How pH opens a H+ channel: The gating mechanism of influenza A M2

Structure

Volumn 13, Issue 12, 2005, Pages 1789-1798

  Kass, Itamar ^a   Arkin, Isaiah T ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

HISTIDINE; HYDROGEN; PROTEIN M2; VIRUS PROTEIN; WATER;

AMINO ACID SEQUENCE; ARTICLE; CHANNEL GATING; ELECTRICITY; ENDOSOME; INFLUENZA VIRUS A; IONIZATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PH; PRIORITY JOURNAL; PROTEIN STABILITY; PROTEIN STRUCTURE; PROTON TRANSPORT; SIMULATION;

HISTIDINE; HYDROGEN-ION CONCENTRATION; ION CHANNEL GATING; ION CHANNELS; MEMBRANES; PROTEIN CONFORMATION; PROTONS; VIRAL MATRIX PROTEINS; WATER;

EID: 28844493428     PISSN: 09692126     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.str.2005.08.022     Document Type: Article

References (64)

1. E. Arbely, Z. Khattari, G. Brotons, M. Akkawi, T. Salditt, and I.T. Arkin A highly unusual palindromic transmembrane helical hairpin formed by SARS coronavirus E protein J. Mol. Biol. 341 2004 769 779
2. D. Bashford, and K. Gerwert Electrostatic calculations of the pKa values of ionizable groups in bacteriorhodopsin J. Mol. Biol. 224 1992 473 486
3. H.J.C. Berendsen, J.P.M. Postma, W.F. van Gunsteren, and J. Hermans Interaction models for water in relation to protein hydration B. Pullman Intermolecular Forces 1981 D. Reidel Publishing Company Dordrecht: The Netherlands 331 342
4. O. Berger, O. Edholm, and F. Jahnig Molecular dynamics simulations of a fluid bilayer of dipalmitoylphosphatidylcholine at full hydration, constant pressure, and constant temperature Biophys. J. 72 1997 2002 2013
5. M.L. Brewer, U.W. Schmitt, and G.A. Voth The formation and dynamics of proton wires in channel environments Biophys. J. 80 2001 1691 1702
6. S. Chanchevalap, Z. Yang, N. Cui, Z. Qu, G. Zhu, C. Liu, L.R. Giwa, L. Abdulkadir, and C. Jiang Involvement of histidine residues in proton sensing of ROMK1 channel J. Biol. Chem. 275 2000 7811 7817
7. I.V. Chizhmakov, F.M. Geraghty, D.C. Ogden, A. Hayhurst, M. Antoniou, and A.J. Hay Selective proton permeability and pH regulation of the influenza virus M2 channel expressed in mouse erythroleukaemia cells J. Physiol. 494 1996 329 336
8. I.V. Chizhmakov, D.C. Ogden, F.M. Geraghty, A. Hayhurst, A. Skinner, T. Betakova, and A.J. Hay Differences in conductance of M2 proton channels of two influenza viruses at low and high pH J. Physiol. 546 2003 427 438
9. T. Darden, D. York, and L. Pedersen Particle mesh Ewald: an N-log(N) method for Ewald sums in large systems J. Chem. Phys. 98 1993 10089 10092
10. B.L. de Groot, and H. Grubmuller Water permeation across biological membranes: mechanism and dynamics of aquaporin-1 and GlpF Science 294 2001 2353 2357
11. K.C. Duff, and R.H. Ashley The transmembrane domain of influenza A M2 protein forms amantadine-sensitive proton channels in planar lipid bilayers Virology 190 1992 485 489
12. K.C. Duff, S.M. Kelly, N.C. Price, and J.P. Bradshaw The secondary structure of influenza A M2 transmembrane domain. A circular dichroism study FEBS Lett. 311 1992 256 258
13. K.C. Duong-Ly, V. Nanda, W.F. Degrado, and K.P. Howard The conformation of the pore region of the M2 proton channel depends on lipid bilayer environment Protein Sci. 14 2005 856 861
14. J.D. Faraldo-Gomez, G.R. Smith, and M.S. Sansom Setting up and optimization of membrane protein simulations Eur. Biophys. J. 31 2002 217 227
15. L.R. Forrest, A. Kukol, I.T. Arkin, D.P. Tieleman, and M.S. Sansom Exploring models of the influenza A M2 channel: MD simulations in a phospholipid bilayer Biophys. J. 78 2000 55 69
16. A.J. Hay, A.J. Wolstenholme, J.J. Skehel, and M.H. Smith The molecular basis of the specific anti-influenza action of amantadine EMBO J. 4 1985 3021 3024
17. J. Hermans, H.J.C. Berendsen, W.F. van Gunsteren, and J.P.M. Postma A consistent empirical potential for water-protein interactions Biopolymers 23 1984 1513 1518
18. B. Hess, H. Bekker, H.J.C. Berendsen, and J.G.E.M. Fraaije LINCS: a linear constraint solver for molecular simulations J. Comp. Chem. 18 1997 1463 1472
