Oligomerization of the mitochondrial protein VDAC1: From structure to function and cancer therapy

Progress in Molecular Biology and Translational Science

Volumn 117, Issue , 2013, Pages 303-334

  Shoshan Barmatz, Varda ^a   Mizrachi, Dario ^a   Keinan, Nurit ^a  

^a BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

Author keywords

Apoptosis; Contact sites; Mitochondria; N terminal domain; Oligomerization; VDAC

Indexed keywords

CYTOCHROME C; MITOCHONDRIAL PROTEIN; OLIGOMER; PROTEIN BAK; PROTEIN BAX; PROTEIN BCL 2; VOLTAGE DEPENDENT ANION CHANNEL 1;

ANIMAL; APOPTOSIS; ARTICLE; BIOLOGICAL MODEL; CANCER THERAPY; CELL CYCLE; CELL DEATH; CELL FUNCTION; CHEMICAL STRUCTURE; CHEMISTRY; ENZYME MECHANISM; GENE OVEREXPRESSION; HUMAN; ION TRANSPORT; MAMMAL CELL; MEMBRANE STRUCTURE; METABOLISM; METABOLITE; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; NEOPLASM; NONHUMAN; OLIGOMERIZATION; OUTER MEMBRANE; PROTEIN FUNCTION; PROTEIN MULTIMERIZATION; PROTEIN POLYMERIZATION; PROTEIN SECRETION; STRUCTURE ANALYSIS;

EID: 84896689626     PISSN: 18771173     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-386931-9.00011-8     Document Type: Chapter

References (160)

1. E. Gulbins, S. Dreschers, and J. Bock Role of mitochondria in apoptosis Exp Physiol 88 2003 85 90
2. G. Kroemer, and J.C. Reed Mitochondrial control of cell death Nat Med 6 2000 513 519
3. S. Desagher, and J.C. Martinou Mitochondria as the central control point of apoptosis Trends Cell Biol 10 2000 369 377
4. J.A. Keeble, and A.P. Gilmore Apoptosis commitment - translating survival signals into decisions on mitochondria Cell Res 17 2007 976 984
5. G. Kroemer, L. Galluzzi, and C. Brenner Mitochondrial membrane permeabilization in cell death Physiol Rev 87 2007 99 163
6. M. Le Bras, M.V. Clement, S. Pervaiz, and C. Brenner Reactive oxygen species and the mitochondrial signaling pathway of cell death Histol Histopathol 20 2005 205 219
7. J.A. Hickman Apoptosis and tumourigenesis Curr Opin Genet Dev 12 2002 67 72
8. R.W. Johnstone, A.A. Ruefli, and S.W. Lowe Apoptosis: a link between cancer genetics and chemotherapy Cell 108 2002 153 164
9. S. Yasuhara, A. Asai, N.D. Sahani, and J.A. Martyn Mitochondria, endoplasmic reticulum, and alternative pathways of cell death in critical illness Crit Care Med 35 2007 S488 S495
10. I. Chowdhury, B. Tharakan, and G.K. Bhat Current concepts in apoptosis: the physiological suicide program revisited Cell Mol Biol Lett 11 2006 506 525
11. D.R. Green, and G.I. Evan A matter of life and death Cancer Cell 1 2002 19 30
12. M. Crompton The mitochondrial permeability transition pore and its role in cell death Biochem J 341 Pt. 2 1999 233 249
13. R.A. Gottlieb Role of mitochondria in apoptosis Crit Rev Eukaryot Gene Expr 10 2000 231 239
14. G.Q. Wang, B.R. Gastman, E. Wieckowski, L.A. Goldstein, A. Gambotto, and T.H. Kim A role for mitochondrial Bak in apoptotic response to anticancer drugs J Biol Chem 276 2001 34307 34317
15. J.F. Lovell, L.P. Billen, S. Bindner, A. Shamas-Din, C. Fradin, and B. Leber Membrane binding by tBid initiates an ordered series of events culminating in membrane permeabilization by Bax Cell 135 2008 1074 1084
16. D. Westphal, G. Dewson, P.E. Czabotar, and R.M. Kluck Molecular biology of Bax and Bak activation and action Biochim Biophys Acta 1813 2011 521 531
17. A. Shamas-Din, H. Brahmbhatt, B. Leber, and D.W. Andrews BH3-only proteins: orchestrators of apoptosis Biochim Biophys Acta 1813 2011 508 520
18. R. Sundararajan, A. Cuconati, D. Nelson, and E. White Tumor necrosis factor-alpha induces Bax-Bak interaction and apoptosis, which is inhibited by adenovirus E1B 19K J Biol Chem 276 2001 45120 45127
19. G.C. Shore Apoptosis: it's BAK to VDAC EMBO Rep 10 2009 1311 1313
20. G.C. Shore, and M. Nguyen Bcl-2 proteins and apoptosis: choose your partner Cell 135 2008 1004 1006
