Charged residues distribution modulates selectivity of the open state of human isoforms of the voltage dependent anion-selective channel

PLoS ONE

Volumn 9, Issue 8, 2014, Pages

  Amodeo, Giuseppe Federico ^a   Scorciapino, Mariano Andrea ^a,b   Messina, Angela ^c,d   De Pinto, Vito ^c,d   Ceccarelli, Matteo ^a,b  

^a UNIVERSITY OF CAGLIARI   (Italy)

^b IOM CNR LABORATORIO TASC   (Italy)

^c UNIVERSITY OF CATANIA   (Italy)

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

Author keywords

[No Author keywords available]

Indexed keywords

VOLTAGE DEPENDENT ANION CHANNEL 1; VOLTAGE DEPENDENT ANION CHANNEL 2; VOLTAGE DEPENDENT ANION CHANNEL 3; CARRIER PROTEIN; ISOPROTEIN; VDAC1 PROTEIN, HUMAN; VDAC3 PROTEIN, HUMAN; VOLTAGE DEPENDENT ANION CHANNEL;

AMINO TERMINAL SEQUENCE; ARTICLE; CHANNEL GATING; CONTROLLED STUDY; ENZYME MECHANISM; HUMAN; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; PROTEIN CONFORMATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN SECONDARY STRUCTURE; RESIDUE ANALYSIS; SIMULATION; AMINO ACID SEQUENCE; CHEMISTRY; GENETICS; METABOLISM; MOLECULAR GENETICS; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; HUMANS; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; PROTEIN ISOFORMS; SEQUENCE HOMOLOGY, AMINO ACID; VOLTAGE-DEPENDENT ANION CHANNEL 1; VOLTAGE-DEPENDENT ANION CHANNELS;

EID: 84905400486     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0103879     Document Type: Article

References (68)