19. L.J. Holsinger, M.A. Shaughnessy, A. Micko, L.H. Pinto, and R.A. Lamb Analysis of the posttranslational modifications of the influenza virus M2 protein J. Virol. 69 1995 1219 1225
20. W. Hoover Canonical dynamics - equilibrium phase-space distributions Phys. Rev. A. 31 1985 1695 1697
21. W. Humphrey, A. Dalke, and K. Schulten VMD: visual molecular dynamics J. Mol. Graph. 14 1996 33 38
22. T. Husslein, P.B. Moore, Q. Zhong, D.M. Newns, P.C. Pattnaik, and M.L. Klein Molecular dynamics simulation of a hydrated diphytanol phosphatidylcholine lipid bilayer containing an α-helical bundle of four transmembrane domains of the influenza A virus M2 protein Faraday Discuss. 111 1998 201 208
23. S. Kim, A.K. Chamberlain, and J.U. Bowie A simple method for modeling transmembrane helix oligomers J. Mol. Biol. 329 2003 831 840
24. F.A. Kovacs, and T.A. Cross Transmembrane four-helix bundle of influenza A M2 protein channel: structural implications from helix tilt and orientation Biophys. J. 73 1997 2511 2517
25. F.A. Kovacs, J.K. Denny, Z. Song, J.R. Quine, and T.A. Cross Helix tilt of the M2 transmembrane peptide from influenza A virus: an intrinsic property J. Mol. Biol. 295 2000 117 125
26. A. Kukol, P.D. Adams, L.M. Rice, A.T. Brunger, and T.I. Arkin Experimentally based orientational refinement of membrane protein models: a structure for the Influenza A M2 H+ channel J. Mol. Biol. 286 1999 951 962
27. J.D. Lear Proton conduction through the M2 protein of the influenza A virus; a quantitative, mechanistic analysis of experimental data FEBS Lett. 552 2003 17 22
28. T.I. Lin, and C. Schroeder Definitive assignment of proton selectivity and attoampere unitary current to the M2 ion channel protein of influenza A virus J. Virol. 75 2001 3647 3656
29. E. Lindahl, B. Hess, and D. van der Spoel GROMACS 3.0: a package for molecular simulation and trajectory analysis J. Mol. Mod. 7 2001 306 317
30. S. Lindskog Structure and mechanism of carbonic anhydrase Pharmacol. Ther. 74 1997 1 20
31. J.A. Mould, R.G. Paterson, M. Takeda, Y. Ohigashi, P. Venkataraman, R.A. Lamb, and L.H. Pinto Influenza B virus BM2 protein has ion channel activity that conducts protons across membranes Dev. Cell 5 2003 175 184
32. K. Nishimura, S. Kim, L. Zhang, and T.A. Cross The closed state of a H+ channel helical bundle combining precise orientational and distance restraints from solid state NMR Biochemistry 41 2002 13170 13177
33. S. Nose A molecular-dynamics method for simulations in the canonical ensemble Mol. Phys. 52 1984 255 268
34. S. Nose, and M. Klein Constant pressure molecular-dynamics for molecular-systems Mol. Phys. 50 1983 1055 1076
35. S.Y. Noskov, S. Berneche, and B. Roux Control of ion selectivity in potassium channels by electrostatic and dynamic properties of carbonyl ligands Nature 431 2004 830 834
36. A. Okada, T. Miura, and H. Takeuchi Protonation of histidine and histidine-tryptophan interaction in the activation of the M2 ion channel from influenza a virus Biochemistry 40 2001 6053 6060
37. B.J. Padanilam, T. Lu, T. Hoshi, B.A. Padanilam, E.F. Shibata, and H.C. Lee Molecular determinants of intracellular pH modulation of human Kv1.4 N-type inactivation Mol. Pharmacol. 62 2002 127 134
38. M. Parrinello, and A. Rahman Polymorphic transitions in single crystals: a new molecular dynamics method J. Appl. Phys. 52 1981 7182 7190
39. Persistence of Vision Raytracer Pty. Ltd. (2004). Persistence of Vision Raytracer (Version 3.6) (http://www.povray.org/).
40. L.H. Pinto, L.J. Holsinger, and R.A. Lamb Influenza virus M2 protein has ion channel activity Cell 69 1992 517 528
41. L.H. Pinto, G.R. Dieckmann, C.S. Gandhi, C.G. Papworth, J. Braman, M.A. Shaughnessy, J.D. Lear, R.A. Lamb, and W.F. DeGrado A functionally defined model for the M2 proton channel of influenza A virus suggests a mechanism for its ion selectivity Proc. Natl. Acad. Sci. USA 94 1997 11301 11306
42. T. Sakaguchi, Q. Tu, L.H. Pinto, and R.A. Lamb The active oligomeric state of the minimalistic influenza virus M2 ion channel is a tetramer Proc. Natl. Acad. Sci. USA 94 1997 5000 5005
