The N-Terminal Peptides of the Three Human Isoforms of the Mitochondrial Voltage-Dependent Anion Channel Have Different Helical Propensities

Biochemistry

Volumn 54, Issue 36, 2015, Pages 5646-5656

  Guardiani, Carlo ^a   Scorciapino, Mariano Andrea ^a,b   Amodeo, Giuseppe Federico ^a   Grdadolnik, Joze ^c   Pappalardo, Giuseppe ^d   De Pinto, Vito ^e   Ceccarelli, Matteo ^a,b   Casu, Mariano ^a  

^a UNIVERSITY OF CAGLIARI   (Italy)

^b IOM CNR LABORATORIO TASC   (Italy)

^c NATIONAL INSTITUTE OF CHEMISTRY   (Slovenia)

^d CNR   (Italy)

^e UNIVERSITY OF CATANIA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CELL DEATH; IONS; PEPTIDES;

CHEMICO-PHYSICAL PROPERTIES; COMPUTER ASSISTED; CONFORMATIONAL EQUILIBRIUM; FOLDING PROPENSITIES; N-TERMINAL DOMAINS; PROTEIN STABILITY; SPECTROSCOPIC TECHNIQUE; VOLTAGE-DEPENDENT ANION CHANNELS;

PROTEINS;

PEPTIDE; VOLTAGE DEPENDENT ANION CHANNEL; CARRIER PROTEIN; ISOPROTEIN; MITOCHONDRIAL PROTEIN; VDAC1 PROTEIN, HUMAN; VDAC2 PROTEIN, HUMAN; VDAC3 PROTEIN, HUMAN; VOLTAGE DEPENDENT ANION CHANNEL 1; VOLTAGE DEPENDENT ANION CHANNEL 2;

AMINO TERMINAL SEQUENCE; ARTICLE; BIOINFORMATICS; CIRCULAR DICHROISM; INFRARED SPECTROSCOPY; MEMBRANE PERMEABILITY; MITOCHONDRION; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN CONFORMATION; BIOLOGY; CHEMISTRY; HUMAN; INFRARED SPECTROPHOTOMETRY; MOLECULAR DYNAMICS; NUCLEAR MAGNETIC RESONANCE; PROTEIN SECONDARY STRUCTURE;

CIRCULAR DICHROISM; COMPUTATIONAL BIOLOGY; HUMANS; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; MITOCHONDRIAL PROTEINS; MOLECULAR DYNAMICS SIMULATION; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PEPTIDES; PROTEIN ISOFORMS; PROTEIN STRUCTURE, SECONDARY; SPECTROPHOTOMETRY, INFRARED; VOLTAGE-DEPENDENT ANION CHANNEL 1; VOLTAGE-DEPENDENT ANION CHANNEL 2; VOLTAGE-DEPENDENT ANION CHANNELS;

EID: 84941640333     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/acs.biochem.5b00469     Document Type: Article

References (64)

