Mechanistic insight into the H2O/D2O isotope effect in the proton transport of the influenza virus M2 protein

Journal of Membrane Biology

Volumn 244, Issue 2, 2011, Pages 93-96

  Zhou, Huan Xiang ^a  

^a Florida State University   (United States)

Author keywords

Conductance mechanism; Drug resistance; Isotope effect; Proton channel

Indexed keywords

DEUTERIUM OXIDE; HISTIDINE; PROTEIN M2; SOLVENT; TRYPTOPHAN; VALINE; WATER;

ARTICLE; BINDING AFFINITY; BINDING SITE; DIFFUSION; INFLUENZA VIRUS; ION CONDUCTANCE; PKA; PROTON TRANSPORT; QUANTITATIVE ANALYSIS; THEORETICAL MODEL; VIRUS REPLICATION;

ANTIVIRAL AGENTS; DEUTERIUM OXIDE; DRUG DESIGN; HISTIDINE; HUMANS; HYDROGEN-ION CONCENTRATION; INFLUENZA A VIRUS; INFLUENZA, HUMAN; ION TRANSPORT; MODELS, MOLECULAR; MOLECULAR TARGETED THERAPY; PROTEIN STRUCTURE, TERTIARY; PROTONS; VIRAL MATRIX PROTEINS; WATER;

ORTHOMYXOVIRIDAE;

EID: 82955247980     PISSN: 00222631     EISSN: 14321424     Source Type: Journal    
DOI: 10.1007/s00232-011-9402-6     Document Type: Article

References (31)

