Functional dynamics in the voltage-dependent anion channel

Proceedings of the National Academy of Sciences of the United States of America

Volumn 107, Issue 52, 2010, Pages 22546-22551

  Villinger, Saskia ^a   Briones, Rodolfo ^a   Giller, Karin ^a   Zachariae, Ulrich ^a   Lange, Adam ^a   De Groot, Bert L ^a   Griesinger, Christian ^a   Becker, Stefan ^a   Zweckstetter, Markus ^a  

^a MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

Author keywords

Membrane protein; Molecular dynamics; NMR spectroscopy; Protein lipid interactions; Structure

Indexed keywords

GLUTAMIC ACID DERIVATIVE; HEXOKINASE; MEMBRANE FACING GLUTAMIC ACID 73; UNCLASSIFIED DRUG; VOLTAGE DEPENDENT ANION CHANNEL 1;

AMINO TERMINAL SEQUENCE; APOPTOSIS; ARTICLE; CHANNEL GATING; CHEMICAL MODIFICATION; CRYSTAL STRUCTURE; MEMBRANE; MITOCHONDRIAL MEMBRANE; MOLECULAR DYNAMICS; NORMAL DISTRIBUTION; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN INTERACTION; SIMULATION;

ANIMALS; CRYSTALLOGRAPHY, X-RAY; DICYCLOHEXYLCARBODIIMIDE; DIMYRISTOYLPHOSPHATIDYLCHOLINE; HUMANS; ION CHANNEL GATING; KINETICS; LIPID BILAYERS; MAGNETIC RESONANCE SPECTROSCOPY; MICE; MITOCHONDRIAL MEMBRANES; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; MUTATION, MISSENSE; PROTEIN STRUCTURE, SECONDARY; SOLUTIONS; TIME FACTORS; VOLTAGE-DEPENDENT ANION CHANNEL 1;

PYRONIA TITHONUS;

EID: 78651092981     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1012310108     Document Type: Article

References (57)