1. Benz, R. (1994) Permeation of hydrophilic solutes through mitochondrial outer membranes: review on mitochondrial porins Biochim. Biophys. Acta, Rev. Biomembr. 1197, 167-196 10.1016/0304-4157(94)90004-3
2. Colombini, M. (2004) VDAC: the channel at the interface between mitochondria and the cytosol Mol. Cell. Biochem. 256-257, 107-115 10.1023/B:MCBI.0000009862.17396.8d
3. Shoshan-Barmatz, V., De Pinto, V., Zweckstetter, M., Raviv, Z., Keinan, N., and Arbel, N. (2010) VDAC, a multi-functional mitochondrial protein regulating cell life and death Mol. Aspects Med. 31, 227-285 10.1016/j.mam.2010.03.002
4. Rostovtseva, T. and Colombini, M. (1997) VDAC channels mediate and gate the flow of ATP: implications for the regulation of mitochondrial function Biophys. J. 72, 1954-1962 10.1016/S0006-3495(97)78841-6
5. Beutner, G., Ruck, A., Riede, B., and 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 10.1042/bst0250151
6. Cheng, E. H. Y., Sheiko, T. V., Fisher, J. K., Craigen, W. J., and Korsmeyer, S. J. (2003) VDAC2 inhibits BAK activation and mitochondrial apoptosis Science 301, 513-517 10.1126/science.1083995
7. Tomasello, F. M., Messina, A., Lartigue, L., Schembri, L., Medina, C., Reina, S., Thoraval, D., Crouzet, M., Ichas, F., De Pinto, V., and De Giorgi, F. (2009) Outer membrane VDAC1 controls permeability transition of the inner mitochondrial membrane in cellulo during stress-induced apoptosis Cell Res. 19, 1363-1376 10.1038/cr.2009.98
8. Shoshan-Barmatz, V., Keinan, N., Abu-Hamad, S., Tyomkin, D., and 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 10.1016/j.bbabio.2010.03.003
9. Shoshan-Barmatz, V. and Ben-Hail, D. (2012) VDAC, a multi-functional mitochondrial protein as a pharmacological target Mitochondrion 12, 24-34 10.1016/j.mito.2011.04.001
10. Maldonado, E. N. and Lemasters, J. J. (2012) Warburg revisited: regulation of mitochondrial metabolism by voltage-dependent anion channels in cancer cells J. Pharmacol. Exp. Ther. 342, 637-641 10.1124/jpet.112.192153
11. Messina, A., Reina, S., Guarino, F., and De Pinto, V. (2012) VDAC isoforms in mammals Biochim. Biophys. Acta, Biomembr. 1818, 1466-1476 10.1016/j.bbamem.2011.10.005
12. De Pinto, V., Guarino, F., Guarnera, A., Messina, A., Reina, S., Tomasello, F. M., Palermo, V., and Mazzoni, C. (2010) Characterization of human VDAC isoforms: a peculiar function for VDAC3? Biochim. Biophys. Acta, Bioenerg. 1797, 1268-1275 10.1016/j.bbabio.2010.01.031
13. Hiller, S., Garces, R. G., Malia, T. J., Orekhov, V. Y., Colombini, M., and Wagner, G. (2008) Solution structure of the integral human membrane protein VDAC-1 in detergent micelles Science 321, 1206-1210 10.1126/science.1161302
14. Ujwal, R., Cascio, D., Colletier, J.-P., Faham, S., Zhang, J., Toro, L., Ping, P., and Abramson, J. (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 10.1073/pnas.0809634105
15. Bayrhuber, M., Meins, T., Habeck, M., Becker, S., Giller, K., Villinger, S., Vonrhein, C., Griesinger, C., Zweckstetter, M., and Zeth, K. (2008) Structure of the human voltage-dependent anion channel Proc. Natl. Acad. Sci. U. S. A. 105, 15370-15375 10.1073/pnas.0808115105
16. Schredelseker, J., Paz, A., López, C. J., Altenbach, C., Leung, C. S., Drexler, M. K., Chen, J.-N., Hubbell, W. L., and Abramson, J. (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 10.1074/jbc.M113.497438
17. Tomasello, F. M., Guarino, F., Reina, S., Messina, A., and 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 10.1371/journal.pone.0081522
