Molecular dynamics calculations suggest a conduction mechanism for the M2 proton channel from influenza A virus

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

Volumn 106, Issue 4, 2009, Pages 1069-1074

  Khurana, Ekta ^a,b   Dal Peraro, Matteo ^a,c   DeVane, Russell ^a   Vemparala, Satyavani ^d   DeGrado, William F ^a   Klein, Michael L ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b YALE UNIVERSITY   (United States)

^c EPFL   (Switzerland)

^d INSTITUTE OF MATHEMATICAL SCIENCES   (India)

Author keywords

His gate; Ion channel; pH activated; Simulations; Transporter

Indexed keywords

HISTIDINE; UNCLASSIFIED DRUG; VIRUS PROTEIN; VIRUS PROTEIN M2;

ARTICLE; BILAYER MEMBRANE; CONTROLLED STUDY; CRYSTAL STRUCTURE; INFLUENZA VIRUS A; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTON TRANSPORT; SIMULATION;

COMPUTER SIMULATION; CRYSTALLOGRAPHY, X-RAY; HYDROGEN-ION CONCENTRATION; INFLUENZA A VIRUS; ION CHANNEL GATING; ION CHANNELS; ION TRANSPORT; MODELS, MOLECULAR; PROTEIN CONFORMATION; PROTONS; VIRAL MATRIX PROTEINS;

INFLUENZA A VIRUS;

EID: 59049103481     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0811720106     Document Type: Article

References (40)

