Solid-state NMR, electrophysiology and molecular dynamics characterization of human VDAC2

Journal of Biomolecular NMR

Volumn 61, Issue 3-4, 2015, Pages 311-320

  Gattin, Zrinka ^a,b   Schneider, Robert ^a,c   Laukat, Yvonne ^a   Giller, Karin ^a   Maier, Elke ^d   Zweckstetter, Markus ^a,e,f   Griesinger, Christian ^a   Benz, Roland ^d,g   Becker, Stefan ^a   Lange, Adam ^a,h  

^a MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

^b MAX PLANCK INSTITUTE FOR DYNAMICS AND SELF ORGANIZATION   (Germany)

^c UNIVERSITÉ DES SCIENCES ET TECHNOLOGIES DE LILLE   (France)

^d UNIVERSITY OF WÜRZBURG   (Germany)

^e GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

^f UNIVERSITY MEDICAL CENTER GÖTTINGEN   (Germany)

^g JACOBS UNIVERSITY BREMEN   (Germany)

^h HUMBOLDT UNIVERSITY   (Germany)

Author keywords

Membrane proteins; Molecular dynamics simulations; Solid state NMR; Voltage dependent anion channel

Indexed keywords

ISOPROTEIN; LIPID BILAYER; VDAC1 PROTEIN, HUMAN; VDAC2 PROTEIN, HUMAN; VOLTAGE DEPENDENT ANION CHANNEL 1; VOLTAGE DEPENDENT ANION CHANNEL 2;

AMINO ACID SEQUENCE; CHEMISTRY; CONFORMATION; ELECTROPHYSIOLOGY; HUMAN; LIPID BILAYER; METABOLISM; MITOCHONDRION; MOLECULAR DYNAMICS; MOLECULAR GENETICS; NUCLEAR MAGNETIC RESONANCE; PHYSIOLOGY; PROCEDURES; SEQUENCE ALIGNMENT; ULTRASTRUCTURE;

AMINO ACID SEQUENCE; ELECTROPHYSIOLOGICAL PHENOMENA; HUMANS; LIPID BILAYERS; MITOCHONDRIA; MOLECULAR CONFORMATION; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN ISOFORMS; SEQUENCE ALIGNMENT; VOLTAGE-DEPENDENT ANION CHANNEL 1; VOLTAGE-DEPENDENT ANION CHANNEL 2;

EID: 84939966319     PISSN: 09252738     EISSN: 15735001     Source Type: Journal    
DOI: 10.1007/s10858-014-9876-5     Document Type: Article

References (56)