21. S.C. Ruffolo, and G.C. Shore BCL-2 selectively interacts with the BID-induced open conformer of BAK, inhibiting BAK auto-oligomerization J Biol Chem 278 2003 25039 25045
22. G. Dewson, T. Kratina, P. Czabotar, C.L. Day, J.M. Adams, and R.M. Kluck Bak activation for apoptosis involves oligomerization of dimers via their alpha6 helices Mol Cell 36 2009 696 703
23. H. Kim, H.C. Tu, D. Ren, O. Takeuchi, J.R. Jeffers, and G.P. Zambetti Stepwise activation of BAX and BAK by tBID, BIM, and PUMA initiates mitochondrial apoptosis Mol Cell 36 2009 487 499
24. D. Ren, H.C. Tu, H. Kim, G.X. Wang, G.R. Bean, and O. Takeuchi BID, BIM, and PUMA are essential for activation of the BAX- and BAK-dependent cell death program Science 330 2010 1390 1393
25. K.D. Hinsch, Asmarinah, E. Hinsch, and L. Konrad VDAC2 (porin-2) expression pattern and localization in the bovine testis Biochim Biophys Acta 1518 2001 329 333
26. L. Thomas, E. Blachly-Dyson, M. Colombini, and M. Forte Mapping of residues forming the voltage sensor of the voltage-dependent anion-selective channel Proc Natl Acad Sci USA 90 1993 5446 5449
27. A. Messina, F. Guarino, M. Oliva, L.P. van den Heuvel, J. Smeitink, and V. De Pinto Characterization of the human porin isoform 1 (HVDAC1) gene by amplification on the whole human genome: a tool for porin deficiency analysis Biochem Biophys Res Commun 270 2000 787 792
28. M.J. Sampson, R.S. Lovell, and W.J. Craigen The murine voltage-dependent anion channel gene family. Conserved structure and function J Biol Chem 272 1997 18966 18973
29. E. Blachly-Dyson, E.B. Zambronicz, W.H. Yu, V. Adams, E.R. McCabe, and J. Adelman Cloning and functional expression in yeast of two human isoforms of the outer mitochondrial membrane channel, the voltage-dependent anion channel J Biol Chem 268 1993 1835 1841
30. X. Xu, W. Decker, M.J. Sampson, W.J. Craigen, and M. Colombini Mouse VDAC isoforms expressed in yeast: channel properties and their roles in mitochondrial outer membrane permeability J Membr Biol 170 1999 89 102
31. M.J. Sampson, R.S. Lovell, D.B. Davison, and W.J. Craigen A novel mouse mitochondrial voltage-dependent anion channel gene localizes to chromosome 8 Genomics 36 1996 192 196
32. K.D. Hinsch, V. De Pinto, V.A. Aires, X. Schneider, A. Messina, and E. Hinsch Voltage-dependent anion-selective channels VDAC2 and VDAC3 are abundant proteins in bovine outer dense fibers, a cytoskeletal component of the sperm flagellum J Biol Chem 279 2004 15281 15288
33. X. Triphan, V.A. Menzel, A.M. Petrunkina, M.C. Cassara, W. Wemheuer, and K.D. Hinsch Localisation and function of voltage-dependent anion channels (VDAC) in bovine spermatozoa Pflugers Arch 455 2008 677 686
34. Y. Shinohara, T. Ishida, M. Hino, N. Yamazaki, Y. Baba, and H. Terada Characterization of porin isoforms expressed in tumor cells Eur J Biochem 267 2000 6067 6073
35. W.H. Yu, W. Wolfgang, and M. Forte Subcellular localization of human voltage-dependent anion channel isoforms J Biol Chem 270 1995 13998 14006
36. M. Huizing, W. Ruitenbeek, L.P. van den Heuvel, V. Dolce, V. Iacobazzi, and J.A. Smeitink Human mitochondrial transmembrane metabolite carriers: tissue distribution and its implication for mitochondrial disorders J Bioenerg Biomembr 30 1998 277 284
37. E.H. Cheng, T.V. Sheiko, J.K. Fisher, W.J. Craigen, and S.J. Korsmeyer VDAC2 inhibits BAK activation and mitochondrial apoptosis Science 301 2003 513 517
38. V. Shoshan-Barmatz, V. De Pinto, M. Zweckstetter, Z. Raviv, N. Keinan, and N. Arbel VDAC, a multi-functional mitochondrial protein regulating cell life and death Mol Aspects Med 31 2010 227 285
39. S. Wu, M.J. Sampson, W.K. Decker, and W.J. Craigen Each mammalian mitochondrial outer membrane porin protein is dispensable: effects on cellular respiration Biochim Biophys Acta 1452 1999 68 78
