VDAC structure, selectivity, and dynamics

Biochimica et Biophysica Acta - Biomembranes

Volumn 1818, Issue 6, 2012, Pages 1457-1465

  Colombini, Marco ^a  

^a Bldg 142   (United States)

Author keywords

Channel; Mitochondrion; Outer membrane; Permeability; Selectivity; Voltage gating

Indexed keywords

ADENOSINE TRIPHOSPHATE; VOLTAGE DEPENDENT ANION CHANNEL;

ALPHA HELIX; AMINO ACID SEQUENCE; BIOTINYLATION; CELL METABOLISM; CHANNEL GATING; ELECTRON MICROSCOPY; HYDROGEN BOND; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL PERMEABILITY; OUTER MEMBRANE; POINT MUTATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN STRUCTURE; QUANTITATIVE ANALYSIS; REVIEW; STATIC ELECTRICITY; TEMPERATURE DEPENDENCE;

AMINO ACID SEQUENCE; ANIMALS; HUMANS; ION CHANNEL GATING; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; THERMODYNAMICS; VOLTAGE-DEPENDENT ANION CHANNELS;

EUKARYOTA;

EID: 84859780328     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2011.12.026     Document Type: Review

References (74)

1. M. Colombini, Candidate for the permeability pathway of the outer mitochondrial-membrane, Nature 279 (1979) 643-645. (Pubitemid 9198862)
2. S.J. Schein, M. Colombini, A. Finkelstein, Reconstitution in planar lipid bilayers of a voltage-dependent anion-selective channel obtained from Paramecium mitochondria, J. Membr. Biol. 30 (1976) 99-120. (Pubitemid 8010351)
3. M. Colombini, Voltage gating in the mitochondrial channel, VDAC, J. Membr. Biol. 111 (1989) 103-111. (Pubitemid 19272950)
4. K. Mihara, R. Sato, Molecular-cloning and sequencing of cDNA for yeast porin, an outer mitochondrial-membrane protein - a search for targeting signal in the primary structure, EMBO J. 4 (1985) 769-774.
5. H. Kayser, H.D. Kratzin, F.P. Thinnes, H. Gotz, W.E. Schmidt, K. Eckart, N. Hilschmann, To the knowledge of human porins. 2. Characterization and primary structure of a 31-kDa porin from human b-lymphocytes (porin 31 HL), Biol. Chem. Hoppe Seyler 370 (1989) 1265-1278. (Pubitemid 20063280)
6. R. Kleene, N. Pfanner, R. Pfaller, T.A. Link, W. Sebald, W. Neupert, M. Tropschug, Mitochondrial porin of Neurospora-crassa - cDNA cloning, in vitro expression and import into mitochondria, EMBO J. 6 (1987) 2627-2633.
7. M. Colombini, Anion channels in the mitochondrial outer-membrane, Current Topics in Membranes, in: W.B. Guggino (Ed.), Chloride Channels, 42, Academic Press, New York, 1994, pp. 73-101.
8. T. Rostovtseva, M. Colombini, ATP flux is controlled by a voltage-gated channel from the mitochondrial outer membrane, J. Biol. Chem. 271 (1996) 28006-28008. (Pubitemid 26374603)
9. R.Z. Sabirov, T. Sheiko, H.T. Liu, D.F. Deng, Y. Okada, W.J. Craigen, Genetic demonstration that the plasma membrane maxianion channel and voltage-dependent anion channels are unrelated proteins, J. Biol. Chem. 281 (2006) 1897-1904. (Pubitemid 43845774)
10. M. Colombini, Pore-size and properties of channels from mitochondria isolated from Neurospora-crassa, J. Membr. Biol. 53 (1980) 79-84. (Pubitemid 10033412)
11. J.M. Song, M. Colombini, Indications of a common folding pattern for VDAC channels from all sources, J. Bioenerg. Biomembr. 28 (1996) 153-161. (Pubitemid 26131529)
12. E.H.Y. 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)
13. 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.
14. M. Forte, H.R. Guy, C.A. Mannella, Molecular-genetics of the VDAC ion channel -structural model and sequence-analysis, J. Bioenerg. Biomembr. 19 (1987) 341-350.
15. C.A. Mannella, A.F. Neuwald, C.E. Lawrence, Detection of likely transmembrane beta-strand regions in sequences of mitochondrial pore proteins using the Gibbs sampler, J. Bioenerg. Biomembr. 28 (1996) 163-169. (Pubitemid 26131530)
