Evaluating how rimantadines control the proton gating of the influenza A M2-proton port via allosteric binding outside of the M2-channel: MD simulations

Journal of Enzyme Inhibition and Medicinal Chemistry

Volumn 26, Issue 2, 2011, Pages 162-168

  Intharathep, Pathumwadee ^a,b   Rungrotmongkol, Thanyada ^a   Decha, Panita ^c   Nunthaboot, Nadtanet ^d   Kaiyawet, Nopphorn ^a   Kerdcharoen, Teerakiat ^b   Sompornpisut, Pornthep ^a   Hannongbua, Supot ^a  

^a CHULALONGKORN UNIVERSITY   (Thailand)

^b Mahidol University ^*  (Thailand)

^c THAKSIN UNIVERSITY   (Thailand)

^d MAHASARAKHAM UNIVERSITY   (Thailand)

Author keywords

H1N1 strain; potential of means force; proton transport; protonation state

Indexed keywords

ASPARAGINE; PROTEIN M2; RIMANTADINE; TRYPTOPHAN;

ALLOSTERISM; ARTICLE; CHANNEL GATING; DRUG PROTEIN BINDING; INFLUENZA A; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTON TRANSPORT; WATER PERMEABILITY;

ALLOSTERIC REGULATION; DRUG DELIVERY SYSTEMS; ION CHANNEL GATING; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; NUCLEIC ACID SYNTHESIS INHIBITORS; PROTEIN BINDING; PROTEINS; PROTONS; RIMANTADINE; TRYPTOPHAN; VIRAL MATRIX PROTEINS;

EID: 79952770348     PISSN: 14756366     EISSN: 14756374     Source Type: Journal    
DOI: 10.3109/14756366.2010.482530     Document Type: Article

References (42)

