Voltage-dependant anion channels: Novel insights into isoform function through genetic models

Biochimica et Biophysica Acta - Biomembranes

Volumn 1818, Issue 6, 2012, Pages 1477-1485

  Raghavan, Adithya ^a   Sheiko, Tatiana ^a   Graham, Brett H ^a   Craigen, William J ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Animal model; Drosophila; Mitochondria; Mouse knock out; Porin; Voltage dependent anion channel

Indexed keywords

COMPLEMENTARY DNA; HEXOKINASE; MITOCHONDRIAL PERMEABILITY TRANSITION PORE; PORIN; PROSTAGLANDIN SYNTHASE; VOLTAGE DEPENDENT ANION CHANNEL; VOLTAGE DEPENDENT ANION CHANNEL 1; VOLTAGE DEPENDENT ANION CHANNEL 3;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; ALTERNATIVE RNA SPLICING; ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; CELL GROWTH; CELL METABOLISM; CELL SURVIVAL; COMPLEX FORMATION; CONTROLLED STUDY; EMBRYONIC STEM CELL; ENZYME REGULATION; EXON; FERTILITY; GENETIC MODEL; GLYCOLYSIS; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; OUTER MEMBRANE; PHENOTYPE; POLYADENYLATION; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; EMBRYONIC STEM CELLS; HUMANS; MODELS, GENETIC; PROTEIN ISOFORMS; VOLTAGE-DEPENDENT ANION CHANNELS;

ANIMALIA; HEXAPODA; MAMMALIA;

EID: 84859747227     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2011.10.019     Document Type: Review

References (87)

1. S. Burdman, R. De Mot, J. Vanderleyden, Y. Okon, E. Jurkevitch, Identification and characterization of the omaA gene encoding the major outer membrane protein of Azospirillum brasilense, DNA Seq. 11 (2000) 225-237.
2. K. Anflous, D.D. Armstrong, W.J. Craigen, Altered mitochondrial sensitivity for ADP and maintenance of creatine-stimulated respiration in oxidative striated muscles from VDAC1-deficient mice, J. Biol. Chem. 276 (2001) 1954-1960. (Pubitemid 32109673)
3. M. Colombini, VDAC: the channel at the interface between mitochondria and the cytosol, Mol. Cell. Biochem. 256-257 (2004) 107-115. (Pubitemid 38181239)
4. J.G. Pastorino, J.B. Hoek, Regulation of hexokinase binding to VDAC, J. Bioenerg. Biomembr. 40 (2008) 171-182.
5. W. Tan, M. Colombini, VDAC closure increases calcium ion flux, Biochim. Biophys. Acta 1768 (2007) 2510-2515. (Pubitemid 47532032)
6. P. Bernardi, Mitochondrial transport of cations: channels, exchangers, and permeability transition, Physiol. Rev. 79 (1999) 1127-1155. (Pubitemid 29473313)
7. M.C. Wei, T. Lindsten, V.K. Mootha, S. Weiler, A. Gross, M. Ashiya, C.B. Thompson, S.J. Korsmeyer, tBID, a membrane-targeted death ligand, oligomerizes BAK to release cytochrome c, Genes Dev. 14 (2000) 2060-2071. (Pubitemid 30637355)
8. V. Shoshan-Barmatz, N. Keinan, H. Zaid, Uncovering the role of VDAC in the regulation of cell life and death, J. Bioenerg. Biomembr. 40 (2008) 183-191.
9. M.J. Young, D.C. Bay, G. Hausner, D.A. Court, The evolutionary history of mitochondrial porins, BMC Evol. Biol. 7 (2007) 31.
10. M.J. Sampson, R.S. Lovell, W.J. Craigen, The murine voltage-dependent anion channel gene family. Conserved structure and function, J. Biol. Chem. 272 (1997) 18966-18973. (Pubitemid 27318251)
11. K. Zeth, M. Thein, Porins in prokaryotes and eukaryotes: common themes and variations, Biochem. J. 431 (2010) 13-22.
12. E. Blachly-Dyson, J. Song, W.J. Wolfgang, M. Colombini, M. Forte, Multicopy suppressors of phenotypes resulting from the absence of yeast VDAC encode a VDAC-like protein, Mol. Cell. Biol. 17 (1997) 5727-5738. (Pubitemid 27411080)
13. M. Dihanich, K. Suda, G. Schatz, A yeast mutant lacking mitochondrial porin is respiratory-deficient, but can recover respiration with simultaneous accumulation of an 86-kd extramitochondrial protein, EMBO J. 6 (1987) 723-728.