1. Anflous K, Armstrong DD, Craigen WJ (2001) Altered mitochondrial sensitivity for ADP and maintenance of creatine-stimulated respiration in oxidative striated muscles from VDAC1-deficient mice. J Biol Chem 276:1954-1960. doi: 10.1074/jbc.M006587200
2. Bauer AJ, Gieschler S, Lemberg KM et al (2011) Functional model of metabolite gating by human voltage-dependent anion channel 2. Biochemistry 50:3408-3410. doi: 10.1021/bi2003247
3. Bayrhuber M, Meins T, Habeck M et al (2008) Structure of the human voltage-dependent anion channel. Proc Natl Acad Sci USA 105:15370-15375. doi: 10.1073/pnas.0808115105
4. Benz R (1994) Permeation of hydrophilic solutes through mitochondrial outer membranes: review on mitochondrial porins. Biochim Biophys Acta 1197:167-196
5. Benz R, Janko K, Boos W, Läuger P (1978) Formation of large, ion-permeable membrane channels by the matrix protein (porin) of Escherichia coli. Biochim Biophys Acta (BBA) 511:305-319
6. Benz R, Schmid A, Hancock R (1985) Ion selectivity of gram-negative bacterial porins. J Bacteriol 162:722-727
7. Berendsen HJC, Postma JPM, van Gunsteren WF et al (1984) Molecular dynamics with coupling to an external bath. J Chem Phys 81:3684. doi: 10.1063/1.448118
8. Berger O, Edholm O, Jähnig F (1997) Molecular dynamics simulations of a fluid bilayer of dipalmitoylphosphatidylcholine at full hydration, constant pressure, and constant temperature. Biophys J 72:2002-2013. doi: 10.1016/S0006-3495(97)78845-3
9. Blachly-Dyson E, Song J (1997) Multicopy suppressors of phenotypes resulting from the absence of yeast VDAC encode a VDAC-like protein. Mol Cell Biochem 17:5727-5738
10. Blachly-Dyson E, Zambronicz EB, Yu WH et al (1993) Cloning and functional expression in yeast of two human isoforms of the outer mitochondrial membrane channel, the voltage-dependent anion channel. J Biol Chem 268:1835-1841
11. Bussi G, Donadio D, Parrinello M (2007) Canonical sampling through velocity rescaling. J Chem Phys 126:014101. doi: 10.1063/1.2408420
12. Cheng EHY, Sheiko TV, Fisher JK et al (2003) VDAC2 inhibits BAK activation and mitochondrial apoptosis. Science 301:513-517. doi: 10.1126/science.1083995
13. Choudhary OP, Paz A, Adelman JL et al (2014) Structure-guided simulations illuminate the mechanism of ATP transport through VDAC1. Nat Struct Mol Biol 21:626-632. doi: 10.1038/nsmb.2841
14. Colombini M (1980) Pore Size and Properties of Channels from Mitoehondria Isolated from Neurospora crassa. J MembrBiol 53:79-84
15. Colombini M (2004) VDAC: the channel at the interface between mitochondria and the cytosol. Mol Cell Biochem 256-257:107-115
16. Darden T, York D, Pedersen L (1993) Particle mesh Ewald: an N·log(N) method for Ewald sums in large systems. J Chem Phys 98:10089. doi: 10.1063/1.464397
17. Daura X, Gademann K, Jaun B et al (1999) Peptide folding: when simulation meets experiment. Angew Chem Int Ed Engl 38:236-240. doi: 10.1002/(SICI)1521-3773(19990115)38:1/2<236:AID-ANIE236>3.0.CO;2-M
18. De Pinto V, Tomasello F, Messina A 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. doi: 10.1002/cbic.200700009
19. Engelhardt H, Meins T, Poynor M et al (2007) High-level expression, refolding and probing the natural fold of the human voltage-dependent anion channel isoforms I and II. J Membr Biol 216:93-105. doi: 10.1007/s00232-007-9038-8
20. Feenstra KA, Hess B, Berendsen HJC (1999) Improving efficiency of large time-scale molecular dynamics simulations of hydrogen-rich systems. J Comput Chem 20:786-798. doi: 10.1002/(SICI)1096-987X(199906)20:8<786:AID-JCC5>3.0.CO;2-B
21. Fung BM, Khitrina K, Ermolaev K (2000) An improved broadband decoupling sequence for liquid crystals and solids. J Magn Reson 142:97-101. doi: 10.1006/jmre.1999.1896
22. Hess B, Bekker H, Berendsen HJC, Fraaije JGEM (1997) LINCS: a linear constraint solver for molecular simulations. J Comput Chem 18:1463-1472. doi: 10.1002/(SICI)1096-987X(199709)18:12<1463:AID-JCC4>3.0.CO;2-H
23. Hess B, Uppsala S, Lindahl E (2008) GROMACS 4: algorithms for highly efficient, load-balanced, and scalable molecular simulation, pp 435-447
24. Hiller S, Garces RG, Malia TJ et al (2008) Solution structure of the integral human membrane protein VDAC-1 in detergent micelles. Science 321:1206-1210. doi: 10.1126/science.1161302
25. Jorgensen W (1996) Development and testing of the OPLS all-atom force field on conformational energetics and properties of organic liquids. J Am Chem Soc 118:11225-11236
26. Jorgensen WL, Madura JD (1983) Solvation and conformation of methanol in water. J Am Chem Soc 105:1407-1413
27. Kabsch W, Sander C (1983) Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 22:2577-2637. doi: 10.1002/bip.360221211
28. Krammer E-M, Homblé F, Prévost M (2011) Concentration dependent ion selectivity in VDAC: a molecular dynamics simulation study. PLoS ONE 6:e27994. doi: 10.1371/journal.pone.0027994