16. V. Depinto, F. Palmieri, Transmembrane arrangement of mitochondrial porin or voltage-dependent anion channel (VDAC), J. Bioenerg. Biomembr. 24 (1992) 21-26.
17. R. Casadio, I. Jacoboni, A. Messina, V. De Pinto, A 3D model of the voltagedependent anion channel (VDAC), FEBS Lett. 520 (2002) 1-7. (Pubitemid 34607263)
18. D.C. Bay, D.A. Court, Origami in the outer membrane: the transmembrane arrangement of mitochondrial porins, Biochem. Cell Biol. 80 (2002) 551-562. (Pubitemid 36124816)
19. L. Shao, K.W. Kinnally, C.A. Mannella, Circular dichroism studies of the mitochondrial channel, VDAC, from Neurospora crassa, Biophys. J. 71 (1996) 778-786. (Pubitemid 26289161)
20. H. Abrecht, E. Goormaghtigh, J.M. Ruysschaert, F. Homble, Structure and orientation of two voltage-dependent anion-selective channel isoforms - an attenuated total reflection Fourier-transform infrared spectroscopy study, J. Biol. Chem. 275 (2000) 40992-40999. (Pubitemid 32054925)
21. L.S. Zalman, H. Nikaido, Y. Kagawa, Mitochondrial outer-membrane contains a protein producing nonspecific diffusion channels, J. Biol. Chem. 255 (1980) 1771-1774.
22. I. Vodyanoy, S.M. Bezrukov, M. Colombini, Measurement of ion channel access resistance, FASEB J. 6 (1992) A114-A114.
23. C.A. Mannella, A. Ribeiro, J. Frank, Structure of the channels in the outer mitochondrial-membrane - electron-microscopic studies of the periodic arrays induced by phospholipase-a2 treatment of the Neurospora membrane, Biophys. J. 49 (1986) 307-318. (Pubitemid 16155469)
24. C.A. Mannella, X.W. Guo, B. Cognon, Diameter of the mitochondrial outermembrane channel - evidence from electron-microscopy of frozen-hydrated membrane crystals, FEBS Lett. 253 (1989) 231-234. (Pubitemid 19212569)
25. C.A. Mannella, X.W. Guo, Interaction between the VDAC channel and a polyanionic effector - an electron-microscopic study, Biophys. J. 57 (1990) 23-31. (Pubitemid 20033743)
26. L. Thomas, E. Kocsis, M. Colombini, E. Erbe, B.L. Trus, A.C. Steven, Surface-topography and molecular stoichiometry of the mitochondrial channel, VDAC, in crystalline arrays, J. Struct. Biol. 106 (1991) 161-171.
27. C.A. Mannella, M. Forte, M. Colombini, Toward the molecular-structure of the mitochondrial channel, VDAC, J. Bioenerg. Biomembr. 24 (1992) 7-19.
28. E. Blachlydyson, S.Z. Peng, M. Colombini, M. Forte, Selectivity changes in sitedirected mutants of the VDAC ion channel - structural implications, Science 247 (1990) 1233-1236.
29. S. Peng, E. Blachlydyson, M. Forte, M. Colombini, Large-scale rearrangement of protein domains is associated with voltage gating of the VDAC channel, Biophys. J. 62 (1992) 123-135.
30. J.M. Song, C. Midson, E. Blachly-Dyson, M. Forte, M. Colombini, The sensor regions of VDAC are translocated from within the membrane to the surface during the gating processes, Biophys. J. 74 (1998) 2926-2944. (Pubitemid 28268117)
31. S. Stanley, J.A. Dias, D. D'Arcangelis, C.A. Mannella, Peptide-specific antibodies as probes of the topography of the voltage-gated channel in the mitochondrial outer membrane of Neurospora crassa, J. Biol. Chem. 270 (1995) 16694-16700.
32. V. Depinto, G. Prezioso, F. Thinnes, T.A. Link, F. Palmieri, Peptide-specific antibodies and proteases as probes of the transmembrane topology of the bovine heart mitochondrial porin, Biochemistry 30 (1991) 10191-10200.
33. S. Hiller, R.G. Garces, T.J. Malia, V.Y. Orekhov, M. Colombini, G. Wagner, Solution structure of the integral human membrane protein VDAC-1 in detergent micelles, Science 321 (2008) 1206-1210.
34. R. Ujwal, D. Cascio, J.P. Colletier, S. Faham, J. Zhang, L. Toro, P.P. Ping, J. Abramson, The crystal structure of mouse VDAC1 at 2.3 Angstrom resolution reveals mechanistic insights into metabolite gating, Proc. Natl. Acad. Sci. U. S. A. 105 (2008) 17742-17747.
