Deletion of β-strands 9 and 10 converts VDAC1 voltage-dependence in an asymmetrical process

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1827, Issue 6, 2013, Pages 793-805

  Reina, Simona ^a,b   Magrì, Andrea ^a,b   Lolicato, Marco ^c   Guarino, Francesca ^a,b   Impellizzeri, Agata ^a,b   Maier, Elke ^d   Benz, Roland ^d,e   Ceccarelli, Matteo ^f   De Pinto, Vito ^a,b   Messina, Angela ^a,b  

^a UNIVERSITY OF CATANIA   (Italy)

^b National Institute of Biomembranes and Biosystems (INBB)   (Italy)

^c UNIVERSITY OF MILAN   (Italy)

^d UNIVERSITY OF WÜRZBURG   (Germany)

^e JACOBS UNIVERSITY BREMEN   (Germany)

^f UNIVERSITY OF CAGLIARI   (Italy)

Author keywords

Molecular dynamics simulation; Mutant protein; Voltage dependent anion channel; Voltage gating process

Indexed keywords

CHIMERIC PROTEIN; VOLTAGE DEPENDENT ANION CHANNEL 1;

APOPTOSIS; ARTICLE; BILAYER MEMBRANE; BIOENERGY; CELL METABOLISM; ELECTRIC POTENTIAL; ELECTROPHYSIOLOGY; MEMBRANE CURRENT; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL PERMEABILITY; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN PURIFICATION; PROTEIN REFOLDING; PROTEIN STRUCTURE; SACCHAROMYCES CEREVISIAE; YEAST;

AMINO ACID SEQUENCE; MEMBRANE POTENTIALS; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; PROTEIN STRUCTURE, SECONDARY; RECOMBINANT FUSION PROTEINS; SEQUENCE ALIGNMENT; VOLTAGE-DEPENDENT ANION CHANNEL 1;

EID: 84876933211     PISSN: 00052728     EISSN: 18792650     Source Type: Journal    
DOI: 10.1016/j.bbabio.2013.03.007     Document Type: Article

References (65)

