Structural and energetic analysis of drug inhibition of the influenza A M2 proton channel

Trends in Pharmacological Sciences

Volumn 34, Issue 10, 2013, Pages 571-580

  Gu, Ruo Xu ^a   Liu, Limin Angela ^b   Wei, Dong Qing ^a  

^a SHANGHAI JIAO TONG UNIVERSITY   (China)

^b Fred Hutchinson Cancer Research Center   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3 AZASPIRO[5.5]UNDECANE; ADAMANTANE DERIVATIVE; AMANTADINE; ANTIVIRUS AGENT; BL 1743; INFLUENZA A M2 PROTON CHANNEL; INFLUENZA A M2 PROTON CHANNEL INHIBITOR; INFLUENZA A VIRUS MATRIX PROTEIN 2; ION CHANNEL; LIGAND; M2WJ332 LIGAND; MATRIX PROTEIN; MOLECULAR SCAFFOLD; RIMANTADINE; SPIRO[5.5]UNDECAN 3 AMINE; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; BINDING AFFINITY; DRUG BINDING SITE; DRUG DESIGN; DRUG FORMULATION; DRUG INHIBITION; DRUG POTENCY; DRUG PROTEIN BINDING; DRUG STRUCTURE; DRUG TARGETING; ENERGY TRANSFER; HYDROGEN BOND; HYDROPHOBICITY; INFLUENZA VIRUS A; MOLECULAR DYNAMICS; MOLECULAR MODEL; NONHUMAN; PRIORITY JOURNAL; PROTEIN DATA BANK; PROTON TRANSPORT; REVIEW; STRUCTURE ANALYSIS; VIRUS RESISTANCE;

EID: 84885185774     PISSN: 01656147     EISSN: 18733735     Source Type: Journal    
DOI: 10.1016/j.tips.2013.08.003     Document Type: Review

References (73)