18. Teijido, O., Ujwal, R., Hillerdal, C.-O., Kullman, L., Rostovtseva, T. K., and Abramson, J. (2012) Affixing N-terminal α-helix to the wall of the voltage-dependent anion channel does not prevent its voltage gating J. Biol. Chem. 287, 11437-11445 10.1074/jbc.M111.314229
19. Zachariae, U., Schneider, R., Briones, R., Gattin, Z., Demers, J., Giller, K., Maier, E., Zweckstetter, M., Griesinger, C., Becker, S., Benz, R., de Groot, B. L., and Lange, A. (2012) b-Barrel Mobility Underlies Closure of the Voltage-Dependent Anion Channel Structure 20, 1540-1549 10.1016/j.str.2012.06.015
20. Rui, H., Lee, K. I., Pastor, R. W., and Im, W. (2011) Molecular dynamics studies of ion permeation in VDAC Biophys. J. 100, 602-610 10.1016/j.bpj.2010.12.3711
21. Choudhary, O. P., Ujwal, R., Kowallis, W., Coalson, R., Abramson, J., and Grabe, M. (2010) The electrostatics of VDAC: implications for selectivity and gating J. Mol. Biol. 396, 580-592 10.1016/j.jmb.2009.12.006
22. Song, J., Midson, C., Blachly-Dyson, E., Forte, M., and 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 10.1016/S0006-3495(98)78000-2
23. Mannella, C. a. (1998) Conformational changes in the mitochondrial channel protein, VDAC, and their functional implications J. Struct. Biol. 121, 207-218 10.1006/jsbi.1997.3954
24. Abu-Hamad, S., Arbel, N., Calo, D., Arzoine, L., Israelson, A., Keinan, N., Ben-Romano, R., Friedman, O., and Shoshan-Barmatz, V. (2009) The VDAC1 N-terminus is essential both for apoptosis and the protective effect of anti-apoptotic proteins J. Cell Sci. 122, 1906-1916 10.1242/jcs.040188
25. Kelly, S. M. and Price, N. C. (2000) The use of circular dichroism in the investigation of protein structure and function Curr. Protein Pept. Sci. 1, 349-384 10.2174/1389203003381315
26. Cavanagh, J., Fairbrother, W. J., Palmer, A. G., III, Rance, M., and Skelton, N. J. (2007) Protein NMR Spectroscopy: Principles and Practice, 2 nd ed., Elsevier Academic Press, Oxford, U.K.
27. Ogg, R., Kingsley, P., and Taylor, J. (1994) WET, a T1- and B1-Insensitive Water-Suppression Method for in Vivo Localized 1H NMR Spectroscopy J. Magn. Reson., Ser. B 104, 1-10 10.1006/jmrb.1994.1048
28. Smallcombe, S., Patt, S. L., and Keifer, P. (1995) WET solvent suppression and its applications to LC NMR and high-resolution NMR spectroscopy J. Magn. Reson., Ser. A 117, 295-303 10.1006/jmra.1995.0759
29. Shen, Y., Delaglio, F., Cornilescu, G., and Bax, A. (2009) TALOS+: a hybrid method for predicting protein backbone torsion angles from NMR chemical shifts J. Biomol. NMR 44, 213-223 10.1007/s10858-009-9333-z
30. Grantham, R. (1974) Amino acid difference formula to help explain protein evolution Science 185, 862-864 10.1126/science.185.4154.862
31. Muñoz, V. and Serrano, L. (1994) Elucidating the folding problem of helical peptides using empirical parameters Nat. Struct. Biol. 1, 399-409 10.1038/nsb0694-399
32. Muñoz, V. and Serrano, L. (1995) Elucidating the folding problem of helical peptides using empirical parameters. II. Helix macrodipole effects and rational modification of the helical content of natural peptides J. Mol. Biol. 245, 275-296 10.1006/jmbi.1994.0023
33. Muñoz, V. and Serrano, L. (1995) Elucidating the folding problem of helical peptides using empirical parameters. III. Temperature and pH dependence J. Mol. Biol. 245, 297-308 10.1006/jmbi.1994.0024
34. Muñoz, V. and Serrano, L. (1997) Development of the multiple sequence approximation within the AGADIR model of alpha-helix formation: comparison with Zimm-Bragg and Lifson-Roig formalisms Biopolymers 41, 495-509 10.1002/(SICI)1097-0282(19970415)41:5<495::AID-BIP2>3.3.CO;2-6