1. 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
2. R. Benz Permeation of hydrophilic solutes through mitochondrial outer membranes: review on mitochondrial porins Biochim. Biophys. Acta 1197 1994 167 196
3. M. Colombini VDAC: the channel at the interface between mitochondria and the cytosol Mol. Cell. Biochem. 256-257 2004 107 115
4. 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
5. G. Kroemer, L. Galluzzi, and C. Brenner Mitochondrial membrane permeabilization in cell death Physiol. Rev. 87 2007 99 163
6. 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
7. T.K. Rostovtseva, B. Antonsson, M. Suzuki, R.J. Youle, M. Colombini, and S.M. Bezrukov Bid, but not Bax, regulates VDAC channels J. Biol. Chem. 279 2004 13575 13583
8. F. Tomasello, A. Messina, L. Lartigue, L. Schembri, C. Medina, S. Reina, D. Thoraval, M. Crouzet, F. Ichas, V. De Pinto, and F. De Giorgi Outer membrane VDAC1 controls permeability transition of the inner mitochondrial membrane in cellulo during stress-induced apoptosis Cell Res. 19 2009 1363 1376
9. 2 +-dependent control of the permeability properties of the mitochondrial outer membrane and voltage-dependent anion-selective channel (VDAC) J. Biol. Chem. 281 2006 17347 17358
10. D. De Stefani, A. Bononi, A. Romagnoli, A. Messina, V. De Pinto, P. Pinton, and R. Rizzuto VDAC1 selectively transfers apoptotic Ca(2 +) signals to mitochondria Cell Death Differ. 19 2012 267 273
11. E.N. Maldonado, and J.J. Lemasters Warburg revisited: regulation of mitochondrial metabolism by voltage-dependent anion channels in cancer cells J. Pharmacol. Exp. Ther. 342 2012 637 641
12. N. Arbel, D. Ben-Hail, and V. Shoshan-Barmatz Mediation of the antiapoptotic activity of Bcl-xL protein upon interaction with VDAC1 protein J. Biol. Chem. 287 2012 23152 23161
13. 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
14. P.L. Pedersen 3-Bromopyruvate (3BP) a fast acting, promising, powerful, specific, and effective "small molecule" anti-cancer agent taken from labside to bedside: introduction to a special issue J. Bioenerg. Biomembr. 44 2012 1 6
15. K.S. McCommis, and C.P. Baines The role of VDAC in cell death: friend or foe? Biochim. Biophys. Acta 1818 2012 1444 1450
16. M. Huizing, W. Ruitenbeek, F. Thinnes, and V. De Pinto Deficiency of the Voltage-Dependent Anion Channel (VDAC): a novel cause of mitochondrial myopathies Lancet 344 1994 762
17. M.J. Young, D.C. Bay, G. Hausner, and D.A. Court The evolutionary history of mitochondrial porins BMC Evol. Biol. 7 2007 31
18. M. Oliva, A. Messina, G. Ragone, C. Caggese, R. Caizzi, and V. De Pinto Sequence of the Drosophila melanogaster mitochondrial porin gene: evidence of a conserved protein domain between fly and mouse FEBS Lett. 430 1998 327 332
19. A. Messina, S. Reina, F. Guarino, and V. De Pinto VDAC isoforms in mammals Biochim. Biophys. Acta 181 2012 1466 1476
20. V. De Pinto, F. Guarino, A. Guarnera, A. Messina, S. Reina, F.M. Tomasello, V. Palermo, and C. Mazzoni Characterization of human VDAC isoforms: a peculiar function for VDAC3? Biochim. Biophys. Acta 1797 2010 1268 1275
21. S. Reina, V. Palermo, A. Guarnera, F. Guarino, A. Messina, C. Mazzoni, and V. De Pinto Swapping of the N-terminus of VDAC1 with VDAC3 restores full activity of the channel and confers anti-aging features to the cell FEBS Lett. 584 2010 2837 2844
22. M. Colombini Voltage gating in the mitochondrial channel VDAC J. Membr. Biol. 111 1989 103 111
23. J. Song, C. Midson, E. Blachly-Dyson, M. Forte, and M. Colombini The topology of VDAC as probed by biotin modification J. Biol. Chem. 273 1998 24406 24413
24. J. Song, C. Midson, E. Blachly-Dyson, M. Forte, and 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
25. 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
26. 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
27. M. Bayrhuber, T. Meins, M. Habeck, S. Becker, K. Giller, S. Villinger, C. Vonrhein, C. Griesinger, M. Zweckstetter, and K. Zeth Structure of the human voltage-dependent anion channel Proc. Natl. Acad. Sci. U. S. A. 105 2008 15370 15375
28. R. Ujwal, D. Cascio, J.P. Colletier, S. Faham, J. Zhang, L. Toro, P. Ping, and 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
29. M. Colombini The published 3D structure of the VDAC channel: native or not? Trends Biochem. Sci. 34 2009 382 389
30. S. Hiller, J. Abramson, C. Mannella, G. Wagner, and K. Zeth The 3D structures of VDAC represent a native conformation Trends Biochem. Sci. 35 2010 514 521
31. V. De Pinto, F. Tomasello, A. Messina, F. Guarino, R. Benz, D. La Mendola, A. Magrì, D. Milardi, and G. Pappalardo 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
32. R. Schneider, M. Etzkorn, K. Giller, V. Daebel, J. Eisfeld, M. Zweckstetter, C. Griesinger, S. Becker, and A. Lange The native conformation of the human VDAC1 N terminus Angew. Chem. Int. Ed Engl. 49 2010 1882 1885
33. S. Villinger, R. Briones, K. Giller, U. Zachariae, A. Lange, B.L. de Groot, C. Griesinger, S. Becker, and M. Zweckstetter Functional dynamics in the voltage-dependent anion channel Proc. Natl. Acad. Sci. U. S. A. 107 2010 22546 22551
