoine, L., Zilberberg, N., Ben-Romano, R., and Shoshan-Barmatz, V. (2009) Voltage-dependent anion channel 1-based peptides interact with hexokinase to prevent its antiapoptotic activity. J. Biol. Chem. 284, 3946-3955
33. Reed, J. C. (2008) Bcl-2 family proteins and hematologic malignancies: history and future prospects. Blood 111, 3322-3330
34. Reed, J. C. (1999) Fenretinide: the death of a tumor cell. J. Nat. Cancer Inst. 91, 1099-1100
35. Kang, M. H., and Reynolds, C. P. (2009) Bcl-2 inhibitors: targeting mitochondrial apoptotic pathways in cancer therapy. Clin. Cancer Res. 15, 1126-1132
36. Adams, J. M., and Cory, S. (1998) The Bcl-2 protein family: arbiters of cell survival. Science 281, 1322-1326 (Pubitemid 28406819)
37. Youle, R. J. (2007) Cell biology: cellular demolition and the rules of engagement. Science 315, 776-777
38. Chipuk, J. E., and Green, D. R. (2008) How do BCL-2 proteins induce mitochondrial outer membrane permeabilization? Trends Cell Biol. 18, 157-164
39. L sequester BH3 domain-only molecules preventing BAX- and BAK-mediated mitochondrial apoptosis. Mol. Cell 8, 705-711
40. Mahajan, N. P., Linder, K., Berry, G., Gordon, G. W., Heim, R., and Herman, B. (1998) Bcl-2 and Bax interactions in mitochondria probed with green fluorescent protein and fluorescence resonance energy transfer. Nat. Biotechnol. 16, 547-552 (Pubitemid 28269812)
41. Zhou, F., Yang, Y., and Xing, D. (2011) Bcl-2 and Bcl-xL play important roles in the crosstalk between autophagy and apoptosis. FEBS J. 278, 403-413
42. Hagn, F., Klein, C., Demmer, O., Marchenko, N., Vaseva, A., Moll, U. M., and Kessler, H. (2010) BclxL changes conformation upon binding to wildtype but not mutant p53 DNA-binding domain. J. Biol. Chem. 285, 3439-3450
43. Petros, A. M., Gunasekera, A., Xu, N., Olejniczak, E. T., and Fesik, S. W. (2004) Defining the p53 DNA-binding domain/Bcl-xL-binding interface using NMR. FEBS Lett. 559, 171-174 (Pubitemid 38186723)
44. Kaufmann, T., Schlipf, S., Sanz, J., Neubert, K., Stein, R., and Borner, C. (2003) Characterization of the signal that directs Bcl-xL, but not Bcl-2, to the mitochondrial outer membrane. J. Cell Biol. 160, 53-64 (Pubitemid 36091716)
45. Zheng, Y., Shi, Y., Tian, C., Jiang, C., Jin, H., Chen, J., Almasan, A., Tang, H., and Chen, Q. (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 (Pubitemid 38297178)
46. Chen-Levy, Z., and Cleary, M. L. (1990) Membrane topology of the Bcl-2 proto-oncogenic protein demonstrated in vitro. J. Biol. Chem. 265, 4929-4933
47. Janiak, F., Leber, B., and Andrews, D. W. (1994) Assembly of Bcl-2 into microsomal and outer mitochondrial membranes. J. Biol. Chem. 269, 9842-9849 (Pubitemid 24196593)
48. Nguyen, M., Millar, D. G., Yong, V. W., Korsmeyer, S. J., and Shore, G. C. (1993) Targeting of Bcl-2 to the mitochondrial outer membrane by a COOH-terminal signal anchor sequence. J. Biol. Chem. 268, 25265-25268 (Pubitemid 23358123)
49. Tanaka, S., Saito, K., and Reed, J. C. (1993) Structure-function analysis of the Bcl-2 oncoprotein: addition of a heterologous transmembrane domain to portions of the Bcl-2β protein restores function as a regulator of cell survival. J. Biol. Chem. 268, 10920-10926 (Pubitemid 23162274)
50. Abu-Hamad, S., Zaid, H., Israelson, A., Nahon, E., and Shoshan-Barmatz, V. (2008) Hexokinase-I protection against apoptotic cell death is mediated via interaction with the voltage-dependent anion channel-1: mapping the site of binding. J. Biol. Chem. 283, 13482-13490
51. Zhai, D., Jin, C., Huang, Z., Satterthwait, A. C., and Reed, J. C. (2008) Differential regulation of Bax and Bak by antiapoptotic Bcl-2 family proteins Bcl-B and Mcl-1. J. Biol. Chem. 283, 9580-9586
52. Gross, A., Yin, X. M., Wang, K., Wei, M. C., Jockel, J., Milliman, C., Erdjument-Bromage, H., Tempst, P., and Korsmeyer, S. J. (1999) Caspase cleaved BID targets mitochondria and is required for cytochrome c release, while BCL-XL prevents this release but not tumor necrosis factor- R1/Fas death. J. Biol. Chem. 274, 1156-1163
53. Yi, X., Yin, X. M., and Dong, Z. (2003) Inhibition of Bid-induced apoptosis by Bcl-2: tBid insertion, Bax translocation, and Bax/Bak oligomerization suppressed. J. Biol. Chem. 278, 16992-16999 (Pubitemid 36799574)
54. Willis, S. N., Chen, L., Dewson, G., Wei, A., Naik, E., Fletcher, J. I., Adams, J. M., and Huang, D. C. (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 (Pubitemid 41003019)
55. 2+ signaling and apoptosis by the BH4 domain of Bcl-2 versus Bcl-Xl. Cell Death Diff. 19, 295-309
56. Khaw, S. L., Huang, D. C., and Roberts, A. W. (2011) Overcoming blocks in apoptosis with BH3-mimetic therapy in hematological malignancies. Pathology 43, 525-535
57. Oltersdorf, T., Elmore, S. W., Shoemaker, A. R., Armstrong, R. C., Augeri, D. J., Belli, B. A., Bruncko, M., Deckwerth, T. L., Dinges, J., Hajduk, P. J., Joseph, M. K., Kitada, S., Korsmeyer, S. J., Kunzer, A. R., Letai, A., Li, C., Mitten, M. J., Nettesheim, D. G., Ng, S., Nimmer, P. M., O'Connor, J. M., Oleksijew, A., Petros, A. M., Reed, J. C., Shen, W., Tahir, S. K., Thompson, C. B., Tomaselli, K. J., Wang, B., Wendt, M. D., Zhang, H., Fesik, S. W., and Rosenberg, S. H. (2005) An inhibitor of Bcl-2 family proteins induces regression of solid tumors. Nature 435, 677-681 (Pubitemid 40825512)
58. Dias, N., and Stein, C. A. (2002) Antisense oligonucleotides: basic concepts and mechanisms. Mol. Cancer Ther. 1, 347-355
59. Vogler, M., Dinsdale, D., Dyer, M. J., and Cohen, G. M. (2009) Bcl-2 inhibitors: small molecules with a big impact on cancer therapy. Cell Death Diff. 16, 360-367
60. Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685