35. Lacroix, E., Viguera, A. R., and Serrano, L. (1998) Elucidating the folding problem of alpha-helices: local motifs, long-range electrostatics, ionic-strength dependence and prediction of NMR parameters J. Mol. Biol. 284, 173-191 10.1006/jmbi.1998.2145
36. Case, D. A., Babin, V., Berryman, J. T., Betz, R. M., Cai, Q., Cerutti, D. S., Cheatham, T. E., III, Darden, T. A., Duke, R. E., Gohlke, H., Goetz, A. W., Gusarov, S., Homeyer, N., Janowski, P., Kaus, J., Kolossvary, I., Kovalenko, A., Lee, T. S., LeGrand, S., Luchko, T., Luo, R., Madej, B., Merz, K. M., Paesani, F., Roe, D. R., Roitberg, A., Sagui, C., Salomon-Ferrer, R., Seabra, G., Simmerling, C. L., Smith, W., Swails, J., Walker, R. C., Wang, J., Wolf, R. M., Wu, X., and Kollman, P. A. (2012) AMBER 14, University of California, San Francisco.
37. Fukunishi, H., Watanabe, O., and Takada, S. (2002) On the Hamiltonian replica exchange method for efficient sampling of biomolecular systems: Application to protein structure prediction J. Chem. Phys. 116, 9058-9067 10.1063/1.1472510
38. Kannan, S. and Zacharias, M. (2007) Enhanced sampling of peptide and protein conformations using replica exchange simulations with a peptide backbone biasing-potential Proteins: Struct., Funct., Genet. 66, 697-706 10.1002/prot.21258
39. Sugita, Y. and Okamoto, Y. (1999) Replica-exchange molecular dynamics method for protein folding Chem. Phys. Lett. 314, 141-151 10.1016/S0009-2614(99)01123-9
40. Bergonzo, C., Henriksen, N. M., Roe, D. R., Swails, J. M., Roitberg, A. E., and Cheatham, T. E. (2014) Multidimensional Replica Exchange Molecular Dynamics Yields a Converged Ensemble of an RNA Tetranucleotide J. Chem. Theory Comput. 10, 492-499 10.1021/ct400862k
41. Kabsch, W. and Sander, C. (1983) Dictionary of Protein Secondary Structure: Pattern Recognition of Hydrogen-Bonded and Geometrical Features Biopolymers 22, 2577-2637 10.1002/bip.360221211
42. Sreerama, N. and Woody, R. W. (1993) A self-consistent method for the analysis of protein secondary structure from circular dichroism Anal. Biochem. 209, 32-44 10.1006/abio.1993.1079
43. Greenfield, N. J. and Fasman, G. D. (1969) Computed circular dichroism spectra for the evaluation of protein conformation Biochemistry 8, 4108-4116 10.1021/bi00838a031
44. Barth, A. (2007) Infrared spectroscopy of proteins Biochim. Biophys. Acta, Bioenerg. 1767, 1073-1101 10.1016/j.bbabio.2007.06.004
45. Wishart, D. S., Sykes, B. D., and Richards, F. M. (1991) Relationship between nuclear magnetic resonance chemical shift and protein secondary structure J. Mol. Biol. 222, 311-333 10.1016/0022-2836(91)90214-Q
46. Wishart, D. S., Sykes, B. D., and Richards, F. M. (1992) The Chemical Shift Index: A Fast and Simple Method for the Assignment of Protein Secondary Structure through NMR Spectroscopy Biochemistry 31, 1647-1651 10.1021/bi00121a010
47. Wishart, D. S. and Sykes, B. D. (1994) The 13C Chemical-Shift Index: A Simple Method for the Identification of Protein Secondary Structure Using 13C Chemical-Shift Data J. Biomol. NMR 4, 171-180 10.1007/BF00175245
48. De Pinto, V., Tomasello, F., Messina, A., Guarino, F., Benz, R., La Mendola, D., Magrì, A., Milardi, D., and Pappalardo, G. (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 10.1002/cbic.200700009
49. Strandberg, E. and Ulrich, A. S. (2004) NMR methods for studying membrane-active antimicrobial peptides Concepts Magn. Reson., Part A 23A, 89-120 10.1002/cmr.a.20024