1. Benz R (1994) Permeation of hydrophilic solutes through mitochondrial outer membranes: review on mitochondrial porins. Biochim Biophys Acta 1197: 167-196.
2. Colombini M (2004) VDAC: the channel at the interface between mitochondria and the cytosol. Mol Cell Biochem 256-257: 107-115.
3. Shoshan-Barmatz V, De Pinto V, Zweckstetter M, Raviv Z, Keinan N, et al. (2010) VDAC, a multi-functional mitochondrial protein regulating cell life and death. Mol Aspects Med 31: 227-285. doi:10.1016/j.mam.2010.03.002.
4. Rostovtseva T, Colombini M (1997) VDAC channels mediate and gate the flow of ATP: implications for the regulation of mitochondrial function. Biophys J 72: 1954-1962. (Pubitemid 27184425)
5. Messina A, Reina S, Guarino F, De Pinto V (2012) VDAC isoforms in mammals. Biochim Biophys acta - Biomembr 1818: 1466-1476.
6. De Pinto V, Guarino F, Guarnera A, Messina A, Reina S, et al. (2010) Characterization of human VDAC isoforms: a peculiar function for VDAC3? Biochim Biophys acta - Bioenerg 1797: 1268-1275.
7. Bathori G, Szabo I, Schmehl F, Tombola A, Messina A, et al. (1998) Novel aspects of the electrophysiology of mitochondrial porin. Biochem Biophys Res Commun 243: 258-263. (Pubitemid 28414224)
8. Beutner G, Ruck A, Riede B, Brdiczka D (1997) Complexes between hexokinase, mitochondrial porin and adenylate translocator in brain: regulation of hexokinase, oxidative phosphorylation and permeability transition pore. Biochem Soc Trans 25: 151-157. (Pubitemid 27092568)
9. Rostovtseva TK, Bezrukov SM (2012) VDAC inhibition of tubulin and its physiological implications. Biochim Biophys Acta 1818: 1526-1535.
10. 2+ signals to mitochondria. Cell Death Differ 19: 267-273.
11. Cheng EHY, Sheiko TV, Fisher JK, Craigen WJ, Korsmeyer SJ (2003) VDAC2 inhibits BAK activation and mitochondrial apoptosis. Science 301: 513-517. (Pubitemid 36900308)
12. Huizing M, Ruitenbeek W, Thinnes F, De Pinto V (1994) Deficiency of the voltage-dependent anion channel (VDAC): a novel cause of mitochondrial myopathies. Lancet 344: 1206-1210.
13. Tomasello FM, Messina A, Lartigue L, Schembri L, Medina C, et al. (2009) Outer membrane VDAC1 controls permeability transition of the inner mitochondrial membrane in cellulo during stress-induced apoptosis. Cell Res 19: 1363-1376.
14. Rostovtseva TK, Antonsson B, Suzuki M, Youle RJ, Colombini M, et al. (2004) Bid, but not Bax, regulates VDAC channels. J Biol Chem 279: 13575-13583. (Pubitemid 38468883)
15. Shoshan-Barmatz V, Keinan N, Abu-Hamad S, Tyomkin D, Aram L (2010) Apoptosis is regulated by the VDAC1 N-terminal region and by VDAC oligomerization: release of cytochrome c, AIF and Smac/Diablo. Biochim Biophys acta - Bioenerg 1797: 1281-1291.
16. Shoshan-Barmatz V, Golan M (2012) Mitochondrial VDAC1: function in cell life and death and a target for cancer therapy. Curr Med Chem 19: 714-735.
17. Maldonado EN, Lemaster JJ (2012) Warburg revisited: regulation of mitochondrial metabolism by voltage-dependent anion channels in cancer cells. J Pharmacol Exp Ther 342: 637-641.
18. Reddy PH (2013) Is the mitochondrial outermembrane protein VDAC1 therapeutic target for Alzheimer's desease? Biochim Biophys Acta 1832: 67-75.
19. De Pinto V, Reina S, Guarino F, Messina A (2008) Structure of the voltage dependent anion channel: state of the art. J Bioenerg Biomembr 40: 139-147.
20. Bayrhuber M, Meins T, Habeck M, Becker S, Giller K, et al. (2008) Structure of the human voltage-dependent anion channel. Proc Natl Acad Sci U S A 105: 15370-15375.
21. Hiller S, Garces RG, Malia TJ, Orekhov VY, Colombini M, et al. (2008) Solution structure of the integral human membrane protein VDAC-1 in detergent micelles. Science 321: 1206-1210.
22. Ujwal R, Cascio D, Colletier J-P, Faham S, Zhang J, et al. (2008) The crystal structure of mouse VDAC1 at 2.3 A resolution reveals mechanistic insights into metabolite gating. Proc Natl Acad Sci U S A 105: 17742-17747.
23. Schulz GE (2000) Beta-barrel membrane proteins. Curr Opin Struct Biol 10: 443-447.