40. M.J. Sampson, W.K. Decker, A.L. Beaudet, W. Ruitenbeek, D. Armstrong, and M.J. Hicks Immotile sperm and infertility in mice lacking mitochondrial voltage-dependent anion channel type 3 J Biol Chem 276 2001 39206 39212
41. E.J. Weeber, M. Levy, M.J. Sampson, K. Anflous, D.L. Armstrong, and S.E. Brown The role of mitochondrial porins and the permeability transition pore in learning and synaptic plasticity J Biol Chem 277 2002 18891 18897
42. D. Chandra, G. Choy, P.T. Daniel, and D.G. Tang Bax-dependent regulation of Bak by voltage-dependent anion channel 2 J Biol Chem 280 2005 19051 19061
43. T. Yamamoto, A. Yamada, M. Watanabe, Y. Yoshimura, N. Yamazaki, and Y. Yoshimura VDAC1, having a shorter N-terminus than VDAC2 but showing the same migration in an SDS-polyacrylamide gel, is the predominant form expressed in mitochondria of various tissues J Proteome Res 5 2006 3336 3344
44. V. De Pinto, F. Guarino, Andrea Guarnera, A. Messina, S. Reina, and F.M. Tomasello Characterization of human vdac isoforms: a peculiar function for vdac3? Biochim Biophys Acta 1797 2010 1268 1275
45. M. Bayrhuber, T. Meins, M. Habeck, S. Becker, K. Giller, and S. Villinger Structure of the human voltage-dependent anion channel Proc Natl Acad Sci USA 105 2008 15370 15375
46. S. Hiller, R.G. Garces, T.J. Malia, V.Y. Orekhov, M. Colombini, and G. Wagner Solution structure of the integral human membrane protein VDAC-1 in detergent micelles Science 321 2008 1206 1210
47. R. Ujwal, D. Cascio, J.P. Colletier, S. Faham, J. Zhang, and L. Toro The crystal structure of mouse VDAC1 at 2.3 A resolution reveals mechanistic insights into metabolite gating Proc Natl Acad Sci USA 105 2008 17742 17747
48. S. Hiller, and G. Wagner The role of solution NMR in the structure determinations of VDAC-1 and other membrane proteins Curr Opin Struct Biol 19 2009 396 401
49. S. Geula, D. Ben-Hail, and V. Shoshan-Barmatz Structure-based analysis of VDAC1: N-terminus location, translocation, channel gating and association with anti-apoptotic proteins Biochem J 444 2012 475 485
50. D.A. Koppel, K.W. Kinnally, P. Masters, M. Forte, E. Blachly-Dyson, and C.A. Mannella Bacterial expression and characterization of the mitochondrial outer membrane channel. Effects of n-terminal modifications J Biol Chem 273 1998 13794 13800
51. C.A. Mannella Minireview: on the structure and gating mechanism of the mitochondrial channel, VDAC J Bioenerg Biomembr 29 1997 525 531
52. B. Popp, D.A. Court, R. Benz, W. Neupert, and R. Lill The role of the N and C termini of recombinant Neurospora mitochondrial porin in channel formation and voltage-dependent gating J Biol Chem 271 1996 13593 13599
53. P.R. Junankar, A.F. Dulhunty, S.M. Curtis, S.M. Pace, and F.P. Thinnes Porin-type 1 proteins in sarcoplasmic reticulum and plasmalemma of striated muscle fibres J Muscle Res Cell Motil 16 1995 595 610
54. S. Abu-Hamad, S. Sivan, and V. Shoshan-Barmatz The expression level of the voltage-dependent anion channel controls life and death of the cell Proc Natl Acad Sci USA 103 2006 5787 5792
55. H. Azoulay-Zohar, A. Israelson, S. Abu-Hamad, and V. Shoshan-Barmatz In self-defence: hexokinase promotes voltage-dependent anion channel closure and prevents mitochondria-mediated apoptotic cell death Biochem J 377 2004 347 355
56. S. Abu-Hamad, N. Arbel, D. Calo, L. Arzoine, A. Israelson, and N. Keinan The VDAC1 N-terminus is essential both for apoptosis and the protective effect of anti-apoptotic proteins J Cell Sci 122 2009 1906 1916
57. Y. Shi, J. Chen, C. Weng, R. Chen, Y. Zheng, and Q. Chen Identification of the protein-protein contact site and interaction mode of human VDAC1 with Bcl-2 family proteins Biochem Biophys Res Commun 305 2003 989 996
58. N. Arbel, D. Ben-Hail, and V. Shoshan-Barmatz Mediation of the anti-apoptotic activity of Bcl-xL upon interaction with VDAC1 J Biol Chem 287 2012 23152 23161