1. Veglia G, Ramamoorthy A (2010) Special issue on "membrane protein dynamics: correlating structure to function". Biochim Biophys Acta 1798:65-67.
2. Tirion MM (1996) Large amplitude elastic motions in proteins from a single-parameter, atomic analysis. Phys Rev Lett 77:1905-1908.
3. Bahar I, Atilgan AR, Erman B (1997) Direct evaluation of thermal fluctuations in proteins using a single-parameter harmonic potential. Fold Des 2:173-181.
4. Traaseth NJ, Veglia G (2010) Probing excited states and activation energy for the integral membrane protein phospholamban by NMR CPMG relaxation dispersion experiments. Biochim Biophys Acta 1798:77-81.
5. Chu S, Coey AT, Lorigan GA (2010) Solid-state (2)H and (15)N NMR studies of side-chain and backbone dynamics of phospholamban in lipid bilayers: investigation of the N27A mutation. Biochim Biophys Acta 1798:210-215.
6. Bhattacharjya S, Ramamoorthy A (2009) Multifunctional host defense peptides: functional and mechanistic insights from NMR structures of potent antimicrobial peptides. FEBS J 276:6465-6473.
7. Salnikov E, Aisenbrey C, Vidovic V, Bechinger B (2010) Solid-state NMR approaches to measure topological equilibria and dynamics of membrane polypeptides. Biochim Biophys Acta 1798:258-265.
8. Hwang PM, Kay LE (2005) Solution structure and dynamics of integral membrane proteins by NMR: a case study involving the enzyme PagP. Methods Enzymol 394:335-350.
9. Liang B, Arora A, Tamm LK (2010) Fast-time scale dynamics of outer membrane protein A by extended model-free analysis of NMR relaxation data. Biochim Biophys Acta 1798:68-76.
10. Arora A, Abildgaard F, Bushweller JH, Tamm LK (2001) Structure of outer membrane protein A transmembrane domain by NMR spectroscopy. Nat Struct Biol 8:334-338.
11. Renault M, et al. (2009) Solution state NMR structure and dynamics of KpOmpA, a 210 residue transmembrane domain possessing a high potential for immunological applications. J Mol Biol 385:117-130.
12. Bayrhuber M, et al. (2008) Structure of the human voltage-dependent anion channel. Proc Natl Acad Sci USA 105:15370-15375.
13. Hiller S, et al. (2008) Solution structure of the integral human membrane protein VDAC-1 in detergent micelles. Science 321:1206-1210.
14. Ujwal R, 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.
15. Benz R (1994) Permeation of hydrophilic solutes through mitochondrial outer membranes: review on mitochondrial porins. Biochim Biophys Acta 1197:167-196.
16. Lemasters JJ, Holmuhamedov E (2006) Voltage-dependent anion channel (VDAC) as mitochondrial governator - thinking outside the box. Biochim Biophys Acta 1762:181-190.
17. 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.
18. Blachly-Dyson E, Forte M (2001) VDAC channels. IUBMB Life 52:113-118.
19. Pavlov E, et al. (2005) The mitochondrial channel VDAC has a cation-selective open state. Biochim Biophys Acta 1710:96-102.
20. Shoshan-Barmatz V, Israelson A, Brdiczka D, Sheu SS (2006) The voltage-dependent anion channel (VDAC): function in intracellular signalling, cell life and cell death. Curr Pharm Design 12:2249-2270.
21. Shoshan-Barmatz V, Keinan N, Zaid H (2008) Uncovering the role of VDAC in the regulation of cell life and death. J Bioenerg Biomembr 40:183-191.
22. Guo XW, Mannella CA (1993) Conformational change in the mitochondrial channel, VDAC, detected by electron cryo-microscopy. Biophys J 64:545-549.
23. Zimmerberg J, Parsegian VA (1986) Polymer inaccessible volume changes during opening and closing of a voltage-dependent ionic channel. Nature 323:36-39.
24. Schneider R, et al. (2010) The native conformation of the human VDAC1 N terminus. Angew Chem Int Ed Engl 49:1882-1885.
25. Zhu G, Xia Y, Nicholson LK, Sze KH (2000) Protein dynamics measurements by TROSYbased NMR experiments. J Magn Reson 143:423-426.
26. Wang C, Rance M, Palmer AG, III (2003) Mapping chemical exchange in proteins with MW > 50 kD. J Am Chem Soc 125:8968-8969.
27. Ringe D, Petsko GA (1986) Study of protein dynamics by X-ray diffraction. Methods Enzymol 131:389-433.
28. Yang LW, et al. (2006) oGNM: online computation of structural dynamics using the Gaussian Network Model. Nucleic Acids Res 34:W24-31.
29. Zaid H, Abu-Hamad S, Israelson A, Nathan I, Shoshan-Barmatz V (2005) The voltage-dependent anion channel-1 modulates apoptotic cell death. Cell Death Differ 12:751-760.
30. De Pinto V, al Jamal JA, Palmieri F (1993) Location of the dicyclohexylcarbodiimide-reactive glutamate residue in the bovine heart mitochondrial porin. J Biol Chem 268:12977-12982.