29. Lindén M, Gellerfors P (1983) Hydrodynamic properties of porin isolated from outer membranes of rat liver mitochondria. Biochim Biophys Acta 736:125-129
30. Miyamoto S, Kollman P (1992) Settle: an analytical version of the SHAKE and RATTLE algorithm for rigid water models. J Comput Chem 13:952-962. doi: 10.1002/jcc.540130805
31. Naghdi S, Varnai P, Hunyady L, Hajnoczky G (2012) The isoform specific N terminus of VDAC2 is dispensable for tBid induced cytochrome C release. Biophys J 102:437a. doi: 10.1016/j.bpj.2011.11.2391
32. Popp B, Court DA, Benz R, Neupert W, Lill R (1996) The role of the N and C termini of recombinant Neurospora mitochondrial porin in channel formation and voltage-dependent gating. J Biol Chem 271:13593-13899
33. Reina S, Palermo V, Guarnera 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. doi: 10.1016/j.febslet.2010.04.066
34. 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. doi: 10.1016/S0006-3495(97)78841-6
35. Rui H, Lee KI, Pastor RW, Im W (2011) Molecular dynamics studies of ion permeation in VDAC. Biophys J 100:602-610. doi: 10.1016/j.bpj.2010.12.3711
36. Runke G, Maier E, Summers W et al (2006) Deletion variants of Neurospora mitochondrial porin: electrophysiological and spectroscopic analysis. Biophys J 90:3155-3164. doi: 10.1529/biophysj.105.072520
37. Šali A, Blundell T (1993) Comparative protein modelling by satisfaction of spatial restraints. J Mol Biol 234:779-815
38. Sampson MJ, Lovell RS, Craigen WJ (1996) Isolation, characterization, and mapping of two mouse mitochondrial voltage-dependent anion channel isoforms. Genomics 33:283-288. doi: 10.1006/geno.1996.0193
39. Sampson MJ, Lovell RS, Craigen WJ (1997) The Murine voltage-dependent anion channel gene family. J Biol Chem 272:18966-18973
40. Sampson MJ, Decker WK, Beaudet AL et al (2001) Immotile sperm and infertility in mice lacking mitochondrial voltage-dependent anion channel type 3. J Biol Chem 276:39206-39212. doi: 10.1074/jbc.M104724200
41. Schein SJ, Colombini M, Finkelstein A (1976) Reconstitution in planar lipid bilayers of a voltage-dependent anion-selective channel obtained from paramecium mitochondria. J Membr Biol 30:99-120
42. Schneider R, Etzkorn M, Giller K et al (2010) The native conformation of the human VDAC1 N terminus. Angew Chem Int Ed Engl 49:1882-1885. doi: 10.1002/anie.200906241
43. Schredelseker J, Paz A, López CJ 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. doi: 10.1074/jbc.M113.497438
44. Smack DP, Colombini M (2014) Voltage-dependent channels found in the membrane fraction of corn mitochondria. 1985:1094-1097
45. Sorgato MC, Moran O (1993) Channels in mitochondrial membranes: knowns, unknowns, and prospects for the future. Crit Rev Biochem Mol Biol 28:127-171
46. Teijido O, Rappaport SM, Chamberlin A et al (2014) Acidification affects voltage-dependent anion channel functioning asymmetrically: role of salt bridges. J Biol Chem. doi: 10.1074/jbc.M114.576314
47. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673-4680
48. Ujwal R, Cascio D, Colletier J-P et al (2008) The crystal structure of mouse VDAC1 at 2.3 A resolution reveals mechanistic insights into metabolite gating. Proc Natl Acad Sci USA 105:17742-17747. doi: 10.1073/pnas.0809634105
49. Villinger S, Briones R, Giller K et al (2010) Functional dynamics in the voltage-dependent anion channel. Proc Natl Acad Sci USA 107:22546-22551. doi: 10.1073/pnas.1012310108
50. Villinger S, Giller K, Bayrhuber M (2014) Nucleotide interactions of the human voltage-dependent anion channel. J Biol Chem 289:13397-13406. doi: 10.1074/jbc.M113.524173
51. Wang J, Wolf RM, Caldwell JW et al (2004) Development and testing of a general amber force field. J Comput Chem 25:1157-1174. doi: 10.1002/jcc.20035
52. Xu X, Decker W, Sampson M (1999) Mouse VDAC isoforms expressed in yeast: channel properties and their roles in mitochondrial outer membrane permeability. J Membr Biol 170:89-102
53. Yagoda N, von Rechenberg M, Zaganjor E et al (2007) RAS-RAF-MEK-dependent oxidative cell death involving voltage-dependent anion channels. Nature 447:864-868. doi: 10.1038/nature05859
54. Yamagata H, Shimizu S, Nishida Y et al (2009) Requirement of voltage-dependent anion channel 2 for pro-apoptotic activity of Bax. Oncogene 28:3563-3572. doi: 10.1038/onc.2009.213
55. Yu T-Y, Raschle T, Hiller S, Wagner G (2012) Solution NMR spectroscopic characterization of human VDAC-2 in detergent micelles and lipid bilayer nanodiscs. Biochim Biophys Acta 1818:1562-1569. doi: 10.1016/j.bbamem.2011.11.012
56. Zachariae U, Schneider R, Briones R et al (2012) β-Barrel mobility underlies closure of the voltage-dependent anion channel. Structure 20:1540-1549. doi: 10.1016/j.str.2012.06.015