59. N. Arbel, and V. Shoshan-Barmatz Voltage-dependent anion channel 1-based peptides interact with Bcl-2 to prevent antiapoptotic activity J Biol Chem 285 2010 6053 6062
60. L. Arzoine, N. Zilberberg, R. Ben-Romano, and V. Shoshan-Barmatz Voltage-dependent anion channel 1-based peptides interact with hexokinase to prevent its anti-apoptotic activity J Biol Chem 284 2009 3946 3955
61. V. Shoshan-Barmatz, N. Arbel, and L. Arzoine VDAC, the voltage-dependent anion channel: function, regulation & mitochondrial signaling in cell life and death Cell Sci 4 2008 74 118
62. R. Zalk, A. Israelson, E. Garty, H. Azoulay-Zohar, and V. Shoshan-Barmatz Oligomeric states of the voltage-dependent anion channel and cytochrome c release from mitochondria Biochem J 386 2005 73 83
63. K. Zeth, T. Meins, and C. Vonrhein Approaching the structure of human VDAC1, a key molecule in mitochondrial cross-talk J Bioenerg Biomembr 40 2008 127 132
64. R.P. Goncalves, N. Buzhynskyy, V. Prima, J.N. Sturgis, and S. Scheuring Supramolecular assembly of VDAC in native mitochondrial outer membranes J Mol Biol 369 2007 413 418
65. B.W. Hoogenboom, K. Suda, A. Engel, and D. Fotiadis The supramolecular assemblies of voltage-dependent anion channels in the native membrane J Mol Biol 370 2007 246 255
66. N. Keinan, D. Tyomkin, and V. Shoshan-Barmatz Oligomerization of the mitochondrial protein voltage-dependent anion channel is coupled to the induction of apoptosis Mol Cell Biol 30 2010 5698 5709
67. T.J. Malia, and G. Wagner NMR structural investigation of the mitochondrial outer membrane protein VDAC and its interaction with antiapoptotic Bcl-xL Biochemistry 46 2007 514 525
68. V. Shoshan-Barmatz, N. Keinan, and H. Zaid Uncovering the role of VDAC in the regulation of cell life and death J Bioenerg Biomembr 40 2008 183 191
69. X.W. Guo, P.R. Smith, B. Cognon, D. D'Arcangelis, E. Dolginova, and C.A. Mannella Molecular design of the voltage-dependent, anion-selective channel in the mitochondrial outer membrane J Struct Biol 114 1995 41 59
70. R. Ujwal, D. Cascio, V. Chaptal, P. Ping, and J. Abramson Crystal packing analysis of murine VDAC1 crystals in a lipidic environment reveals novel insights on oligomerization and orientation Channels (Austin) 3 2009 167 170
71. V. Betaneli, E.P. Petrov, and P. Schwille The role of lipids in VDAC oligomerization Biophys J 102 2012 523 531
72. G. Xie, and J.E. Wilson Tetrameric structure of mitochondrially bound rat brain hexokinase: a crosslinking study Arch Biochem Biophys 276 1990 285 293
73. D. Brdiczka, P. Kaldis, and T. Wallimann In vitro complex formation between the octamer of mitochondrial creatine kinase and porin J Biol Chem 269 1994 27640 27644
74. O. Stachowiak, U. Schlattner, M. Dolder, and T. Wallimann Oligomeric state and membrane binding behaviour of creatine kinase isoenzymes: implications for cellular function and mitochondrial structure Mol Cell Biochem 184 1998 141 151
75. U. Schlattner, M. Dolder, T. Wallimann, and M. Tokarska-Schlattner Mitochondrial creatine kinase and mitochondrial outer membrane porin show a direct interaction that is modulated by calcium J Biol Chem 276 2001 48027 48030
76. D. Gincel, H. Zaid, and V. Shoshan-Barmatz Calcium binding and translocation by the voltage-dependent anion channel: a possible regulatory mechanism in mitochondrial function Biochem J 358 2001 147 155
77. R. Benz Permeation of hydrophilic solutes through mitochondrial outer membranes: review on mitochondrial porins Biochim Biophys Acta 1197 1994 167 196
78. M. Colombini Structure and mode of action of a voltage dependent anion-selective channel (VDAC) located in the outer mitochondrial membrane Ann N Y Acad Sci 341 1980 552 563