1. Lamb RA, Holsinger LJ, Pinto LH (1994) in Receptor-Mediated Virus Entry into Cell, ed Wimmer E (Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY), pp 303-321.
2. Salom D, Hill BR, Lear JD, DeGrado WF (2000) pH-dependent tetramerization and amantadine binding of the transmembrane helix of M2 from the influenza A virus. Biochemistry 39:14160-14170.
3. Nishimura K, Kim S, Zhang L, Cross TA (2002) The Closed State of a H+ Channel Helical Bundle Combining Precise Orientational and Distance Restraints from Solid State NMR. Biochemistry 41:13170-13177.
4. Hu J, et al. (2006) Histidines, heart of the hydrogen ion channel from influenza A virus: Toward an understanding of conductance and proton selectivity. Proc Natl Acad Sci USA 103:6865-6870.
5. Cady SD, Hong M (2008) Amantadine-induced conformational and dynamical changes of the influenza M2 transmembrane proton channel. Proc Natl Acad Sci USA 105:1483-1488.
6. Witter R, et al. (2008) Solid-state F-19 NMR spectroscopy reveals that Trp(41) participates in the gating mechanism of the M2 proton channel of influenza a virus. J Am Chem Soc 130:918-924.
7. Pinto LH, et al. (1997) A functionally defined model for the M-2 proton channel of influenza A virus suggests a mechanism for its ion selectivity. Proc Natl Acad Sci USA 94:11301-11306.
8. Wang J, Kim S, Kovacs F, Cross TA (2001) Structure of the transmembrane region of the M2 protein H+ channel. Protein Sci 10:2241-2250.
9. Cady SD, Goodman C, Tatko CD, DeGrado WF, Hong M (2007) Determining the Orientation of Uniaxially Rotating Membrane Proteins Using Unoriented Samples: A 2H, 13C, and 15N Solid-State NMR Investigation of the Dynamics and Orientation of a Transmembrane Helical Bundle. J Am Chem Soc 129:5719-5729.
10. Sansom MSP, Kerr ID, Smith GR, Son HS (1997) The influenza A virus M2 channel: A molecular modeling and simulation study. Virology 233:163-173.
11. Zhong QF, Newns DM, Pattnaik P, Lear JD, Klein ML (2000) Two possible conducting states of the influenza A virus M2 ion channel. FEBS Letters 473:195-198.
12. Zhong QF, et al. (1998) The M2 channel of influenza A virus: A molecular dynamics study. FEBS Lett 434:265-271.
13. Ayton GS, Voth GA (2007) Multiscale simulation of transmembrane proteins. J Struct Biol 157:570-578.
14. + channel: The gating mechanism of influenza A M2. Structure 13:1789-1798.
15. Chen HN, Wu YJ, Voth GA (2007) Proton transport Behavior through the influenza a M2 channel: Insights from molecular simulation. Biophys J 93:3470-3479.
16. Wu YJ, Voth GA (2005) A computational study of the closed and open states of the influenza A M2 proton channel. Biophys J 89:2402-2411.
17. Smondyrev AV, Voth GA (2002) Molecular Dynamics Simulation of Proton Transport through the Influenza A Virus M2 Channel. Biophys J 83:1987-1996.
18. Yi M, Cross TA, Zhou HX (2008) A secondary gate as a mechanism for inhibition of the M2 proton channel by amantadine. J Phys Chem B 112:7977-7979.
19. Schnell JR, Chou JJ (2008) Structure and mechanism of the M2 proton channel of influenza A virus. Nature 451:591-595.
20. Stouffer AL, et al. (2008) Structural basis for the function and inhibition of an influenza virus proton channel. Nature 451:596-599.
21. Pinto LH, Lamb RA (2006) Influenza virus proton channels. Photochem Photobiol Sci 5:629-632.
22. Mould JA, et al. (2000) Mechanism for proton conduction of the M-2 ion channel of influenza A virus. J Biol Chem 275:8592-8599.
23. Lin T-I, Schroeder C (2001) Definitive Assignment of Proton Selectivity and Attoampere Unitary Current to the M2 Ion Channel Protein of Influenza A Virus. J Virol 75:3647-3656.
24. Chizhmakov IV, et al. (2003) Differences in conductance of M2 proton channels of two influenza viruses at low and high pH. J Physiol-London 546:427-438.
25. Tang YJ, Zaitseva F, Lamb RA, Pinto LH (2002) The gate of the influenza virus M-2 proton channel is formed by a single tryptophan residue. J Biol Chem 277:39880-39886.
26. Kolocouris N, et al. (1996) Synthesis and antiviral activity evaluation of some new aminoadamantane derivatives. 2. J Med Chem 39:3307-3318.
27. Miller C (2008) Ion channels: Coughing up flu's proton channels. Nature 451:532-533.
28. Belshe RB, Smith MH, Hall CB, Betts R, Hay AJ (1988) Genetic-Basis of Resistance to Rimantadine Emerging During Treatment of Influenza-Virus Infection. J Virol 62:1508-1512.
29. Hay AJ, Zambon MC, Wolstenholme AJ, Skehel JJ, Smith MH (1986) Molecular-Basis of Resistance of Influenza-A Viruses to Amantadine. J Antimicrob Chemother 18:19-29.
30. Jing X, et al. (2008) Functional studies indicate amantadine binds to the pore of the influenza A virus M2 proton-selective ion channel. Proc Natl Acad Sci USA 105:10967-10972.
31. Humphrey W, Dalke A, Schulten K (1996) VMD-Visual Molecular Dynamics. J Mol Graph 14:33-38.
32. Phillips JC, et al. (2005) Scalable molecular dynamics with NAMD. J Comput Chem 26:1781-1802.
33. MacKerell AD, et al. (1998) All-Atom Empirical Potential for Molecular Modeling and Dynamics Studies of Proteins. J Phys Chem B 102:3586-3616.
34. Feller SE, Yin D, Pastor RW, MacKerell AD (1997) Molecular dynamics simulation of unsaturated lipid bilayers at low hydration: Parameterization and comparison with diffraction studies. Biophys J 73:2269-2279.
35. Jorgensen WL, Chandrasekhar J, Madura JD, Impey RW, Klein ML (1983) Comparison of simple potential functions for simulating liquid water. J Chem Phys 79:926-935.
36. Ryckaert JP, Ciccotti G, Berendson HJC (1977) Numerical integration of the cartesian equations of motion of a system with constraints: Molecular dynamics of n-alkanes. J Comput Phys 23:327-341.
37. Miyamoto S, Kollman PA (1992) SETTLE: An Analytical Version of the SHAKE and RATTLE Algorithm for Rigid Water Models. J Comput Chem 13:952-962.
38. Darden T, York D, Pedersen L (1993) Particle Mesh Ewald - an N. Log(N) Method for Ewald Sums in Large Systems. J Chem Phys 98:10089-10092.
39. Essmann U, et al. (1995)ASmooth Particle Mesh Ewald Method. J Chem Phys 103:8577-8593.
40. Smart OS, Goodfellow JM, Wallace BA (1993) The Pore Dimensions of Gramicidin A. Biophys J 65:2455-2460.