The Interplay of Functional Tuning, Drug Resistance, and Thermodynamic Stability in the Evolution of the M2 Proton Channel from the Influenza A Virus

Structure

Volumn 16, Issue 7, 2008, Pages 1067-1076

  Stouffer, Amanda L ^a   Ma, Chunlong ^b   Cristian, Lidia ^a   Ohigashi, Yuki ^b   Lamb, Robert A ^b   Lear, James D ^a   Pinto, Lawrence H ^b   DeGrado, William F ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

Author keywords

MICROBIO; PROTEINS

Indexed keywords

AMANTADINE; CATION CHANNEL; DISULFIDE; ION CHANNEL; MEMBRANE PROTEIN; PROTEIN M2; THIOL;

ALLOSTERISM; AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; BINDING SITE; CONTROLLED STUDY; DRUG BINDING SITE; DRUG RESISTANCE; DRUG SENSITIVITY; ELECTROPHYSIOLOGY; FEMALE; INFLUENZA VIRUS A; LIPID VESICLE; MICELLE; MUTATIONAL ANALYSIS; NONHUMAN; OOCYTE; PHOSPHOLIPID BILAYER; PRIORITY JOURNAL; THERMODYNAMICS; THERMOSTABILITY;

AMANTADINE; AMINO ACID SEQUENCE; ANIMALS; ANTIVIRAL AGENTS; CELLS, CULTURED; DISULFIDES; DRUG RESISTANCE, VIRAL; EVOLUTION, MOLECULAR; ION CHANNELS; LIPID BILAYERS; MICELLES; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; PATCH-CLAMP TECHNIQUES; PHOSPHOLIPIDS; PROTONS; THERMODYNAMICS; VIRAL MATRIX PROTEINS; XENOPUS LAEVIS;

INFLUENZA A VIRUS;

EID: 46049110693     PISSN: 09692126     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.str.2008.04.011     Document Type: Article

References (59)