14. S. Shimizu, M. Narita, Y. Tsujimoto, Bcl-2 family proteins regulate the release of apoptogenic cytochrome c by the mitochondrial channel VDAC, Nature 399 (1999) 483-487. (Pubitemid 29258855)
15. S. Shimizu, Y. Shinohara, Y. Tsujimoto, Bax and Bcl-xL independently regulate apoptotic changes of yeast mitochondria that require VDAC but not adenine nucleotide translocator, Oncogene 19 (2000) 4309-4318.
16. M.H. Harris, M.G. Vander Heiden, S.J. Kron, C.B. Thompson, Role of oxidative phosphorylation in Bax toxicity, Mol. Cell. Biol. 20 (2000) 3590-3596. (Pubitemid 30243904)
17. H. Zaid, S. Abu-Hamad, A. Israelson, I. Nathan, V. Shoshan-Barmatz, The voltage-dependent anion channel-1 modulates apoptotic cell death, Cell Death Differ. 12 (2005) 751-760. (Pubitemid 40945982)
18. M. Priault, B. Chaudhuri, A. Clow, N. Camougrand, S. Manon, Investigation of bax-induced release of cytochrome c from yeast mitochondria permeability of mitochondrial membranes, role of VDAC and ATP requirement, Eur. J. Biochem. 260 (1999) 684-691. (Pubitemid 29148633)
19. P. Polcic, M. Forte, Response of yeast to the regulated expression of proteins in the Bcl-2 family, Biochem. J. 374 (2003) 393-402. (Pubitemid 37094098)
20. H. Galganska, M. Antoniewicz, M. Budzinska, L. Galganski, H. Kmita, VDAC contributes to mRNA levels in Saccharomyces cerevisiae cells by the intracellular reduction/oxidation state dependent and independent mechanisms, J. Bioenerg. Biomembr. 42 (2010) 483-489.
21. H. Galganska, A. Karachitos, M. Wojtkowska, O. Stobienia, M. Budzinska, H. Kmita, Communication between mitochondria and nucleus: putative role for VDAC in reduction/oxidation mechanism, Biochim. Biophys. Acta 1797 (2010) 1276-1280.
22. N. Averet, H. Aguilaniu, O. Bunoust, L. Gustafsson, M. Rigoulet, NADH is specifically channeled through the mitochondrial porin channel in Saccharomyces cerevisiae, J. Bioenerg. Biomembr. 34 (2002) 499-506. (Pubitemid 36384286)
23. H. Galganska, M. Budzinska, M. Wojtkowska, H. Kmita, Redox regulation of protein expression in Saccharomyces cerevisiae mitochondria: possible role of VDAC, Arch. Biochem. Biophys. 479 (2008) 39-45.
24. L. Thomas, E. Blachly-Dyson, M. Colombini, M. Forte, Mapping of residues forming the voltage sensor of the voltage-dependent anion-selective channel, Proc. Natl. Acad. Sci. U. S. A. 90 (1993) 5446-5449. (Pubitemid 23176177)
25. B.H. Graham, W.J. Craigen, Mitochondrial voltage-dependent anion channel gene family in Drosophila melanogaster: complex patterns of evolution, genomic organization, and developmental expression, Mol. Genet. Metab. 85 (2005) 308-317. (Pubitemid 41074115)
26. V. Shoshan-Barmatz, V. De Pinto, M. Zweckstetter, Z. Raviv, N. Keinan, N. Arbel, VDAC, a multi-functional mitochondrial protein regulating cell life and death, Mol. Aspects Med. 31 (2010) 227-285.