43. M.S.P. Sansom, I.D. Kerr, G.R. Smith, and H.S. Son The influenza A virus M2 channel: a molecular modeling and simulation study Virology 233 1997 163 173
44. M.S. Sansom, D.P. Tieleman, L.R. Forrest, and H.J. Berendsen Molecular dynamics simulations of membranes with embedded proteins and peptides: porin, alamethicin and influenza virus M2 Biochem. Soc. Trans. 26 1998 438 443
45. U. Schmitt, and G. Voth Multistate empirical valence bond model for proton transport in water J. Phys. Chem. B 102 1998 5547 5551
46. U. Schmitt, and G. Voth Quantum properties of the excess proton in liquid water Isr. J. Chem. 39 1999 483 492
47. U.W. Schmitt, and G.A. Voth The computer simulation of proton transport in water J. Phys. Chem. 111 1999 9361 9381
48. O.S. Smart, J.G. Neduvelil, X. Wang, B.A. Wallace, and M.S. Sansom HOLE: a program for the analysis of the pore dimensions of ion channel structural models J. Mol. Graph. 14 1996 354 360
49. A.M. Smondyrev, and G.A. Voth Molecular dynamics simulation of proton transport through the influenza A virus M2 channel Biophys. J. 83 2002 1987 1996
50. Z. Song, F.A. Kovacs, J. Wang, J.K. Denny, S.C. Shekar, J.R. Quine, and T.A. Cross Transmembrane domain of M2 protein from influenza A virus studied by solid-state (15)N polarization inversion spin exchange at magic angle NMR Biophys. J. 79 2000 767 775
51. E.L. Sonnhammer, G. von Heijne, and A. Krogh A hidden Markov model for predicting transmembrane helices in protein sequences Proc. Int. Conf. Intell. Syst. Mol. Biol. 6 1998 175 182
52. R.J. Sugrue, and A.J. Hay Structural characteristics of the M2 protein of influenza A viruses: evidence that it forms a tetrameric channel Virology 180 1991 617 624
53. E. Tajkhorshid, P. Nollert, M.O. Jensen, L.J. Miercke, J. O'Connell, R.M. Stroud, and K. Schulten Control of the selectivity of the aquaporin water channel family by global orientational tuning Science 296 2002 525 530
54. H. Takeuchi, A. Okada, and T. Miura Roles of the histidine and tryptophan side chains in the M2 proton channel from influenza A virus FEBS Lett. 552 2003 35 38
55. J. Torres, and I.T. Arkin C-deuterated alanine: a new label to study membrane protein structure using site-specific infrared dichroism Biophys. J. 82 2002 1068 1075
56. J. Torres, A. Kukol, and I.T. Arkin Use of a single glycine residue to determine the tilt and orientation of a transmembrane helix. A new structural label for infrared spectroscopy Biophys. J. 79 2000 3139 3143
57. J. Torres, A. Kukol, J.M. Goodman, and I.T. Arkin Site-specific examination of secondary structure and orientation determination in membrane proteins: the peptidic (13)C=(18)O group as a novel infrared probe Biopolymers 59 2001 396 401
58. V. Vijayvergiya, R. Wilson, A. Chorak, P.F. Gao, T.A. Cross, and D.D. Busath Proton conductance of influenza virus M2 protein in planar lipid bilayers Biophys. J. 87 2004 1697 1704
59. C. Wang, R.A. Lamb, and L.H. Pinto Activation of the M2 ion channel of influenza virus: a role for the transmembrane domain histidine residue Biophys. J. 69 1995 1363 1371
60. J. Wang, S. Kim, F. Kovacs, and T.A. Cross Structure of the transmembrane region of the M2 protein H(+) channel Protein Sci. 10 2001 2241 2250
61. J. Warwicker, and H.C. Watson Calculation of the electric potential in the active site cleft due to alpha-helix dipoles J. Mol. Biol. 157 1982 671 679
62. H. Xu, J. Wu, N. Cui, L. Abdulkadir, R. Wang, J. Mao, L.R. Giwa, S. Chanchevalap, and C. Jiang Distinct histidine residues control the acid-induced activation and inhibition of the cloned K(ATP) channel J. Biol. Chem. 276 2001 38690 38696
63. Q. Zhong, T. Husslein, P.B. Moore, D.M. Newns, P. Pattnaik, and M.L. Klein The M2 channel of influenza A virus: a molecular dynamics study FEBS Lett. 434 1998 265 271
64. Q. Zhong, D.M. Newns, P. Pattnaik, J.D. Lear, and M.L. Klein Two possible conducting states of the influenza A virus M2 ion channel FEBS Lett. 473 2000 195 198