1. Abed Y., Goyette N., and Boivin G. Generation and characterization of recombinant influenza A (H1N1) viruses harboring amantadine resistance mutations. Antimicrob. Agents Chemother. 49 (2005) 556-559
2. Betakova T., Ciampor F., and Hay A.J. Influence of residue 44 on the activity of the M2 proton channel of influenza A virus. J. Gen. Virol. 86 (2005) 181-184
3. Beumer T.L., Veenstra G.J., Hage W.J., and Destree O.H. Whole-mount immunohistochemistry on Xenopus embryos using far-red fluorescent dyes. Trends Genet. 11 (1995) 9
4. Bowie J.U. Stabilizing membrane proteins. Curr. Opin. Struct. Biol. 11 (2001) 397-402
5. Bowie J.U. Membrane proteins: a new method enters the fold. Proc. Natl. Acad. Sci. USA 101 (2004) 3995-3996
6. Bright R.A., Medina M.J., Xu X.Y., Perez-Oronoz G., Wallis T.R., Davis X.H.M., Povinelli L., Cox N.J., and Klimov A.I. Incidence of adamantane resistance among influenza A (H3N2) viruses isolated worldwide from 1994 to 2005: a cause for concern. Lancet 366 (2005) 1175-1181
7. Bright R.A., Shay D.K., Shu B., Cox N.J., and Klimov A.I. Adamantane resistance among influenza A viruses isolated early during the 2005-2006 influenza season in the United States. JAMA 295 (2006) 891-894
8. Chen H., Wu Y., and Voth G.A. Proton transport behavior through the influenza A M2 channel: insights from molecular simulation. Biophys. J. 93 (2007) 3470-3479
9. Chizhmakov I.V., Geraghty F.M., Ogden D.C., Hayhurst A., Antoniou M., and Hay A.J. Selective proton permeability and pH regulation of the influenza virus M2 channel expressed in mouse erythroleukaemia cells. J. Physiol. 494 (1996) 329-336
10. Chizhmakov I.V., Ogden D.C., Geraghty F.M., Hayhurst A., Skinner A., Betakova T., and Hay A.J. Differences in conductance of M2 proton channels of two influenza viruses at low and high pH. J. Physiol. 546 (2003) 427-438
11. Choma C., Gratkowski H., Lear J.D., and DeGrado W.F. Asparagine-mediated self-association of a model transmembrane helix. Nat. Struct. Biol. 7 (2000) 161-166
12. Ciampor F., Thompson C.A., Grambas S., and Hay A.J. Regulation of pH by the M2 protein of influenza A viruses. Virus Res. 22 (1992) 247-258
13. Cristian L., Lear J.D., and DeGrado W.F. Determination of membrane protein stability via thermodynamic coupling of folding to thiol-disulfide interchange. Protein Sci. 12 (2003) 1732-1740
14. Cristian L., Lear J.D., and DeGrado W.F. Use of thiol-disulfide equilibria to measure the energetics of assembly of transmembrane helices in phospholipid bilayers. Proc. Natl. Acad. Sci. USA 100 (2003) 14772-14777
15. Czabotar P.E., Martin S.R., and Hay A.J. Studies of structural changes in the M2 proton channel of influenza A virus by tryptophan fluorescence. Virus Res. 99 (2004) 57-61
16. Deyde V.M., Xu X., Bright R.A., Shaw M., Smith C.B., Zhang Y., Shu Y., Gubareva L.V., Cox N.J., and Klimov A.I. Surveillance of resistance to adamantanes among influenza A(H3N2) and A(H1N1) viruses isolated worldwide. J. Infect. Dis. 196 (2007) 249-257
17. Fernandez C., Hilty C., Wider G., and Wuthrich K. Lipid-protein interactions in DHPC micelles containing the integral membrane protein OmpX investigated by NMR spectroscopy. Proc. Natl. Acad. Sci. USA 99 (2002) 13533-13537
18. Fisher L.E., Engelman D.M., and Sturgis J.N. Detergents modulate dimerization, but not helicity, of the glycophorin A transmembrane domain. J. Mol. Biol. 293 (1999) 639-651
19. Fleming K.G., and Engelman D.M. Specificity in transmembrane helix-helix interactions can define a hierarchy of stability for sequence variants. Proc. Natl. Acad. Sci. USA 98 (2001) 14340-14344
20. Fleming K.G., Ackerman A.L., and Engelman D.M. The effect of point mutations on the free energy of transmembrane α-helix dimerization. J. Mol. Biol. 272 (1997) 266-275
21. Fleming K.G., Ren C.C., Doura A.K., Eisley M.E., Kobus F.J., and Stanley A.M. Thermodynamics of glycophorin A transmembrane helix dimerization in C14 betaine micelles. Biophys. Chem. 108 (2004) 43-49
22. Gandhi C.S., Shuck K., Lear J.D., Dieckmann G.R., DeGrado W.F., Lamb R.A., and Pinto L.H. Cu(II) inhibition of the proton translocation machinery of the influenza A virus M2 protein. J. Biol. Chem. 274 (1999) 5474-5482
23. Grambas S., Bennett M.S., and Hay A.J. Influence of amantadine resistance mutations on the pH regulatory function of the M2 protein of influenza A viruses. Virology 191 (1992) 541-549