79. D. Gincel, S.D. Silberberg, and V. Shoshan-Barmatz Modulation of the voltage-dependent anion channel (VDAC) by glutamate J Bioenerg Biomembr 32 2000 571 583
80. V. De Pinto, M. Tommasino, R. Benz, and F. Palmieri The 35 kDa DCCD-binding protein from pig heart mitochondria is the mitochondrial porin Biochim Biophys Acta 813 1985 230 242
81. C.A. Mannella, X.W. Guo, and B. Cognon Diameter of the mitochondrial outer membrane channel: evidence from electron microscopy of frozen-hydrated membrane crystals FEBS Lett 253 1989 231 234
82. T. Hodge, and M. Colombini Regulation of metabolite flux through voltage-gating of VDAC channels J Membr Biol 157 1997 271 279
83. T. Rostovtseva, and M. Colombini VDAC channels mediate and gate the flow of ATP: implications for the regulation of mitochondrial function Biophys J 72 1997 1954 1962
84. R. Benz, M. Kottke, and D. Brdiczka The cationically selective state of the mitochondrial outer membrane pore: a study with intact mitochondria and reconstituted mitochondrial porin Biochim Biophys Acta 1022 1990 311 318
85. Y. Tsujimoto, and S. Shimizu The voltage-dependent anion channel: an essential player in apoptosis Biochimie 84 2002 187 193
86. V. De Pinto, A. Messina, R. Accardi, R. Aiello, F. Guarino, and M.F. Tomasello New functions of an old protein: the eukaryotic porin or voltage dependent anion selective channel (VDAC) Ital J Biochem 52 2003 17 24
87. M.Y. Vyssokikh, and D. Brdiczka 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 2003 389 404
88. D.J. Granville, and R.A. Gottlieb The mitochondrial voltage-dependent anion channel (VDAC) as a therapeutic target for initiating cell death Curr Med Chem 10 2003 1527 1533
89. J.J. Lemasters, and E. Holmuhamedov Voltage-dependent anion channel (VDAC) as mitochondrial governator - thinking outside the box Biochim Biophys Acta 1762 2006 181 190
90. V. Shoshan-Barmatz, and D. Gincel The voltage-dependent anion channel: characterization, modulation, and role in mitochondrial function in cell life and death Cell Biochem Biophys 39 2003 279 292
91. V. Shoshan-Barmatz, A. Israelson, D. Brdiczka, and S.S. Sheu The voltage-dependent anion channel (VDAC): function in intracellular signalling, cell life and cell death Curr Pharm Des 12 2006 2249 2270
92. V. Shoshan-Barmatz, and D. Ben-Hail VDAC, a multi-functional mitochondrial protein as a pharmacological target Mitochondrion 12 2012 24 34
93. V. Shoshan-Barmatz, and M. Golan Mitochondrial VDAC1: function in cell life and death and a target for cancer therapy Curr Med Chem 19 2012 714 735
94. P. Bernardi Mitochondrial transport of cations: channels, exchangers, and permeability transition Physiol Rev 79 1999 1127 1155
95. Y. Tsujimoto, and S. Shimizu Role of the mitochondrial membrane permeability transition in cell death Apoptosis 12 2007 835 840
96. J.J. Lemasters Modulation of mitochondrial membrane permeability in pathogenesis, autophagy and control of metabolism J Gastroenterol Hepatol 22 Suppl. 1 2007 S31 S37
97. S. Shimizu, M. Narita, and Y. Tsujimoto Bcl-2 family proteins regulate the release of apoptogenic cytochrome c by the mitochondrial channel VDAC Nature 399 1999 483 487
98. S. Shimizu, T. Ide, T. Yanagida, and Y. Tsujimoto 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 2000 12321 12325
99. M.G. Vander Heiden, N.S. Chandel, X.X. Li, P.T. Schumacker, M. Colombini, and C.B. Thompson Outer mitochondrial membrane permeability can regulate coupled respiration and cell survival Proc Natl Acad Sci USA 97 2000 4666 4671
100. T.K. Rostovtseva, W. Tan, and M. Colombini On the role of VDAC in apoptosis: fact and fiction J Bioenerg Biomembr 37 2005 129 142
101. C.P. Baines, R.A. Kaiser, T. Sheiko, W.J. Craigen, and J.D. Molkentin Voltage-dependent anion channels are dispensable for mitochondrial-dependent cell death Nat Cell Biol 9 2007 550 555