31. Shoshan-Barmatz V, et al. (2010) VDAC, a multi-functional mitochondrial protein regulating cell life and death. Mol Aspects Med 31:227-285.
32. 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.
33. Yildiz O, Vinothkumar KR, Goswami P, Kuhlbrandt W (2006) Structure of the monomeric outer-membrane porin OmpG in the open and closed conformation. EMBO J 25:3702-3713.
34. Hong H, Szabo G, Tamm LK (2006) Electrostatic couplings in OmpA ion-channel gating suggest a mechanism for pore opening. Nat Chem Biol 2:627-635.
35. Clore GM, Schwieters CD (2006) Concordance of residual dipolar couplings, backbone order parameters and crystallographic B-factors for a small alpha/beta protein: a unified picture of high probability, fast atomic motions in proteins. J Mol Biol 355:879-886.
36. Yang J, Tasayco ML, Polenova T (2009) Dynamics of reassembled thioredoxin studied by magic angle spinning NMR: snapshots from different time scales. J Am Chem Soc 131:13690-13702.
37. Sevvana M, et al. (2008) A ligand-induced switch in the periplasmic domain of sensor histidine kinase CitA. J Mol Biol 377:512-523.
38. Loria JP, Rance M, Palmer AG (1999) A relaxation-compensated Carr-Purcell-Meiboom- Gill Sequence for characterizing chemical exchange by NMR Spectroscopy. J Am Chem Soc 121:2331-2332.
39. Loria JP, Rance M, Palmer AG, 3rd (1999) A TROSY CPMG sequence for characterizing chemical exchange in large proteins. J Biomol NMR 15:151-155.
40. Valiyaveetil F, Hermolin J, Fillingame RH (2002) pH dependent inactivation of solubilized F1F0 ATP synthase by dicyclohexylcarbodiimide: pK(a) of detergent unmasked aspartyl-61 in Escherichia coli subunit c. Biochim Biophys Acta 1553:296-301.
41. Khorana HG (1953) The chemistry of carbodiimides. British Columbia Research Council 145-166.
42. Shafir I, Feng W, Shoshan-Barmatz V (1998) Dicyclohexylcarbodiimide interaction with the voltage-dependent anion channel from sarcoplasmic reticulum. Eur J Biochem 253:627-636.
43. Thomas L, Blachly-Dyson E, Colombini M, Forte M (1993) Mapping of residues forming the voltage sensor of the voltage-dependent anion-selective channel. Proc Natl Acad Sci USA 90:5446-5449.
44. Abu-Hamad S, Zaid H, Israelson A, Nahon E, Shoshan-Barmatz V (2008) Hexokinase-I protection against apoptotic cell death is mediated via interaction with the voltage-dependent anion channel-1: mapping the site of binding. J Biol Chem 283:13482-13490.
45. Nakashima RA, Mangan PS, Colombini M, Pedersen PL (1986) Hexokinase receptor complex in hepatoma mitochondria: evidence from N,N′- dicyclohexylcarbodiimide-labeling studies for the involvement of the pore-forming protein VDAC. Biochemistry 25:1015-1021.
46. Naveed H, Jackups R, II, Liang J (2009) Predicting weakly stable regions, oligomerization state, and protein-protein interfaces in transmembrane domains of outer membrane proteins. Proc Natl Acad Sci USA 106:12735-12740.
47. Nyholm TK, Ozdirekcan S, Killian JA (2007) How protein transmembrane segments sense the lipid environment. Biochemistry 46:1457-1465.
48. Langosch D, Arkin IT (2009) Interaction and conformational dynamics of membrane-spanning protein helices. Protein Sci 18:1343-1358.
49. Kagan BL, Thundimadathil J (2010) Amyloid peptide pores and the beta sheet conformation. Adv Exp Med Biol 677:150-167.
50. Galdiero S, Galdiero M, Pedone C (2007) beta-Barrel membrane bacterial proteins: structure, function, assembly and interaction with lipids. Curr Protein Pept Sci 8:63-82.
51. Bogdanov M, Heacock P, Guan Z, Dowhan W (2010) Plasticity of lipid-protein interactions in the function and topogenesis of the membrane protein lactose permease from Escherichia coli. Proc Natl Acad Sci USA 107:15057-15062.
52. Hunte C, Richers S (2008) Lipids and membrane protein structures. Curr Opin Struct Biol 18:406-411.
53. Rostovtseva TK, Bezrukov SM (2008) VDAC regulation: role of cytosolic proteins and mitochondrial lipids. J Bioenerg Biomembr 40:163-170.
54. de Kroon AI, Dolis D, Mayer A, Lill R, de Kruijff B (1997) Phospholipid composition of highly purified mitochondrial outer membranes of rat liver and Neurospora crassa. Is cardiolipin present in the mitochondrial outer membrane? Biochim Biophys Acta 1325:108-116.
55. Rostovtseva TK, Tan W, Colombini M (2005) On the role of VDAC in apoptosis: fact and fiction. J Bioenerg Biomembr 37:129-142.
56. Eletsky A, Kienhofer A, Pervushin K (2001) TROSY NMR with partially deuterated proteins. J Biomol NMR 20:177-180.
57. Zhu G, Kong XM, Sze KH (1999) Gradient and sensitivity enhancement of 2D TROSY with water flip-back, 3D NOESY-TROSY and TOCSY-TROSY experiments. J Biomol NMR 13:77-81.