27. L.C. Boffa, G. Cutrona, M. Cilli, M.R. Mariani, S. Matis, M. Pastorino, G. Damonte, E. Millo, S. Roncella, M. Ferrarini, Therapeutically promising PNA complementary to a regulatory sequence for c-myc: pharmacokinetics in an animal model of human Burkitt's lymphoma, Oligonucleotides 15 (2005) 85-93. (Pubitemid 40967414)
28. B.H. Graham, Z. Li, E.P. Alesii, P. Versteken, C. Lee, J. Wang, W.J. Craigen, Neurologic dysfunction and male infertility in Drosophila porin mutants: a new model for mitochondrial dysfunction and disease, J. Biol. Chem. 285 (2010) 11143-11153.
29. J. Park, Y. Kim, S. Choi, H. Koh, S.H. Lee, J.M. Kim, J. Chung, Drosophila Porin/VDAC affects mitochondrial morphology, PLoS One 5 (2010) e13151.
30. M.J. Sampson, R.S. Lovell, W.J. Craigen, Isolation, characterization, and mapping of two mouse mitochondrial voltage-dependent anion channel isoforms, Genomics 33 (1996) 283-288. (Pubitemid 26132124)
31. M.J. Sampson, R.S. Lovell, D.B. Davison, W.J. Craigen, A novel mouse mitochondrial voltage-dependent anion channel gene localizes to chromosome 8, Genomics 36 (1996) 192-196. (Pubitemid 26277778)
32. A. Messina, M. Oliva, C. Rosato, M. Huizing, W. Ruitenbeek, L.P. van den Heuvel, M. Forte, M. Rocchi, V. De Pinto, Mapping of the human voltage-dependent anion channel isoforms 1 and 2 reconsidered, Biochem. Biophys. Res. Commun. 255 (1999) 707-710. (Pubitemid 29294863)
33. E. Blachly-Dyson, E.B. Zambronicz, W.H. Yu, V. Adams, E.R. McCabe, J. Adelman, M. Colombini, M. Forte, 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. (Pubitemid 23033582)
34. H. Ha, P. Hajek, D.M. Bedwell, P.D. Burrows, A mitochondrial porin cDNA predicts the existence of multiple human porins, J. Biol. Chem. 268 (1993) 12143-12149. (Pubitemid 23168182)
35. K. Anflous, O. Blondel, A. Bernard, M. Khrestchatisky, R. Ventura-Clapier, Characterization of rat porin isoforms: cloning of a cardiac type-3 variant encoding an additional methionine at its putative N-terminal region, Biochim. Biophys. Acta 1399 (1998) 47-50. (Pubitemid 28374914)
36. W.K. Decker, W.J. Craigen, The tissue-specific, alternatively spliced single ATG exon of the type 3 voltage-dependent anion channel gene does not create a truncated protein isoform in vivo, Mol. Genet. Metab. 70 (2000) 69-74. (Pubitemid 30396206)
37. M.J. Sampson, L. Ross, W.K. Decker, W.J. Craigen, A novel isoform of the mitochondrial outer membrane protein VDAC3 via alternative splicing of a 3-base exon. Functional characteristics and subcellular localization, J. Biol. Chem. 273 (1998) 30482-30486. (Pubitemid 28545523)
38. S. Kuersten, E.B. Goodwin, The power of the 3′ UTR: translational control and development, Nat. Rev. Genet. 4 (2003) 626-637. (Pubitemid 36917504)
39. B. Mazumder, V. Seshadri, P.L. Fox, Translational control by the 3′-UTR: the ends specify the means, Trends Biochem. Sci. 28 (2003) 91-98. (Pubitemid 36165138)
40. T. Bonome, J.Y. Lee, D.C. Park, M. Radonovich, C. Pise-Masison, J. Brady, G.J. Gardner, K. Hao, W.H. Wong, J.C. Barrett, K.H. Lu, A.K. Sood, D.M. Gershenson, S.C. Mok, M.J. Birrer, Expression profiling of serous low malignant potential, low-grade, and high-grade tumors of the ovary, Cancer Res. 65 (2005) 10602-10612. (Pubitemid 41743756)
41. M. Legendre, W. Ritchie, F. Lopez, D. Gautheret, Differential repression of alternative transcripts: a screen for miRNA targets, PLoS Comput. Biol. 2 (2006) e43.