24. Hiller S, Wagner G (2009) The role of solution NMR in the structure determinations of VDAC-1 and other membrane proteins. Curr Opin Struct Biol 19: 396-401.
25. Colombini M (2009) The published 3D structure of the VDAC channel: native or not? Trends Biochem Sci 34: 382-389.
26. Teijido O, Ujwal R, Hillerdal C-O, Kullman L, Rostovtseva TK, et al. (2012) Affixing N-terminal a-helix to the wall of the voltage-dependent anion channel does not prevent its voltage gating. J Biol Chem 287: 11437-11445.
27. Hiller S, Abramson J, Mannella C, Wagner G, Zeth K (2010) The 3D structures of VDAC represent a native conformation. Trends Biochem Sci 35: 514-521.
28. Zachariae U, Schneider R, Briones R, Gattin Z, Demers J, et al. (2012) b-Barrel Mobility Underlies Closure of the Voltage-Dependent Anion Channel. Structure 20: 1540-1549.
29. Rui H, Lee K Il, Pastor RW, Im W (2011) Molecular dynamics studies of ion permeation in VDAC. Biophys J 100: 602-610.
30. Schredelseker J, Paz A, López CJ, Altenbach C, Leung CS, et al. (2014) High resolution structure and double electron-electron resonance of the zebrafish voltage-dependent anion channel 2 reveal an oligomeric population. J Biol Chem 289: 12566-12577.
31. Lide DR (2007) CRC Handbook of Chemistry and Physics. 87th ed. Boca Raton (FL) - U.S.A.: Taylor and Francis.
32. Tomasello FM, Guarino F, Reina S, Messina A, De Pinto V (2013) The voltage-dependent anion selective channel 1 (VDAC1) topography in the mitochondrion outer membrane as detected in intact cell. PLoS One 8: e81522.
33. Choudhary OP, Ujwal R, Kowallis W, Coalson R, Abramson J, et al. (2010) The electrostatics of VDAC: implications for selectivity and gating. J Mol Biol 396: 580-592.
34. Schneider R, Etzkorn M, Giller K, Daebel V, Eisfeld J, et al. (2010) The native conformation of the human VDAC1 N terminus. Angew Chemie - Int Ed 49: 1882-1885.
35. Song J, Midson C, Blachly-Dyson E, Forte M, Colombini M (1998) The sensor regions of VDAC are translocated from within the membrane to the surface during the gating processes. Biophys J 74: 2926-2944. (Pubitemid 28268117)
36. Mannella CA (1998) Conformational changes in the mitochondrial channel protein, VDAC, and their functional implications. J Struct Biol 121: 207-218.
37. Reina S, Palermo V, Guarnera A, Guarino F, Messina A, et al. (2010) 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: 2837-2844.
38. Shoshan-Barmatz V, Ben-Hail D (2012) VDAC, a multi-functional mitochondrial protein as a pharmacological target. Mitochondrion 12: 24-34.
39. Abu-Hamad S, Arbel N, Calo D, Arzoine L, Israelson A, et al. (2009) The VDAC1 N-terminus is essential both for apoptosis and the protective effect of anti-apoptotic proteins. J Cell Sci 122: 1906-1916.
40. Villinger S, Briones R, Giller K, Zachariae U, Lange A, et al. (2010) Functional dynamics in the voltage-dependent anion channel. Proc Natl Acad Sci U S A 107: 22546-22551.
41. Reina S, Magrì A, Lolicato M, Guarino F, Impellizzeri A, et al. (2013) Deletion of b-strands 9 and 10 converts VDAC1 voltage-dependence in an asymmetrical process. Biochim Biophys Acta 1827: 793-805.
42. Maurya SR, Mahalakshmi R (2013) Modulation of human mitochondrial voltage-dependent anion channel 2 (hVDAC2): structural stability by cysteine-assisted barrel-lipid interactions. J Biol Chem 288: 25584-25592.
43. De Pinto V, Tomasello F, Messina A, Guarino F, Benz R, et al. (2007) Determination of the conformation of the human VDAC1 N-terminal peptide, a protein moiety essential for the functional properties of the pore. Chembiochem 8: 744-756. (Pubitemid 47183631)
44. Yehezkel G, Abu-hamad S, Shoshan-Barmatz V (2007) An N-Terminal Nucleotide-Binding Site in VDAC1: Involvement in Regulating Mitochondrial Function. J Cell Physiol 212: 551-561. (Pubitemid 47025645)
45. Guo XW, Smith PR, Cognon B, D'Arcangelis D, Dolginova E, et al. (1995) Molecular Design of the Voltage-Dependent, Anion-Selective Channel in the Mitochondrial Outer Membrane. J Struct Biol 114: 41-59.