34. U. Zachariae, R. Schneider, R. Briones, Z. Gattin, J.P. Demers, K. Giller, E. Maier, M. Zweckstetter, C. Griesinger, S. Becker, R. Benz, B.L. de Groot, and A. Lange β-Barrel mobility underlies closure of the voltage-dependent anion channel Structure 20 2012 1540 1549
35. G.A. Reid Effects of nitrogen supplements on degradation of aspen wood lignin and carbohydrate components by Phanerochaete chrysosporium Methods Enzymol. 97 1983 324 329
36. M. Suissa, K. Suda, and G. Schatz Isolation of the nuclear yeast genes for citrate synthase and fifteen other mitochondrial proteins by a new screening method EMBO J. 3 1984 1773 1781
37. C. Gregg, P. Kyryakov, and V.I. Titorenko Purification of mitochondria from yeast cells J. Vis. Exp. 30 2009 e1417
38. V. De Pinto, R. Benz, and F. Palmieri Interaction of non-classical detergents with the mitochondrial porin: a new purification procedure and characterization of the pore-forming unit Eur. J. Biochem. 183 1989 179 187
39. S.N. Ho, H.D. Hunt, R.M. Horton, J.K. Pullen, and L.R. Pease Site-directed mutagenesis by overlap extension using the polymerase chain reaction Gene 77 1989 51 59
40. R.M. Horton, H.D. Hunt, S.N. Ho, J.K. Pullen, and L.R. Pease Engineering hybrid genes without the use of restriction enzymes: gene splicing by overlap extension Gene 77 1989 61 68
41. Y. Shi, C. Jiang, Q. Chen, and H. Tang One-step on-column affinity refolding purification and functional analysis of recombinant human VDAC1 Biochem. Biophys. Res. Commun. 303 2003 475 482
42. R. Benz, K. Janko, W. Boos, and P. Läuger Formation of large, ion-permeable membrane channels by the matrix protein (porin) of Escherichia coli Biochim. Biophys. Acta 511 1978 305 319
43. R. Benz, A. Schmid, and R.E. Hancock Ion selectivity of gram-negative bacterial porins J. Bacteriol. 162 1985 722 727
44. K. Lindorff-Larsen, S. Piana, K. Palmo, P. Maragakis, and J.L. Klepeis Improved side-chain torsion potentials for the Amber ff99SB protein force field Proteins 78 2010 1950 1958
45. B. Jojart, and T.A. Martinek Performance of the general amber force field in modeling aqueous POPC membrane bilayers J. Comput. Chem. 28 2007 2051 2058
46. A. Fiser, and A. Sali Modeller: generation and refinement of homology-based protein structure models Methods Enzymol. 374 2003 461 491
47. M.J. Harvey, G. Giupponi, and G. De Fabritiis ACEMD: accelerating biomolecular dynamics in the microsecond time scale J. Chem. Theory Comput. 5 2009 1632 1639
48. A. Kumar, E. Hajjar, P. Ruggerone, and M. Ceccarelli Molecular simulations reveal the mechanism and the determinants for ampicillin translocation through OmpF J. Phys. Chem. 114 2010 9608 9616
49. 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
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. G. Runke, E. Maier, W.A. Summers, D.C. Bay, R. Benz, and D.A. Court Deletion variants of Neurospora mitochondrial porin: electrophysiological and spectroscopic analysis Biophys. J. 90 2006 3155 3164
52. S. Abu-Hamad, N. Arbel, D. Calo, L. Arzoine, A. Israelson, N. Keinan, R. Ben-Romano, O. Friedman, and V. Shoshan-Barmatz The VDAC1 N-terminus is essential both for apoptosis and the protective effect of anti-apoptotic proteins J. Cell Sci. 122 2009 1906 1916
53. E.M. Krammer, F. Homblé, and M. Prévost Concentration dependent ion selectivity in VDAC: a molecular dynamics simulation study PLoS One 6 2011 e27994
54. 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
55. B. Mertins, G. Psakis, W. Grosse, K.C. Back, and A. Salisowski Flexibility of the N-terminal mVDAC1 segment controls the channel's gating behavior PLoS One 7 2012 e47938
56. O. Teijido, R. Ujwal, C.O. Hillerdal, L. Kullman, T.K. Rostovtseva, and J. Abramson Affixing the N-terminal alpha helix of the voltage dependent anion channel to the channel's wall does not prevent its voltage gating J. Biol. Chem. 287 2012 11437 11445
57. 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. U. S. A. 90 1993 5446 5449
58. 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
59. R. Benz, L. Wojtczak, W. Bosch, and D. Brdiczka Inhibition of adenine nucleotide transport through the mitochondrial porin by a synthetic polyanion FEBS Lett. 231 1988 75 80
60. M. Colombini, C.L. Yeung, J. Tung, and T. König The mitochondrial outer membrane channel, VDAC, is regulated by a synthetic polyanion Biochim. Biophys. Acta 905 1987 279 286
61. G. Bàthori, I. Szabo, I. Schmehl, F. Tombola, A. Messina, V. De Pinto, and M. Zoratti Novel aspects of the electrophysiology of mitochondrial porin Biochem. Biophys. Res. Commun. 243 1998 258 263
62. K.A. Bowen, K. Tam, and M. Colombini Evidence for titratable gating charges controlling the voltage dependence of the outer mitochondrial membrane channel, VDAC J. Membr. Biol. 86 1985 51 59
63. V. De Pinto, J.A. Al Jamal, R. Benz, and F. Palmieri Positive residues involved in the voltage-gating of the mitochondrial porin-channel are localized in the external moiety of the pore FEBS Lett. 274 1990 122 126
64. C. Doring, and M. Colombini The mitochondrial voltage-dependent channel, VDAC, is modified asymmetrically by succinic anhydride J. Membr. Biol. 83 1985 87 94
65. V. De Pinto, S. Reina, F. Guarino, and A. Messina The structure of voltage-dependent anion selective channel: state of the art J. Bioenerg. Biomembr. 40 2008 139 147