42. C.S. Lutz, Alternative polyadenylation: a twist on mRNA 3′ end formation, ACS Chem. Biol. 3 (2008) 609-617.
43. E.H. Kislauskis, Z. Li, R.H. Singer, K.L. Taneja, Isoform-specific 3′-untranslated sequences sort alpha-cardiac and beta-cytoplasmic actin messenger RNAs to different cytoplasmic compartments, J. Cell Biol. 123 (1993) 165-172. (Pubitemid 23284872)
44. W.K. Decker, K.R. Bowles, E.C. Schatte, J.A. Towbin, W.J. Craigen, Revised fine mapping of the human voltage-dependent anion channel loci by radiation hybrid analysis, Mamm. Genome 10 (1999) 1041-1042. (Pubitemid 29470953)
45. X. Xu, W. Decker, M.J. Sampson, W.J. Craigen, 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. (Pubitemid 29367689)
46. S. Wu, M.J. Sampson, W.K. Decker, W.J. Craigen, Each mammalian mitochondrial outer membrane porin protein is dispensable: effects on cellular respiration, Biochim. Biophys. Acta 1452 (1999) 68-78. (Pubitemid 29486743)
47. E.J. Weeber, M. Levy, M.J. Sampson, K. Anflous, D.L. Armstrong, S.E. Brown, J.D. Sweatt, W.J. Craigen, The role of mitochondrial porins and the permeability transition pore in learning and synaptic plasticity, J. Biol. Chem. 277 (2002) 18891-18897. (Pubitemid 34952449)
48. B.H. Graham, J. David Sweatt, W.J. Craigen, Noninvasive, in vivo approaches to evaluating behavior and exercise physiology in mouse models of mitochondrial disease, Methods 26 (2002) 364-370. (Pubitemid 34971577)
49. M. Crompton, S. Virji, J.M. Ward, Cyclophilin-D binds strongly to complexes of the voltage-dependent anion channel and the adenine nucleotide translocase to form the permeability transition pore, Eur. J. Biochem. 258 (1998) 729-735. (Pubitemid 28557940)
50. I. Szabo, V. De Pinto, M. Zoratti, 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 (1993) 206-210.
51. M.W. McEnery, A.M. Snowman, R.R. Trifiletti, S.H. Snyder, Isolation of the mitochondrial benzodiazepine receptor: association with the voltage-dependent anion channel and the adenine nucleotide carrier, Proc. Natl. Acad. Sci. U. S. A. 89 (1992) 3170-3174.
52. A.P. Halestrap, What is the mitochondrial permeability transition pore? J. Mol. Cell. Cardiol. 46 (2009) 821-831.
53. F. Ichas, L.S. Jouaville, J.P. Mazat, Mitochondria are excitable organelles capable of generating and conveying electrical and calcium signals, Cell 89 (1997) 1145-1153. (Pubitemid 127678747)
54. J.M. Dubinsky, N. Brustovetsky, V. Pinelis, B.S. Kristal, C. Herman, X. Li, The mitochondrial permeability transition: the brain's point of view, Biochem. Soc. Symp. 66 (1999) 75-84. (Pubitemid 129639024)
55. M. Levy, G.C. Faas, P. Saggau, W.J. Craigen, J.D. Sweatt, Mitochondrial regulation of synaptic plasticity in the hippocampus, J. Biol. Chem. 278 (2003) 17727-17734. (Pubitemid 36799375)
56. C.P. Baines, R.A. Kaiser, T. Sheiko, W.J. Craigen, J.D. Molkentin, Voltage-dependent anion channels are dispensable for mitochondrial-dependent cell death, Nat. Cell Biol. 9 (2007) 550-555. (Pubitemid 46696536)
57. J.C. St John, R.P. Jokhi, C.L. Barratt, The impact of mitochondrial genetics on male infertility, Int. J. Androl. 28 (2005) 65-73. (Pubitemid 40461175)
58. M.J. Sampson, W.K. Decker, A.L. Beaudet, W. Ruitenbeek, D. Armstrong, M.J. Hicks, W.J. Craigen, Immotile sperm and infertility in mice lacking mitochondrial voltage-dependent anion channel type 3, J. Biol. Chem. 276 (2001) 39206-39212.