35. M. Bayrhuber, T. Meins, M. Habeck, S. Becker, K. Giller, S. Villinger, C. Vonrhein, C. Griesinger, M. Zweckstetter, K. Zeth, Structure of the human voltage-dependent anion channel, Proc. Natl. Acad. Sci. U. S. A. 105 (2008) 15370-15375.
36. M. Colombini, The published 3D structure of the VDAC channel: native or not? Trends Biochem. Sci. 34 (2009) 382-389.
37. C.A. Mannella, Electron-microscopy and image-analysis of the mitochondrial outer-membrane channel, VDAC, J. Bioenerg. Biomembr. 19 (1987) 329-340.
38. S.Z. Peng, E. Blachlydyson, M. Colombini, M. Forte, Determination of the number of polypeptide subunits in a functional VDAC channel from Saccharomyces-cerevisiae, J. Bioenerg. Biomembr. 24 (1992) 27-31.
39. J.M. Song, C. Midson, E. Blachly-Dyson, M. Forte, M. Colombini, The topology of VDAC as probed by biotin modification, J. Biol. Chem. 273 (1998) 24406-24413. (Pubitemid 28454931)
40. E. Blachlydyson, S.Z. Peng, M. Colombini, M. Forte, Probing the structure of the mitochondrial channel, VDAC, by site-directed mutagenesis - a progress report, J. Bioenerg. Biomembr. 21 (1989) 471-483. (Pubitemid 19257189)
41. G. Runke, E. Maier, W.A.T. Summers, D.C. Bay, R. Benz, D.A. Court, Deletion variants of Neurospora mitochondrial porin: electrophysiological and spectroscopic analysis, Biophys. J. 90 (2006) 3155-3164.
42. L. Thomas, E. Blachlydyson, 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)
43. C.A. Mannella, Structural-analysis of mitochondrial pores, Experientia 46 (1990) 137-145.
44. D.A. Koppel, K.W. Kinnally, P. Masters, M. Forte, E. Blachly-Dyson, 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. (Pubitemid 28268429)
45. M. Colombini, E. Balchly-Dyson, M. Forte, VDAC, a channel in the outer mitochondrial membrane, in: T. Narahashi (Ed.), Ion Channels, Vol. 4, Plenum Press, New York, 1996, pp. 169-202.
46. B. Popp, D.A. Court, R. Benz, W. Neupert, R. Lill, The role of the N and C termini of recombinant Neurospora mitochondrial porin in channel formation and voltagedependent gating, J. Biol. Chem. 271 (1996) 13593-13599. (Pubitemid 26185406)
47. S. Hiller, J. Abramson, C. Mannella, G. Wagner, K. Zeth, The 3D structures of VDAC represent a native conformation, Trends Biochem. Sci. 35 (2010) 514-521.
48. V. Depinto, J.A. Aljamal, F. Palmieri, Location of the dicyclohexylcarbodiimidereactive glutamate residue in the bovine heart mitochondrial porin, J. Biol. Chem. 268 (1993) 12977-12982. (Pubitemid 23182473)
49. M. Colombini, C.L. Yeung, J. Tung, T. Konig, The mitochondrial outer-membrane channel, VDAC, is regulated by a synthetic polyanion, Biochim. Biophys. Acta 905 (1987) 279-286. (Pubitemid 18004526)
50. T.K. Rostovtseva, A. Komarov, S.M. Bezrukov, M. Colombini, VDAC channels differentiate between natural metabolites and synthetic molecules, J. Membr. Biol. 187 (2002) 147-156. (Pubitemid 34526479)
51. T.K. Rostovtseva, N. Kazemi, M. Weinrich, S.M. Bezrukov, Voltage gating of VDAC is regulated by nonlamellar lipids of mitochondrial membranes, J. Biol. Chem. 281 (2006) 37496-37506. (Pubitemid 46042053)
52. T. Hodge, M. Colombini, Regulation of metabolite flux through voltage-gating of VDAC channels, J. Membr. Biol. 157 (1997) 271-279. (Pubitemid 27276169)
53. E.B. Zambrowicz, M. Colombini, Zero-current potentials in a large membrane channel - a simple theory accounts for complex behavior, Biophys. J. 65 (1993) 1093-1100. (Pubitemid 23263925)
54. R. Benz, M. Kottke, 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. (Pubitemid 20079112)
55. M. Colombini, Structure and mode of action of a voltage-dependent anionselective channel (VDAC) located in the outer mitochondrial membrane, Ann. N. Y. Acad. Sci. 341 (1980) 552-563.