1. S.D. Cady Structure and function of the influenza A M2 proton channel Biochemistry 48 2009 7356 7364
2. L.H. Pinto, and R.A. Lamb Influenza virus proton channels Photochem. Photobiol. Sci. 5 2006 629 632
3. L.H. Pinto, and R.A. Lamb The M2 proton channels of influenza A and B viruses J. Biol. Chem. 281 2006 8997 9000
4. J. Wang Structural and dynamic mechanisms for the function and inhibition of the M2 proton channel from influenza A virus Curr. Opin. Struct. Biol. 21 2011 68 80
5. K. Das Antivirals targeting influenza A virus J. Med. Chem. 55 2012 6263 6277
6. J. Du Recent progress in structure-based anti-influenza drug design Drug Discov. Today 17 2012 1111 1120
7. I. Chizhmakov Selective proton permeability and pH regulation of the influenza virus M2 channel expressed in mouse erythroleukaemia cells J. Physiol. 494 1996 329 336
8. L.J. Holsinger Influenza A virus M2 ion channel protein: a structure-function analysis J. Virol. 68 1994 1551 1563
9. C. Wang Ion channel activity of influenza A virus M2 protein: characterization of the amantadine block J. Virol. 67 1993 5585 5594
10. T. Sakaguchi The active oligomeric state of the minimalistic influenza virus M2 ion channel is a tetramer Proc. Natl. Acad. Sci. U.S.A. 94 1997 5000 5005
11. R.A. Lamb Influenza virus M2 protein is an integral membrane protein expressed on the infected-cell surface Cell 40 1985 627 633
12. J.R. Schnell, and J.J. Chou Structure and mechanism of the M2 proton channel of influenza A virus Nature 451 2008 591 595
13. A.L. Stouffer Structural basis for the function and inhibition of an influenza virus proton channel Nature 451 2008 596 599
14. M. Yi A secondary gate as a mechanism for inhibition of the M2 proton channel by amantadine J. Phys. Chem. B 112 2008 7977 7979
15. R-X. Gu Free energy calculations on the two drug binding sites in the M2 proton channel J. Am. Chem. Soc. 133 2011 10817 10825
16. P. Venkataraman Chemical rescue of histidine selectivity filter mutants of the M2 ion channel of influenza A virus J. Biol. Chem. 280 2005 21463 21472
17. Y. Tang The gate of the influenza virus M2 proton channel is formed by a single tryptophan residue J. Biol. Chem. 277 2002 39880 39886
18. F. Hu Mechanisms of proton conduction and gating in influenza M2 proton channels from solid-state NMR Science 330 2010 505 508
19. J. Hu Backbone structure of the amantadine-blocked trans-membrane domain M2 proton channel from influenza A virus Biophys. J. 92 2007 4335 4343
20. J. Hu The chemical and dynamical influence of the anti-viral drug amantadine on the M2 proton channel transmembrane domain Biophys. J. 93 2007 276 283
21. E. Khurana Molecular dynamics calculations suggest a conduction mechanism for the M2 proton channel from influenza A virus Proc. Natl. Acad. Sci. U.S.A. 106 2009 1069 1074
22. R.M. Pielak, and J.J. Chou Kinetic analysis of the M2 proton conduction of the influenza virus J. Am. Chem. Soc. 132 2010 17695 17697
23. M. Sharma Insight into the mechanism of the influenza A proton channel from a structure in a lipid bilayer Science 330 2010 509 512
24. M. Yi Conformational heterogeneity of the M2 proton channel and a structural model for channel activation Proc. Natl. Acad. Sci. U.S.A. 106 2009 13311 13316
25. H. Chen Proton transport behavior through the influenza A M2 channel: insights from molecular simulation Biophys. J. 93 2007 3470 3479
26. A. Okada Protonation of histidine and histidine-tryptophan interaction in the activation of the M2 ion channel from influenza A virus Biochemistry 40 2001 6053 6060
27. J.A. Mould Mechanism for proton conduction of the M2 ion channel of influenza A virus J. Biol. Chem. 275 2000 8592 8599
28. L.H. Pinto A functionally defined model for the M2 proton channel of influenza A virus suggests a mechanism for its ion selectivity Proc. Natl. Acad. Sci. U.S.A. 94 1997 11301 11306
29. M. Sansom The influenza A virus M2 channel: a molecular modeling and simulation study Virology 233 1997 163 173
30. M. Hong, and W.F. DeGrado Structural basis for proton conduction and inhibition by the influenza M2 protein Protein Sci. 21 2012 1620 1633
31. H.X. Zhou, and T.A. Cross Modeling the membrane environment has implications for membrane protein structure and function: influenza A M2 protein Protein Sci. 22 2013 381 394
32. G.G. Kochendoerfer Total chemical synthesis of the integral membrane protein influenza A virus M2: role of its C-terminal domain in tetramer assembly Biochemistry 38 1999 11905 11913
33. C. Ma Identification of the functional core of the influenza A virus A/M2 proton-selective ion channel Proc. Natl. Acad. Sci. U.S.A. 106 2009 12283 12288
34. J.S. Rossman Influenza virus m2 ion channel protein is necessary for filamentous virion formation J. Virol. 84 2010 5078 5088
35. J.S. Rossman, and R.A. Lamb Influenza virus assembly and budding Virology 411 2011 229 236
36. T. Leiding Proton and cation transport activity of the M2 proton channel from influenza A virus Proc. Natl. Acad. Sci. U.S.A. 107 2010 15409 15414
37. 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
38. J.C. Moffat Proton transport through influenza A virus M2 protein reconstituted in vesicles Biophys. J. 94 2008 434 445
39. T.A. Cross M2 protein from influenza A: from multiple structures to biophysical and functional insights Curr. Opin. Virol. 2 2012 128 133
40. T.A. Cross Influence of solubilizing environments on membrane protein structures Trends Biochem. Sci. 36 2011 117 125