59. K. Anflous-Pharayra, N. Lee, D.L. Armstrong, W.J. Craigen, VDAC3 has differing mitochondrial functions in two types of striated muscles, Biochim. Biophys. Acta 1807 (2011) 150-156.
60. P.L. Pedersen, Voltage dependent anion channels (VDACs): a brief introduction with a focus on the outer mitochondrial compartment's roles together with hexokinase-2 in the "Warburg effect" in cancer, J. Bioenerg. Biomembr. 40 (2008) 123-126.
61. R.A. Nakashima, P.S. Mangan, M. Colombini, P.L. Pedersen, Hexokinase receptor complex in hepatoma mitochondria: evidence from N, N′- dicyclohexylcarbodiimide- labeling studies for the involvement of the pore-forming protein VDAC, Biochemistry 25 (1986) 1015-1021. (Pubitemid 16099500)
62. J.A. Al Jamal, Involvement of porin N,N-dicyclohexylcarbodiimide-reactive domain in hexokinase binding to the outer mitochondrial membrane, Protein J. 24 (2005) 1-8. (Pubitemid 40933097)
63. S.P. Mathupala, P.L. Pedersen, Voltage dependent anion channel-1 (VDAC-1) as an anti-cancer target, Cancer Biol. Ther. 9 (2010) 1053-1056.
64. J.G. Pastorino, J.B. Hoek, N. Shulga, 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 (2005) 10545-10554. (Pubitemid 41743749)
65. K.K. Arora, P.L. Pedersen, Functional significance of mitochondrial bound hexokinase in tumor cell metabolism. Evidence for preferential phosphorylation of glucose by intramitochondrially generated ATP, J. Biol. Chem. 263 (1988) 17422-17428. (Pubitemid 19029327)
66. O. Warburg, On respiratory impairment in cancer cells, Science 124 (1956) 269-270.
67. K. Anflous-Pharayra, Z.J. Cai, W.J. Craigen, VDAC1 serves as a mitochondrial binding site for hexokinase in oxidative muscles, Biochim. Biophys. Acta 1767 (2007) 136-142. (Pubitemid 46282604)
68. K. Gottlob, N. Majewski, S. Kennedy, E. Kandel, R.B. Robey, N. Hay, Inhibition of early apoptotic events by Akt/PKB is dependent on the first committed step of glycolysis and mitochondrial hexokinase, Genes Dev. 15 (2001) 1406-1418. (Pubitemid 32524647)
69. M.G. Vander Heiden, N.S. Chandel, X.X. Li, P.T. Schumacker, M. Colombini, C.B. Thompson, Outer mitochondrial membrane permeability can regulate coupled respiration and cell survival, Proc. Natl. Acad. Sci. U. S. A. 97 (2000) 4666-4671. (Pubitemid 30238615)
70. N. Majewski, V. Nogueira, R.B. Robey, N. Hay, Akt inhibits apoptosis downstream of BID cleavage via a glucose-dependent mechanism involving mitochondrial hexokinases, Mol. Cell. Biol. 24 (2004) 730-740. (Pubitemid 38057924)
71. N. Majewski, V. Nogueira, P. Bhaskar, P.E. Coy, J.E. Skeen, K. Gottlob, N.S. Chandel, C.B. Thompson, R.B. Robey, N. Hay, Hexokinase-mitochondria interaction mediated by Akt is required to inhibit apoptosis in the presence or absence of Bax and Bak, Mol. Cell 16 (2004) 819-830. (Pubitemid 39586539)
72. J.G. Pastorino, J.B. Hoek, Hexokinase II: the integration of energy metabolism and control of apoptosis, Curr. Med. Chem. 10 (2003) 1535-1551. (Pubitemid 36896555)
73. Q. Wang, R. Somwar, P.J. Bilan, Z. Liu, J. Jin, J.R. Woodgett, A. Klip, Protein kinase B/Akt participates in GLUT4 translocation by insulin in L6 myoblasts, Mol. Cell. Biol. 19 (1999) 4008-4018. (Pubitemid 29241975)
74. H. Zaid, C.N. Antonescu, V.K. Randhawa, A. Klip, Insulin action on glucose transporters through molecular switches, tracks and tethers, Biochem. J. 413 (2008) 201-215.