1. WHO, Global Alert and Response (GAR), Online at: http://www. who.int/csr/disease/avian-infuenza/country/en/, accessed September 2009.
2. WHO, Global Alert and Response (GAR), Online at: http://www. who.int/csr/don/2009-10-09/en/index.html, accessed October 2009.
3. Helenius A. Unpacking the incoming infuenza-virus. Cell 1992;69: 577-578.
4. Ciampor F, Bayley PM, Nermut MV, Hirst EM, Sugrue RJ, Hay AJ. Evidence that the amantadine-induced, M2-mediated conversion of infuenza virus A hemagglutinin to the low pH conformation occurs in an acidic trans Golgi compartment. Virology 1992;188:14-24.
5. Lamb RA, Holsinger LJ, Pinto LH. In: Wimmer E, ed. Receptor-mediated Virus Entry into Cells. New York: Cold Spring Harbor Laboratory Press, 1994:303-321.
6. Hille B. Ionic Channels of Excitable Membranes. Sunderland, MA: Sinauer Associates, 2001.
7. Stoufer AL, Acharya R, Salom D, Levine AS, Di Costanzo L, Soto CS, Tereshko V, Nanda V, Stayrook S, DeGrado WF. Structural basis for the function and inhibition of an infuenza virus proton channel. Nature 2008;451:596-599. (Pubitemid 351186271)
8. Schnell JR, Chou JJ. Structure and mechanism of the M2 proton channel of infuenza A virus. Nature 2008;451:591-595. (Pubitemid 351186272)
9. Wang C, Takeuchi K, Pinto LH, Lamb RA. Ion channel activity of infuenza A virus M2 protein: Characterization of the amantadine block. J Virol 1993;67:5585-5594. (Pubitemid 23241395)
10. Salom D, Hill BR, Lear JD, DeGrado WF. pH-dependent tetramerization and amantadine binding of the transmembrane helix of M2 from the infuenza A virus. Biochemistry 2000;39:14160-14170.
11. Nishimura K, Kim S, Zhang L, Cross TA. Te closed state of a H+ channel helical bundle combining precise orientational and distance restraints from solid state NMR. Biochemistry 2002;41:13170-13177. (Pubitemid 35244706)
12. Hu J, Fu R, Nishimura K, Zhang L, Zhou HX, Busath DD, Vijayvergiya V, Cross TA. Histidines, heart of the hydrogen ion channel from infuenza A virus: Toward an understanding of conductance and proton selectivity. P Natl Acad Sci USA 2006;103:6865-6870.
13. Cady SD, Hong M. Amantadine-induced conformational and dynamical changes of the infuenza M2 transmembrane proton channel. P Natl Acad Sci USA 2008;105:1483-1488. (Pubitemid 351346540)
14. Witter R, Nozirov F, Sternberg U, Cross TA, Ulrich AS, Fu RQ. Solid-state F-19 NMR spectroscopy reveals that Trp(41) participates in the gating mechanism of the M2 proton channel of infuenza a virus. J Am Chem Soc 2008;130:918-924.
15. Pinto LH, Dieckmann GR, Gandhi CS, Papworth CG, Braman J, Shaughnessy MA, Lear JD, Lamb RA, DeGrado WF. A functionally defned model for the M-2 proton channel of infuenza A virus suggests a mechanism for its ion selectivity. P Natl Acad Sci USA 1997;94:11301-11306.
16. Wang JF, Kim S, Kovacs F, Cross TA. Structure of the transmembrane region of the M2 protein H+ channel. Protein Sci 2001;10:2241-2250. (Pubitemid 32988641)
17. Cady SD, Goodman C, Tatko CD, DeGrado WF, Hong M. Determining the orientation of uniaxially rotating membrane proteins using unoriented samples: A H-2, C-13, and N-15 solid-state NMR investigation of the dynamics and orientation of a transmembrane helical bundle. J Am Chem Soc 2007;129:5719-5729. (Pubitemid 46697663)
18. Sansom MSP, Kerr ID, Smith GR, Son HS. Te infuenza A virus M2 channel: A molecular modeling and simulation study. Virology 1997;233:163-173. (Pubitemid 27348778)
19. Zhong QF, Newns DM, Pattnaik P, Lear JD, Klein ML. Two possible conducting states of the infuenza A virus M2 ion channel. Febs Lett 2000;473:195-198. (Pubitemid 30254289)
20. Zhong QF, Husslein T, Moore PB, Newns DM, Pattnaik P, Klein ML. Te M2 channel of infuenza A virus: a molecular dynamics study. Febs Lett 1998;434:265-271. (Pubitemid 29052238)
21. Ayton GS, Voth GA. Multiscale simulation of transmembrane proteins. J Struct Biol 2007;157:570-578.
22. Kass I, Arkin IT How pH opens a H+ channel: Te gating mechanism of infuenza a M2. Structure 2005;13:1789-1798. (Pubitemid 41772947)
23. Chen HN, Wu YJ, Voth GA. Proton transport Behavior through the infuenza a M2 channel: Insights from molecular simulation. Biophys J 2007;93:3470-3479. (Pubitemid 350190810)
24. Wu YJ, Voth GA. A computational study of the closed and open states of the infuenza A M2 proton channel. Biophys J 2005;89:2402-2411. (Pubitemid 41401030)
25. Smondyrev AM, Voth GA. Molecular dynamics simulation of proton transport through the infuenza A virus M2 channel. Biophys J 2002;83:1987-1996.
26. Yi M, Cross TA, Zhou HX. A secondary gate as a mechanism for inhibition of the M2 proton channel by amantadine. J Phys Chem B 2008;112:7977-7979.
27. Hay AJ, Wolstenholme AJ, Skehel JJ, Smith HH. Te molecular basis of the specifc anti-infuenza action of amantadine. EMBO J 1985;4: 3021-3024.
28. Intharathep P, Laohpongspaisan C, Rungrotmongkol T, Loisruangsin A, Malaisree M, Decha P, Aruksakunwong O, Chuenpennit K, Kaiyawet N, Sompornpisut P, Pianwanit S, Hannongbu S. How amantadine and rimantadine inhibit proton transport in the M2 protein channel. J Mol Graph Model 2008;27:342-348.
29. Huang RB, Du QS, Wang CH, Chou KC. An in-depth analysis of the biological functional studies based on the NMR M2 channel structure of infuenza A virus. Biochim Bioph Res Commun 2008;377:1243-1247.
30. Jing XH, Ma CL, Ohigashi Y Oliveira FA, Jardetzky TS, Pinto LH, Lamb RA. Functional studies indicate amantadine binds to the pore of the infuenza A virus M2 proton-selective ion channel. P Natl Acad Sci USA 2008;105:10967-10972.
31. Cady S, Schmidt-Rohr K, Wang J, Soto C, DeGrado W, Hong M. Structure of the amantadine binding site of infuenza M2 proton channels in lipid bilayers. Nature 2010;463:689-692.
32. Ma C, Polishchuk A, Ohigashi Y Stoufer A, Schön A, Magavern E, Jing X, Lear J, Freire E, Lamb R, DeGrado d, Pinto L. Identifcation of the functional core of the infuenza A virus A/M2 proton-selective ion channel. Proc Natl Acad Sci USA. 2009;106:12283-12288.
33. Spector R. Transport of amantadine and rimantadine through the blood-brain barrier. J Pharm Exp Ter 1988;244:516-519. (Pubitemid 18076589)
34. Forrest LR, Tieleman DP, Sansom MSP. Defning the transmembrane helix of M2 protein from infuenza A by molecular dynamics simulations in a lipid bilayer. Biophys J 1999;76:1886-1896. (Pubitemid 29266345)
35. Berendsen HJC, Postma JPM, van Gunsteren WF, Hermans J. Intermolecular Forces. In: Pullman B, ed. Dordrecht Te Netherlands: D. Reidel Publishing Company, 1981. pp. 331-342.
36. Lindahl E, Hess B, Spoel Dvd. GROMACS 3.0: a package for molecular simulation and trajectory analysis. J Mol Model 2001;7:306-317. (Pubitemid 36153547)
37. Hermans J, Berendsen HJC, van Gunsteren WF, Postma JPM. A consistent empirical potential for water-protein interactions. Biopolymers 1984;23:1513-1518.
38. Rungrotmongkol T, Intharathep P, Malaisree M, Nunthaboot N, Kaiyawet N, Sompornpisut P, Payungporn S, Poovorawan Y Hannongbua S. Susceptibility of antiviral drugs against 2009 infuenza A (H1N1) virus. Biochem Bioph Res Co 2009;385:390-394.
39. Hess B, Bekker H, Berendsen HJC, Fraaije JGEM. LINCS: a linear constraint solver for molecular simulations. J Comp Chem 1997;18:1463-1472. (Pubitemid 127637344)
40. Berendsen HJC, Postma JPM, van Gunsteren WF, DiNola A, Haak JR. Molecular dynamics with coupling to an external bath. J Chem Phys 1984;81:3684-3690.
41. Darden T, York D, Pedersen L. Particle mesh Ewald: an N-log(N) method for Ewald sums in large systems. J Chem Phys 1993;98:10089-10092.
42. Raschke TM, Levitt M. Detailed hydration maps of benzene and cyclohexane reveal distinct water structures. J Phys Chem B 2004;108:13492-13500.