46. Colombini M (2012) VDAC structure, selectivity, and dynamics. Biochim Biophys acta - Biomembr 1818: 1457-1465.
47. Menzel VA, Cassara MC, Benz R, De Pinto V, Messina A, et al. (2009) Molecular and functional characterization of VDAC2 purified from mammal spermatozoa. Biosci Rep 29: 351-362.
48. Krammer E, Homblé F, Prévost M (2013) Molecular origin of VDAC selectivity towards inorganicions: A combined molecular and Brownian dynamics study. Biochim Biophys acta - Biomembr 1828: 1284-1292.
49. Xu X, Decker W, Sampson MJ, Craigen WJ, Colombini M (1999) Mouse VDAC Isoforms Expressed in Yeast: Channel Properties and Their Roles in Mitochondrial Outer Membrane Permeability. J Membr Biol 170: 89-102. (Pubitemid 29367689)
50. Krammer E-M, Homblé F, Prévost M (2011) Concentration dependent ion selectivity in VDAC: a molecular dynamics simulation study. PLoS One 6: e27994.
51. Lee K Il, Rui H, Pastor RW, ImW (2011) Brownian dynamics simulations of ion transport through the VDAC. Biophys J 100: 611-619.
52. Eswar N, Marti-Renom MA, Webb B, Madhusudhan MS, Eramian D, et al. (2006) Comparative Protein Structure Modeling With MODELLER. Curr Protoc Bioinforma 15: 5.6.1-5.6.30.
53. Sali A, Blundell TL (1993) Comparative protein modelling by satisfaction of spatial restraints. J Mol Biol 234: 779-815. (Pubitemid 24007801)
54. Phillips JC, Braun R, Wang W, Gumbart J, Tajkhorshid E, et al. (2005) Scalable molecular dynamics with NAMD. J Comput Chem 26: 1781-1802. (Pubitemid 43078511)
55. Harvey M, Giupponi G, De Fabritiis G (2009) ACEMD: Accelerating Biomolecular Dynamics in the Microsecond Time Scale. J Chem Theory Comput 5: 1632-1639.
56. Buch I, Giorgino T, De Fabritiis G (2011) Complete reconstruction of an enzyme-inhibitor binding process by molecular dynamics simulations. Proc Natl Acad Sci U S A 108: 10184-10189.
57. Sindhikara DJ, Kim S, Voter AF, Roitberg AE (2009) Bad Seeds Sprout Perilous Dynamics: Stochastic Thermostat Induced Trajectory Synchronization in Biomolecules. J Chem Theory Comput 5: 1624-1631.
58. Lindorff-Larsen K, Piana S, Palmo K, Maragakis P, Klepeis JL, et al. (2010) Improved side-chain torsion potentials for the Amber ff99SB protein force field. Proteins 78: 1950-1958.
59. Jorgensen W, Chandrasekhar J, Madura J, Impey R, Klein M (1983) Comparison of simple potential functions for simulating liquid water. J Chem Phys 79: 926-936.
60. Kumar A, Hajjar E, Ruggerone P, Ceccarelli M (2010) Structural and dynamical properties of the porins OmpF and OmpC: insights from molecular simulations. J Phys Condens matter 22: 454125.
61. Kyte J, Doolittle RF (1982) A simple method for displaying the hydropathic character of a protein. J Mol Biol 157: 105-132.
62. Mezei M (2010) Simulaid: A simulation facilitator and analysis program. J Comput Chem 31: 2658-2668.
63. Baker NA, Sept D, Joseph S, Holst MJ, McCammon JA (2001) Electrostatics of nanosystems: application to microtubules and the ribosome. Proc Natl Acad Sci U S A 98: 10037-10041. (Pubitemid 32802969)
64. Humphrey W, Dalke A, Schulten K (1996) VMD: visual molecular dynamics. J Mol Graph Model 14: 33-38. (Pubitemid 26152973)
65. Dolinsky TJ, Nielsen JE, McCammon JA, Baker NA (2004) PDB2PQR: an automated pipeline for the setup of Piosson-Boltzmann electrostatics calculations. Nucleic Acids Res 32: 665-667.
66. Dolinsky TJ, Czodrowski P, Li H, Nielsen JE, Jensen JH, et al. (2007) PDB2PQR: expanding and upgrading automated preparation of biomolecular structures for molecular simulations. Nucleic Acids Res 35: 522-525.
67. Li H, Robertson AD, Jensen JH (2005) Very fast empirical and rationalization of protein pKa values. Proteins 61: 704-721. (Pubitemid 41753142)
68. Im W, Roux B (2002) Ion permeation and selectivity of OmpF porin: a theoretical study based on molecular dynamics, Brownian dynamics, and continuum electrodiffusion theory. J Mol Biol 322: 851-869. della Ricerca