102. K.S. McCommis, and C.P. Baines The role of VDAC in cell death: friend or foe? Biochim Biophys Acta 1818 2012 1444 1450
103. M. Madesh, and G. Hajnoczky VDAC-dependent permeabilization of the outer mitochondrial membrane by superoxide induces rapid and massive cytochrome c release J Cell Biol 155 2001 1003 1015
104. S. Shimizu, Y. Matsuoka, Y. Shinohara, Y. Yoneda, and Y. Tsujimoto Essential role of voltage-dependent anion channel in various forms of apoptosis in mammalian cells J Cell Biol 152 2001 237 250
105. Y. Zheng, Y. Shi, C. Tian, C. Jiang, H. Jin, and J. Chen 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 2004 1239 1247
106. S. Abu-Hamad, H. Zaid, A. Israelson, E. Nahon, and V. Shoshan-Barmatz 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 2008 13482 13490
107. H. Zaid, S. Abu-Hamad, A. Israelson, I. Nathan, and V. Shoshan-Barmatz The voltage-dependent anion channel-1 modulates apoptotic cell death Cell Death Differ 12 2005 751 760
108. A. Israelson, H. Zaid, S. Abu-Hamad, E. Nahon, and V. Shoshan-Barmatz Mapping the ruthenium red-binding site of the voltage-dependent anion channel-1 Cell Calcium 43 2008 196 204
109. A. Israelson, S. Abu-Hamad, H. Zaid, E. Nahon, and V. Shoshan-Barmatz Localization of the voltage-dependent anion channel-1 Ca2+-binding sites Cell Calcium 41 2007 235 244
110. N. Tajeddine, L. Galluzzi, O. Kepp, E. Hangen, E. Morselli, and L. Senovilla Hierarchical involvement of Bak, VDAC1 and Bax in cisplatin-induced cell death Oncogene 27 2008 4221 4232
111. S. Yuan, Y. Fu, X. Wang, H. Shi, Y. Huang, and X. Song Voltage-dependent anion channel 1 is involved in endostatin-induced endothelial cell apoptosis FASEB J 22 2008 2809 2820
112. V. Shoshan-Barmatz, N. Keinan, S. Abu-Hamad, D. Tyomkin, and L. Aram Apoptosis is regulated by the VDAC1 N-terminal region and by VDAC oligomerization: release of cytochrome c AIF and Smac/Diablo Biochim Biophys Acta 1797 2010 1281 1291
113. A. Mader, S. Abu-Hamad, N. Arbel, M. Gutierrez-Aguilar, and V. Shoshan-Barmatz Dominant-negative VDAC1 mutants reveal oligomeric VDAC1 to be the active unit in mitochondria-mediated apoptosis Biochem J 429 2010 147 155
114. S. Geula, H. Naveed, J. Liang, and V. Shoshan-Barmatz Structure-based analysis of VDAC1 protein: defining oligomer contact sites J Biol Chem 287 2012 2179 2190
115. V. Shoshan-Barmatz, and D. Mizrachi VDAC1: from structure to cancer therapy Front Oncol 2 2012 164
116. L. Aram, S. Geula, N. Arbel, and V. Shoshan-Barmatz VDAC1 cysteine residues: topology and function in channel activity and apoptosis Biochem J 427 2010 445 454
117. S.M. Moin, M. Panteva, and S. Jameel The hepatitis E virus Orf3 protein protects cells from mitochondrial depolarization and death J Biol Chem 282 2007 21124 21133
118. A.M. Florea, and D. Busselberg Anti-cancer drugs interfere with intracellular calcium signaling Neurotoxicology 30 2009 803 810
119. A. Rasola, and P. Bernardi Mitochondrial permeability transition in Ca(2 +)-dependent apoptosis and necrosis Cell Calcium 50 2011 222 233
120. Y. Shidoji, K. Hayashi, S. Komura, N. Ohishi, and K. Yagi Loss of molecular interaction between cytochrome c and cardiolipin due to lipid peroxidation Biochem Biophys Res Commun 264 1999 343 347
121. Y. Huang, L. Liu, C. Shi, J. Huang, and G. Li Electrochemical analysis of the effect of Ca2 + on cardiolipin-cytochrome c interaction Biochim Biophys Acta 1760 2006 1827 1830
122. J. Liu, A. Weiss, D. Durrant, N.W. Chi, and R.M. Lee The cardiolipin-binding domain of Bid affects mitochondrial respiration and enhances cytochrome c release Apoptosis 9 2004 533 541
123. V. Shoshan-Barmatz, N. Hadad, W. Feng, I. Shafir, I. Orr, and M. Varsanyi VDAC/porin is present in sarcoplasmic reticulum from skeletal muscle FEBS Lett 386 1996 205 210
124. E. Simamura, K. Hirai, H. Shimada, J. Koyama, Y. Niwa, and S. Shimizu 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 2006 1523 1529