56. T. Rostovtseva, M. Colombini, VDAC channels mediate and gate the flow of ATP: implications for the regulation of mitochondrial function, Biophys. J. 72 (1997) 1954-1962. (Pubitemid 27184425)
57. A.G. Komarov, D.F. Deng, W.J. Craigen, M. Colombini, New insights into the mechanism of permeation through large channels, Biophys. J. 89 (2005) 3950-3959. (Pubitemid 41725616)
58. M. Zizi, M. Forte, E. Blachlydyson,M. Colombini, NADH regulates the gating of VDAC, the mitochondrial outer-membrane channel, J. Biol. Chem. 269 (1994) 1614-1616. (Pubitemid 24035349)
59. W.Z. Tan, M. Colombini, VDAC closure increases calcium ion flux, Biochim. Biophys. Acta 1768 (2007) 2510-2515. (Pubitemid 47532032)
60. D.W. Zhang, M. Colombini, Group-IIIA-metal hydroxides indirectly neutralize the voltage sensor of the voltage-dependent mitochondrial channel, VDAC, by interacting with a dynamic binding-site, Biochim. Biophys. Acta 1025 (1990) 127-134. (Pubitemid 20199619)
61. M.J. Holden, M. Colombini, The mitochondrial outer-membrane channel, VDAC, is modulated by a soluble-protein, FEBS Lett. 241 (1988) 105-109.
62. M. Colombini, Voltage gating in VDAC: toward a molecular mechanism, in: C. Miller (Ed.), Ion Channel Reconstitution, Plenum Publishing, New York, 1986, pp. 533-552.
63. E.T. Dill, Probing the nature of the voltage-sensing mechanism of the mitochondrial outer membrane channel, VDAC: initial kinetic analysis and aluminum chloride-induced alterations, Doctoral Thesis, Dept. Zoology, University of Maryland, College Park, Maryland, 1987. http://hdl.handle.net/ 1903/12145
64. J. Zimmerberg, V.A. Parsegian, Polymer inaccessible volume changes during opening and closing of a voltage-dependent ionic channel, Nature 323 (1986) 36-39.
65. P.S. Mangan, M. Colombini, Ultrasteep voltage dependence in amembrane channel, Proc. Natl. Acad. Sci. U. S. A. 84 (1987) 4896-4900.
66. M. Colombini, M.J. Holden, P.S. Mangan, Modulation of the mitochondrial channel VDAC by a variety of agents, in: A. Azzi, K.A. Nalecz, M.J. Nalecz, L. Wojtczak (Eds.), Anion Carriers of Mitochondrial Membranes, Springer-Verlag, Berlin, 1989, pp. 215-224.
67. M. Zizi, L. Thomas, E. Blachlydyson, M. Forte, M. Colombini, Oriented channel insertion reveals the motion of a transmembrane beta-strand during voltage gating of VDAC, J. Membr. Biol. 144 (1995) 121-129.
68. X.F. Xu, M. Colombini, Self-catalyzed insertion of proteins into phospholipid membranes, J. Biol. Chem. 271 (1996) 23675-23682. (Pubitemid 26327332)
69. X.F. Xu, M. Colombini, Autodirected insertion: preinserted VDAC channels greatly shorten the delay to the insertion of new channels, Biophys. J. 72 (1997) 2129-2136. (Pubitemid 27184439)
70. M.Y. Liu, M. Colombini, Voltage gating of the mitochondrial outer-membrane channel VDAC is regulated by a very conserved protein, Am. J. Physiol. 260 (1991) C371-C374.
71. M.Y. Liu, M. Colombini, A soluble mitochondrial protein increases the voltage dependence of the mitochondrial channel, VDAC, J. Bioenerg. Biomembr. 24 (1992) 41-46.
72. M.Y. Liu, M. Colombini, Regulation of mitochondrial respiration by controlling the permeability of the outer-membrane through the mitochondrial channel, VDAC, Biochim. Biophys. Acta 1098 (1992) 255-260.
73. M.Y. Liu, A. Torgrimson, M. Colombini, Characterization and partial-purification of the VDAC-channel-modulating protein from calf liver-mitochondria, Biochim. Biophys. Acta 1185 (1994) 203-212. (Pubitemid 24130888)
74. M. Zizi, C. Byrd, R. Boxus, M. Colombini, The voltage-gating process of the voltage-dependent anion channel is sensitive to ion flow, Biophys. J. 75 (1998) 704-713. (Pubitemid 28357512)