75. T. Yoshizaki, T. Imamura, J.L. Babendure, J.C. Lu, N. Sonoda, J.M. Olefsky, Myosin 5a is an insulin-stimulated Akt2 (protein kinase Bbeta) substrate modulating GLUT4 vesicle translocation, Mol. Cell. Biol. 27 (2007) 5172-5183. (Pubitemid 47068291)
76. V. Shoshan-Barmatz, D. Ben-Hail, VDAC, amulti-functionalmitochondrial protein as a pharmacological target, Mitochondrion (2011) [Electronic publication ahead of print].
77. K.W. Kinnally, P.M. Peixoto, S.Y. Ryu, L.M. Dejean, Is mPTP the gatekeeper for necrosis, apoptosis, or both? Biochim. Biophys. Acta 1813 (2011) 616-622.
78. E.H. Cheng, T.V. Sheiko, J.K. Fisher, W.J. Craigen, S.J. Korsmeyer, VDAC2 inhibits BAK activation and mitochondrial apoptosis, Science 301 (2003) 513-517. (Pubitemid 36900308)
79. A.J. Bauer, S. Gieschler, K.M. Lemberg, A.E. McDermott, B.R. Stockwell, Functional model of metabolite gating by human voltage-dependent anion channel 2, Biochemistry 50 (2011) 3408-3410.
80. A.G. Komarov, D. Deng, W.J. Craigen, M. Colombini, New insights into the mechanism of permeation through large channels, Biophys. J. 89 (2005) 3950-3959. (Pubitemid 41725616)
81. S.S. Roy, A.M. Ehrlich, W.J. Craigen, G. Hajnoczky, VDAC2 is required for truncated BID-induced mitochondrial apoptosis by recruiting BAK to the mitochondria, EMBO Rep. 10 (2009) 1341-1347.
82. M. Lazarou, D. Stojanovski, A.E. Frazier, A. Kotevski, G. Dewson, W.J. Craigen, R.M. Kluck, D.L. Vaux, M.T. Ryan, Inhibition of Bak activation by VDAC2 is dependent on the Bak transmembrane anchor, J. Biol. Chem. 285 (2010) 36876-36883.
83. D. Ren, H. Kim, H.C. Tu, T.D. Westergard, J.K. Fisher, J.A. Rubens, S.J. Korsmeyer, J.J. Hsieh, E.H. Cheng, The VDAC2-BAK rheostat controls thymocyte survival, Sci. Signal. 2 (2009) ra48.
84. A. Israelson, N. Arbel, S. Da Cruz, H. Ilieva, K. Yamanaka, V. Shoshan-Barmatz, D.W. Cleveland, Misfolded mutant SOD1 directly inhibits VDAC1 conductance in a mouse model of inherited ALS, Neuron 67 (2010) 575-587.
85. D.W. Cleveland, J.D. Rothstein, From Charcot to Lou Gehrig: deciphering selective motor neuron death in ALS, Nat. Rev. Neurosci. 2 (2001) 806-819. (Pubitemid 33674062)
86. P.C. Wong, C.A. Pardo, D.R. Borchelt, M.K. Lee, N.G. Copeland, N.A. Jenkins, S.S. Sisodia, D.W. Cleveland, D.L. Price, An adverse property of a familial ALS-linked SOD1 mutation causes motor neuron disease characterized by vacuolar degeneration of mitochondria, Neuron 14 (1995) 1105-1116.
87. S.F. Okada, W.K. O'Neal, P. Huang, R.A. Nicholas, L.E. Ostrowski, W.J. Craigen, E.R. Lazarowski, R.C. Boucher, Voltage-dependent anion channel-1 (VDAC-1) contributes to ATP release and cell volume regulation in murine cells, J. Gen. Physiol. 124 (2004) 513-526. (Pubitemid 39506287)