125. L. Veenman, Y. Shandalov, and M. Gavish VDAC activation by the 18 kDa translocator protein (TSPO), implications for apoptosis J Bioenerg Biomembr 40 2008 199 205
126. M. Gavish, I. Bachman, R. Shoukrun, Y. Katz, L. Veenman, and G. Weisinger Enigma of the peripheral benzodiazepine receptor Pharmacol Rev 51 1999 629 650
127. E. Levin, A. Premkumar, L. Veenman, W. Kugler, S. Leschiner, and I. Spanier The peripheral-type benzodiazepine receptor and tumorigenicity: isoquinoline binding protein (IBP) antisense knockdown in the C6 glioma cell line Biochemistry 44 2005 9924 9935
128. L. Veenman, E. Levin, G. Weisinger, S. Leschiner, I. Spanier, and S.H. Snyder Peripheral-type benzodiazepine receptor density and in vitro tumorigenicity of glioma cell lines Biochem Pharmacol 68 2004 689 698
129. I. Golani, A. Weizman, S. Leschiner, I. Spanier, N. Eckstein, and R. Limor Hormonal regulation of peripheral benzodiazepine receptor binding properties is mediated by subunit interaction Biochemistry 40 2001 10213 10222
130. L. Veenman, S. Leschiner, I. Spanier, G. Weisinger, A. Weizman, and M. Gavish PK 11195 attenuates kainic acid-induced seizures and alterations in peripheral-type benzodiazepine receptor (PBR) protein components in the rat brain J Neurochem 80 2002 917 927
131. L. Veenman, V. Papadopoulos, and M. Gavish Channel-like functions of the 18-kDa translocator protein (TSPO): regulation of apoptosis and steroidogenesis as part of the host-defense response Curr Pharm Des 13 2007 2385 2405
132. J.Y. Jung, C.R. Han, Y.J. Jeong, H.J. Kim, H.S. Lim, and K.H. Lee Epigallocatechin gallate inhibits nitric oxide-induced apoptosis in rat PC12 cells Neurosci Lett 411 2007 222 227
133. A. Godbole, J. Varghese, A. Sarin, and M.K. Mathew VDAC is a conserved element of death pathways in plant and animal systems Biochim Biophys Acta 1642 2003 87 96
134. A.J. Lu, C.W. Dong, C.S. Du, and Q.Y. Zhang Characterization and expression analysis of Paralichthys olivaceus voltage-dependent anion channel (VDAC) gene in response to virus infection Fish Shellfish Immunol 23 2007 601 613
135. I. Shafir, W. Feng, and V. Shoshan-Barmataz Voltage-dependent anion channel proteins in synaptosomes of the torpedo electric organ: immunolocalization, purification, and characterization J Bioenerg Biomembr 30 1998 499 510
136. T. Ghosh, N. Pandey, A. Maitra, S.K. Brahmachari, and B. Pillai A role for voltage-dependent anion channel Vdac1 in polyglutamine-mediated neuronal cell death PLoS One 2 2007 e1170
137. N. Jiang, S.K. Kham, G.S. Koh, J.Y. Suang Lim, H. Ariffin, and F.T. Chew Identification of prognostic protein biomarkers in childhood acute lymphoblastic leukemia (ALL) J Proteomics 74 2011 843 857
138. A. Castagna, P. Antonioli, H. Astner, M. Hamdan, S.C. Righetti, and P. Perego A proteomic approach to cisplatin resistance in the cervix squamous cell carcinoma cell line A431 Proteomics 4 2004 3246 3267
139. D.W. Voehringer, D.L. Hirschberg, J. Xiao, Q. Lu, M. Roederer, and C.B. Lock Gene microarray identification of redox and mitochondrial elements that control resistance or sensitivity to apoptosis Proc Natl Acad Sci USA 97 2000 2680 2685
140. J. Nawarak, R. Huang-Liu, S.H. Kao, H.H. Liao, S. Sinchaikul, and S.T. Chen Proteomics analysis of A375 human malignant melanoma cells in response to arbutin treatment Biochim Biophys Acta 1794 2009 159 167
141. S.L. Cheng, R.H. Liu, J.N. Sheu, S.T. Chen, S. Sinchaikul, and G.J. Tsay Toxicogenomics of A375 human malignant melanoma cells treated with arbutin J Biomed Sci 14 2007 87 105
142. J.C. Lai, W. Tan, L. Benimetskaya, P. Miller, M. Colombini, and C.A. Stein A pharmacologic target of G3139 in melanoma cells may be the mitochondrial VDAC Proc Natl Acad Sci USA 103 2006 7494 7499