41. J. Wang Structure and inhibition of the drug-resistant S31N mutant of the M2 ion channel of influenza A virus Proc. Natl. Acad. Sci. U.S.A. 110 2013 1315 1320
42. R. Acharya Structure and mechanism of proton transport through the transmembrane tetrameric M2 protein bundle of the influenza A virus Proc. Natl. Acad. Sci. U.S.A. 107 2010 15075 15080
43. S.D. Cady Structure of the amantadine binding site of influenza M2 proton channels in lipid bilayers Nature 463 2010 689 692
44. M.R. Rosenberg, and M.G. Casarotto Coexistence of two adamantane binding sites in the influenza A M2 ion channel Proc. Natl. Acad. Sci. U.S.A. 107 2010 13866 13871
45. X. Jing Functional studies indicate amantadine binds to the pore of the influenza A virus M2 proton-selective ion channel Proc. Natl. Acad. Sci. U.S.A. 105 2008 10967 10972
46. Y. Ohigashi An amantadine-sensitive chimeric BM2 ion channel of influenza B virus has implications for the mechanism of drug inhibition Proc. Natl. Acad. Sci. U.S.A. 106 2009 18775 18779
47. G-Y. Chuang Binding hot spots and amantadine orientation in the influenza A virus M2 proton channel Biophys. J. 97 2009 2846 2853
48. R. Brenke Fragment-based identification of druggable 'hot spots' of proteins using Fourier domain correlation techniques Bioinformatics 25 2009 621 627
49. D. Kozakov Where does amantadine bind to the influenza virus M2 proton channel? Trends Biochem. Sci. 35 2010 471 475
50. E. Khurana Computational study of drug binding to the membrane-bound tetrameric M2 peptide bundle from influenza A virus Biochem. Biophys. Acta 1808 2011 530 537
51. C.F. Chew Distribution and dynamics of adamantanes in a lipid bilayer Biophys. J. 95 2008 5627 5636
52. V. Balannik Design and pharmacological characterization of inhibitors of amantadine-resistant mutants of the M2 ion channel of influenza A virus Biochemistry 48 2009 11872 11882
53. J. Wang Discovery of spiro-piperidine inhibitors and their modulation of the dynamics of the M2 proton channel from influenza A virus J. Am. Chem. Soc. 131 2009 8066 8076
54. R.M. Pielak Structural investigation of rimantadine inhibition of the AM2-BM2 chimera channel of influenza viruses Structure 19 2011 1655 1663
55. R-X. Gu Structural comparison of the wild-type and drug-resistant mutants of the influenza A M2 proton channel by molecular dynamics simulations J. Phys. Chem. B 117 2013 6042 6051
56. P.E. Aldrich Antiviral agents. 2. Structure-activity relations of compounds related to 1-adamantanamine J. Med. Chem. 14 1971 535 543
57. A. Kolocouris Synthesis of 2-(2-adamantyl) piperidines and structure anti-influenza virus A activity relationship study using a combination of NMR spectroscopy and molecular modeling Bioorg. Med. Chem. Lett. 9 1999 3465 3470
58. J. Wang Molecular dynamics simulation directed rational design of inhibitors targeting drug-resistant mutants of influenza A virus M2 J. Am. Chem. Soc. 133 2011 12834 12841
59. V.M. Deyde Surveillance of resistance to adamantanes among influenza A (H3N2) and A (H1N1) viruses isolated worldwide J. Infect. Dis. 196 2007 249 257
60. R. Saito Frequency of amantadine-resistant influenza A viruses during two seasons featuring cocirculation of H1N1 and H3N2 J. Clin. Mircobiol. 41 2003 2164 2165
61. P. Gkeka Free energy calculations reveal the origin of binding preference for aminoadamantane blockers of influenza A/M2TM pore J. Chem. Theory Comput. 9 2012 1272 1281
62. M.D. Duque Inhibitors of the M2 channel of influenza A virus D. Muñoz-Torrero, Recent Advances in Pharmaceutical Sciences 2011 Transworld Research Network 35 64
63. J. Wang Exploring the requirements for the hydrophobic scaffold and polar amine in inhibitors of M2 from influenza A virus ACS Med. Chem. Lett. 2 2011 307 312
64. Q.S. Du Designing inhibitors of M2 proton channel against H1N1 swine influenza virus PLoS ONE 5 2010 e9388
65. M.D. Duque Exploring the size limit of templates for inhibitors of the M2 ion channel of influenza A virus J. Med. Chem. 54 2011 2646 2657
66. W. Hu Identification of hits as matrix-2 protein inhibitors through the focused screening of a small primary amine library J. Med. Chem. 53 2010 3831 3834
67. S. Kurtz Growth impairment resulting from expression of influenza virus M2 protein in Saccharomyces cerevisiae: identification of a novel inhibitor of influenza virus Antimicrob. Agents Chemother. 39 1995 2204 2209
68. J. Wang Discovery of novel dual inhibitors of wild-type and the most prevalent drug-resistant mutant, S31N, of M2 proton channel from influenza A virus J. Med. Chem. 56 2013 2804 2812
69. O.S. Smart HOLE: a program for the analysis of the pore dimensions of ion channel structural models J. Mol. Graph. 14 1996 354 360
70. + channel helical bundle combining precise orientational and distance restraints from solid state NMR Biochemistry 41 2002 13170 13177
71. S.D. Cady Structure of amantadine-bound M2 transmembrane peptide of influenza A in lipid bilayers from magic-angle-spinning solid-state NMR: the role of Ser31 in amantadine binding J. Mol. Biol. 385 2009 1127 1141
72. R.M. Pielak Mechanism of drug inhibition and drug resistance of influenza A M2 channel Proc. Natl. Acad. Sci. U.S.A. 106 2009 7379 7384
73. R.M. Pielak, and J.J. Chou Solution NMR structure of the V27A drug resistant mutant of influenza A M2 channel Biochem. Biophys. Res. Commun. 401 2010 58 63