50. Manzo, G., Sanna, R., Casu, M., Mignogna, G., Mangoni, M. L., Rinaldi, A. C., and Scorciapino, M. A. (2012) Toward an improved structural model of the frog-skin antimicrobial peptide esculentin-1b(1-18) Biopolymers 97, 873-881 10.1002/bip.22086
51. Scorciapino, M. A., Pirri, G., Vargiu, A. V., Ruggerone, P., Giuliani, A., Casu, M., Buerck, J., Wadhwani, P., Ulrich, A. S., and Rinaldi, A. C. (2012) A novel dendrimeric peptide with antimicrobial properties: structure-function analysis of SB056 Biophys. J. 102, 1039-1048 10.1016/j.bpj.2012.01.048
52. Crevenna, A. H., Naredi-Rainer, N., Lamb, D. C., Wedlich-Söldner, R., and Dzubiella, J. (2012) Effects of Hofmeister Ions on the α-Helical Structure of Proteins Biophys. J. 102, 907-915 10.1016/j.bpj.2012.01.035
53. Dolinsky, T. J., Nielsen, J. E., McCammon, J. A., and Baker, N. A. (2004) PDB2PQR: an automated pipeline for the setup of Piosson-Boltzmann electrostatics calculations Nucleic Acids Res. 32, W665-W667 10.1093/nar/gkh381
54. Amodeo, G. F., Scorciapino, M. A., Messina, A., De Pinto, V., and Ceccarelli, M. (2014) Charged Residues Distribution Modulates Selectivity of the Open State of Human Isoforms of the Voltage Dependent Anion-Selective Channel PLoS One 9, e103879 10.1371/journal.pone.0103879
55. Hiller, S., Abramson, J., Mannella, C., Wagner, G., and Zeth, K. (2010) The 3D structures of VDAC represent a native conformation Trends Biochem. Sci. 35, 514-521 10.1016/j.tibs.2010.03.005
56. Guo, X. W., Smith, P. R., Cognon, B., D'Arcangelis, D., Dolginova, E., and Mannella, C. A. (1995) Molecular Design of the Voltage-Dependent, Anion-Selective Channel in the Mitochondrial Outer Membrane J. Struct. Biol. 114, 41-59 10.1006/jsbi.1995.1004
57. Schneider, R., Etzkorn, M., Giller, K., Daebel, V., Eisfeld, J., Zweckstetter, M., Griesinger, C., Becker, S., and Lange, A. (2010) The native conformation of the human VDAC1 N terminus Angew. Chem., Int. Ed. 49, 1882-1885 10.1002/anie.200906241
58. D'Abramo, M., Rinaldi, A. C., Bozzi, A., Amadei, A., Mignogna, G., Di Nola, A., and Aschi, M. (2006) Conformational behavior of temporin A and temporin L in aqueous solution: a computational/experimental study Biopolymers 81, 215-224 10.1002/bip.20404
59. Roccatano, D., Colombo, G., Fioroni, M., and Mark, A. E. (2002) Mechanism by which 2,2,2-trifluoroethanol/water mixtures stabilize secondary-structure formation in peptides: A molecular dynamics study Proc. Natl. Acad. Sci. U. S. A. 99, 12179-12184 10.1073/pnas.182199699
60. Geula, S., Ben-Hail, D., and Shoshan-Barmatz, V. (2012) Structure-based analysis of VDAC1: N-terminus location, translocation, channel gating and association with anti-apoptotic proteins Biochem. J. 444, 475-485 10.1042/BJ20112079
61. Villinger, S., Briones, R., Giller, K., Zachariae, U., Lange, A., de Groot, B. L., Griesinger, C., Becker, S., and Zweckstetter, M. (2010) Functional dynamics in the voltage-dependent anion channel Proc. Natl. Acad. Sci. U. S. A. 107, 22546-22551 10.1073/pnas.1012310108
62. Reina, S., Magrì, A., Lolicato, M., Guarino, F., Impellizzeri, A., Maier, E., Benz, R., Ceccarelli, M., De Pinto, V., and Messina, A. (2013) Deletion of b-strands 9 and 10 converts VDAC1 voltage-dependence in an asymmetrical process Biochim. Biophys. Acta, Bioenerg. 1827, 793-805 10.1016/j.bbabio.2013.03.007
63. Boehr, D. D., Nussinov, R., and Wright, P. E. (2009) The role of dynamic conformational ensembles in biomolecular recognition Nat. Chem. Biol. 5, 789-796 10.1038/nchembio.232
64. Reina, S., Palermo, V., Guarnera, A., Guarino, F., Messina, A., Mazzoni, C., and De Pinto, V. (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 10.1016/j.febslet.2010.04.066