1. R Acharya V Carnevale G Fiorin BG Levine AL Polishchuk V Balannik I Samish RA Lamb LH Pinto WF DeGrado ML Klein 2010 Structure and mechanism of proton transport through the transmembrane tetrameric M2 protein bundle of the influenza A virus Proc Natl Acad Sci USA 107 15075 15080 20689043 10.1073/pnas.1007071107 1:CAS:528:DC%2BC3cXhtFSmt7jO
2. M Akeson DW Deamer 1991 Proton conductance by the gramicidin water wire. Model for proton conductance in the F1F0 ATPases? Biophys J 60 101 109 1715764 10.1016/S0006-3495(91)82034-3 1:CAS:528:DyaK3MXks1Kqs7w%3D
3. 1H-NMR parameters of the common amino acid residues measured in aqueous solutions of the linear tetrapeptides H-Gly-Gly-X-L-Ala-OH Biopolymers 18 285 297 10.1002/bip.1979.360180206 1:CAS:528:DyaE1MXhvVOgsL0%3D
4. H Chen Y Wu GA Voth 2007 Proton transport behavior through the influenza A M2 channel: insights from molecular simulation Biophys J 93 3470 3479 17693473 10.1529/biophysj.107.105742 1:CAS:528:DC%2BD2sXht12jsrfI (Pubitemid 350190810)
5. A Chernyshev R Pomès S Cukierman 2003 Kinetic isotope effects of proton transfer in aqueous and methanol containing solutions, and in gramicidin A channels Biophys Chem 103 179 190 12568940 10.1016/S0301-4622(02)00255-7 1:CAS:528:DC%2BD3sXptFeqsA%3D%3D (Pubitemid 36140024)
6. IV Chizhmakov FM Geraghty DC Ogden A Hayhurst M Antoniou AJ Hay 1996 Selective proton permeability and pH regulation of the influenza virus M2 channel expressed in mouse erythroleukaemia cells J Physiol 494 Pt 2 329 336 8841994 1:CAS:528:DyaK28XkslWlurk%3D (Pubitemid 26318773)
7. IV Chizhmakov DC Ogden FM Geraghty A Hayhurst A Skinner T Betakova AJ Hay 2003 Differences in conductance of M2 proton channels of two influenza viruses at low and high pH J Physiol 546 427 438 12527729 10.1113/jphysiol.2002.028910 1:CAS:528:DC%2BD3sXitVWru7w%3D (Pubitemid 36175978)
8. TE DeCoursey VV Cherny 1997 Deuterium isotope effects on permeation and gating of proton channels in rat alveolar epithelium J Gen Physiol 109 415 434 9101402 10.1085/jgp.109.4.415 1:CAS:528:DyaK2sXisFyitL0%3D (Pubitemid 27164461)
9. L Gubareva M Okomo-Adhiambo V Deyde AM Fry TG Sheu R Garten C Smith J Barnes A Myrick M Hillman M Shaw C Bridges A Klimov N Cox 2009 Update: drug susceptibility of swine-origin influenza A (H1N1) viruses, April 2009 MMWR Morb Mortal Wkly Rep 58 433 435
10. J Hu R Fu K Nishimura L Zhang HX Zhou DD Busath V Vijayvergiya TA Cross 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 16632600 10.1073/pnas.0601944103 1:CAS:528: DC%2BD28XkslCks7c%3D
11. F Hu W Luo M Hong 2010 Mechanisms of proton conduction and gating in influenza M2 proton channels from solid-state NMR Science 330 505 508 20966251 10.1126/science.1191714 1:CAS:528:DC%2BC3cXhtlSjsb3E
12. E Khurana M Dal Peraro R DeVane S Vemparala WF DeGrado ML Klein 2009 Molecular dynamics calculations suggest a conduction mechanism for the M2 proton channel from influenza A virus Proc Natl Acad Sci USA 106 1069 1074 19144924 10.1073/pnas.0811720106 1:CAS:528:DC%2BD1MXhs1Whu7w%3D
13. JD Lear 2003 Proton conduction through the M2 protein of the influenza A virus; a quantitative, mechanistic analysis of experimental data FEBS Lett 552 17 22 12972146 10.1016/S0014-5793(03)00778-6 1:CAS:528:DC%2BD3sXntVCjtLY%3D
14. T Leiding J Wang J Martinsson WF DeGrado SP Arskold 2010 Proton and cation transport activity of the M2 proton channel from influenza A virus Proc Natl Acad Sci USA 107 15409 15414 20713739 10.1073/pnas.1009997107 1:CAS:528:DC%2BC3cXhtFaqurbF
15. 2O J Am Chem Soc 55 3504 3506 10.1021/ja01335a510
16. TI Lin C Schroeder 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 11264354 10.1128/JVI.75.8.3647-3656.2001 1:CAS:528: DC%2BD3MXisVSmsr4%3D (Pubitemid 32246374)
17. JA Mould H-C Li CS Dudlak JD Lear A Pekosz RA Lamb LH Pinto 2000 Mechanism for proton conduction of the M2 ion channel of influenza A virus J Biol Chem 275 8592 8599 10722698 10.1074/jbc.275.12.8592 1:CAS:528: DC%2BD3cXit1enu7c%3D (Pubitemid 30180208)
18. MI Nelson L Simonsen C Viboud MA Miller EC Holmes 2009 The origin and global emergence of adamantane resistant A/H3N2 influenza viruses Virology 388 270 278 19394063 10.1016/j.virol.2009.03.026 1:CAS:528:DC%2BD1MXlvF2qsLw%3D
19. E Peterson T Ryser S Funk D Inouye M Sharma H Qin TA Cross DD Busath 2011 Functional reconstitution of influenza A M2(22-62) Biochim Biophys Acta Biomembr 1808 516 521 10.1016/j.bbamem.2010.10.010 1:CAS:528:DC%2BC3cXhsFyltbzO
20. RM Pielak JJ Chou 2010 Kinetic analysis of the M2 proton conduction of the influenza virus J Am Chem Soc 132 17695 17697 21090748 10.1021/ja108458u 1:CAS:528:DC%2BC3cXhsVGkt7jJ
21. LH Pinto GR Dieckmann CS Gandhi CG Papworth J Braman MA Shaughnessy JD Lear RA Lamb WF DeGrado 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 9326604 10.1073/pnas.94.21.11301 1:CAS:528:DyaK2sXmslaqtLY%3D (Pubitemid 27450993)
22. AL Polishchuk JD Lear C Ma RA Lamb LH Pinto WF Degrado 2010 A pH-dependent conformational ensemble mediates proton transport through the influenza A/M2 protein Biochemistry 49 10061 10071 20968306 10.1021/bi101229m 1:CAS:528:DC%2BC3cXhtlOiu7fN
23. NK Roberts HL Northey 1974 Proton and deuteron mobility in normal and heavy water solutions of electrolytes J Chem Soc Faraday Trans I 70 253 262 10.1039/f19747000253 1:CAS:528:DyaE2cXktVKkurc%3D
24. MS Sansom ID Kerr GR Smith HS Son 1997 The influenza A virus M2 channel: a molecular modeling and simulation study Virology 233 163 173 9201226 10.1006/viro.1997.8578 1:CAS:528:DyaK2sXktlajtrw%3D (Pubitemid 27348778)
25. Schowen RL (1977) Solvent isotope effects on enzymic reactions. In: Cleland WW, O'Leary MH, Northop DB (eds) Isotope effects on enzyme-catalyzed reactions. University Park Press, Baltimore, pp 64-99
26. M Sharma M Yi H Dong H Qin E Peterson DD Busath HX Zhou TA Cross 2010 Insight into the mechanism of the influenza A proton channel from a structure in a lipid bilayer Science 330 509 512 20966252 10.1126/science.1191750 1:CAS:528:DC%2BC3cXhtlSjsb3F
27. P Venkataraman RA Lamb LH Pinto 2005 Chemical rescue of histidine selectivity filter mutants of the M2 ion channel of influenza A virus J Biol Chem 280 21463 21472 15784624 10.1074/jbc.M412406200 1:CAS:528: DC%2BD2MXks1eltr0%3D (Pubitemid 40805711)
28. M Yi TA Cross HX Zhou 2009 Conformational heterogeneity of the M2 proton channel and a structural model for channel activation Proc Natl Acad Sci USA 106 13311 13316 19633188 10.1073/pnas.0906553106 1:CAS:528:DC%2BD1MXhtVOitr%2FF
29. HX Zhou 2010 Diffusion-influenced transport of ions across a transmembrane channel with an internal binding site J Phys Chem Lett 1 1973 1976 20625440 10.1021/jz100683t 1:CAS:528:DC%2BC3cXntlCls74%3D
30. HX Zhou 2011 A theory for the proton transport of the influenza virus M2 protein: extensive test against conductance data Biophys. J. 100 912 921 21320435 10.1016/j.bpj.2011.01.002 1:CAS:528:DC%2BC3MXhvFKnsrg%3D
31. Zhou H-X, Szabo A (2012) Role of diffusion in the kinetics of reversible enzyme-catalyzed reactions. Bull Korean Chem Soc (to be published)