143. N. Tajeddine, L. Galluzzi, O. Kepp, E. Hangen, E. Morselli, and L. Senovilla Hierarchical involvement of Bak, VDAC1 and Bax in cisplatin-induced cell death Oncogene 10 2008 4221 4232
144. F. Tomasello, A. Messina, L. Lartigue, L. Schembri, C. Medina, and S. Reina Outer membrane VDAC1 controls permeability transition of the inner mitochondrial membrane in cellulo during stress-induced apoptosis Cell Res 19 2009 1363 1376
145. E. Simamura, H. Shimada, Y. Ishigaki, T. Hatta, N. Higashi, and K. Hirai Bioreductive activation of quinone antitumor drugs by mitochondrial voltage-dependent anion channel 1 Anat Sci Int 83 2008 261 266
146. S. Liu, H. Ishikawa, N. Tsuyama, F.J. Li, S. Abroun, and K.I. Otsuyama Increased susceptibility to apoptosis in CD45(+) myeloma cells accompanied by the increased expression of VDAC1 Oncogene 25 2006 419 429
147. Y. Takagi-Morishita, N. Yamada, A. Sugihara, T. Iwasaki, T. Tsujimura, and N. Terada Mouse uterine epithelial apoptosis is associated with expression of mitochondrial voltage-dependent anion channels, release of cytochrome C from mitochondria, and the ratio of Bax to Bcl-2 or Bcl-X Biol Reprod 68 2003 1178 1184
148. O. Sharaf el dein, C. Gallerne, C. Brenner, and C. Lemaire Increased expression of VDAC1 sensitizes carcinoma cells to apoptosis induced by DNA cross-linking agents Biochem Pharmacol 83 2012 1172 1182
149. V. De Pinto, F. Tomasello, A. Messina, F. Guarino, R. Benz, and D. La Mendola Determination of the conformation of the human VDAC1 N-terminal peptide, a protein moiety essential for the functional properties of the pore Chembiochem 8 2007 744 756
150. J. Banerjee, and S. Ghosh Bax increases the pore size of rat brain mitochondrial voltage-dependent anion channel in the presence of tBid Biochem Biophys Res Commun 323 2004 310 314
151. J. Yu, H. Qian, Y. Li, Y. Wang, X. Zhang, and X. Liang Therapeutic effect of arsenic trioxide (As2O3) on cervical cancer in vitro and in vivo through apoptosis induction Cancer Biol Ther 6 2007 580 586
152. J.G. Pastorino, N. Shulga, and J.B. Hoek Mitochondrial binding of hexokinase II inhibits Bax-induced cytochrome c release and apoptosis J Biol Chem 277 2002 7610 7618
153. S. Shimizu, and Y. Tsujimoto Proapoptotic BH3-only Bcl-2 family members induce cytochrome c release, but not mitochondrial membrane potential loss, and do not directly modulate voltage-dependent anion channel activity Proc Natl Acad Sci USA 97 2000 577 582
154. K.M. Debatin, D. Poncet, and G. Kroemer Chemotherapy: targeting the mitochondrial cell death pathway Oncogene 21 2002 8786 8803
155. D.B. Huckabee, and M.B. Jekabsons Identification of Bax-voltage-dependent anion channel 1 complexes in digitonin-solubilized cerebellar granule neurons J Neurochem 119 2011 1137 1150
156. M. Adachi, H. Higuchi, S. Miura, T. Azuma, S. Inokuchi, and H. Saito Bax interacts with the voltage-dependent anion channel and mediates ethanol-induced apoptosis in rat hepatocytes Am J Physiol Gastrointest Liver Physiol 287 2004 G695 G705
157. M.B. Heaton, K. Siler-Marsiglio, M. Paiva, A. Kotler, J. Rogozinski, and S. Kubovec Ethanol influences on bax associations with mitochondrial membrane proteins in neonatal rat cerebellum Dev Neurobiol 73 2013 127 141
158. G. Cao, M. Minami, W. Pei, C. Yan, D. Chen, and C. O'Horo Intracellular Bax translocation after transient cerebral ischemia: implications for a role of the mitochondrial apoptotic signaling pathway in ischemic neuronal death J Cereb Blood Flow Metab 21 2001 321 333
159. S.S. Roy, A.M. Ehrlich, W.J. Craigen, and G. Hajnoczky VDAC2 is required for truncated BID-induced mitochondrial apoptosis by recruiting BAK to the mitochondria EMBO Rep 10 2009 1341 1347
160. P. Costantini, E. Jacotot, D. Decaudin, and G. Kroemer Mitochondrion as a novel target of anticancer chemotherapy J Natl Cancer Inst 92 2000 1042 1053