24. Gratkowski H., Lear J.D., and DeGrado W.F. Polar side chains drive the association of model transmembrane peptides. Proc. Natl. Acad. Sci. USA 98 (2001) 880-885
25. Hayden F.G. Antiviral resistance in influenza viruses-implications for management and pandemic response. N. Engl. J. Med. 354 (2006) 785-788
26. Hilty C., Wider G., Fernandez C., and Wuthrich K. Membrane protein-lipid interactions in mixed micelles studied by NMR spectroscopy with the use of paramagnetic reagents. ChemBioChem 5 (2004) 467-473
27. Holsinger L.J., and Lamb R.A. Influenza virus M2 integral membrane protein is a homotetramer stabilized by formation of disulfide bonds. Virology 183 (1991) 32-43
28. Holsinger L.J., Nichani D., Pinto L.H., and Lamb R.A. Influenza A virus M2 ion channel protein: a structure-function analysis. J. Virol. 68 (1994) 1551-1563
29. Howard K.P., Lear J.D., and DeGrado W.F. Sequence determinants of the energetics of folding of a transmembrane four-helix-bundle protein. Proc. Natl. Acad. Sci. USA 99 (2002) 8568-8572
30. Hu J., Asbury T., Achuthan S., Li C., Bertram R., Quine J.R., Fu R., and Cross T.A. Backbone structure of the amantadine-blocked trans-membrane domain M2 proton channel from influenza A virus. Biophys. J. 92 (2007) 4335-4343
31. Kitahori Y., Nakano M., and Inoue Y. Frequency of amantadine-resistant influenza A virus isolated from 2001-02 to 2004-05 in Nara Prefecture. Jpn. J. Infect. Dis. 59 (2006) 197-199
32. Lamb R.A., Holsinger L.J., and Pinto L.H. The influenza A virus M2 ion channel protein and its role in the influenza virus life cycle. In: Wimmer E. (Ed). Cellular Receptors and Animal Viruses (1994), Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY 303-321
33. Lear J.D., Gratkowski H., Adamian L., Liang J., and DeGrado W.F. Position-dependence of stabilizing polar interactions of asparagine in transmembrane helical bundles. Biochemistry 42 (2003) 6400-6407
34. Lin T.I., and Schroeder C. 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
35. Lin T.-I., Heider H., and Schroeder C. Different modes of inhibition by adamantane amine derivatives and natural polyamines of the functionally reconstituted influenza virus M2 proton channel protein. J. Gen. Virol. 78 (1997) 767-774
36. Mould J.A., Drury J.E., Frings S.M., Kaupp U.B., Pekosz A., Lamb R.A., and Pinto L.H. Permeation and activation of the M2 ion channel of influenza A virus. J. Biol. Chem. 275 (2000) 31038-31050
37. + channel helical bundle combining precise orientational and distance restraints from solid state NMR. Biochemistry 41 (2002) 13170-13177
38. Okada A., Miura T., and Takeuchi H. Protonation of histidine and histidine-tryptophan interaction in the activation of the M2 ion channel from influenza A virus. Biochemistry 40 (2001) 6053-6060
39. Pinto L.H., and Lamb R.A. The M2 proton channels of influenza A and B viruses. J. Biol. Chem. 281 (2006) 8997-9000
40. Pinto L.H., Dieckmann G.R., Gandhi C.S., Papworth C.G., Braman J., Shaughnessy M.A., Lear J.D., Lamb R.A., and DeGrado W.F. 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
41. Russ W.P., and Engelman D.M. TOXCAT: a measure of transmembrane helix association in a biological membrane. Proc. Natl. Acad. Sci. USA 96 (1999) 863-868
42. Russ W.P., and Engelman D.M. The GxxxG motif: a framework for transmembrane helix-helix association. J. Mol. Biol. 296 (2000) 911-919
43. Salom D., Hill B.R., Lear J.D., and DeGrado W.F. pH-dependent tetramerization and amantadine binding of the transmembrane helix of M2 from the influenza A virus. Biochemistry 39 (2000) 14160-14170
44. Schnell J.R., and Chou J.J. Structure and mechanism of the M2 proton channel of influenza A virus. Nature 451 (2008) 591-595
45. Senes A., Gerstein M., and Engelman D.M. Statistical analysis of amino acid patterns in transmembrane helices: the GxxxG motif occurs frequently and in association with β-branched residues at neighboring positions. J. Mol. Biol. 296 (2000) 921-936
46. Senes A., Engel D.E., and DeGrado W.F. Folding of helical membrane proteins: the role of polar, GxxxG-like and proline motifs. Curr. Opin. Struct. Biol. 14 (2004) 465-479
47. Shimbo K., Brassard D.L., Lamb R.A., and Pinto L.H. Ion selectivity and activation of the M2 ion channel of influenza virus. Biophys. J. 70 (1996) 1335-1346
48. Simonsen L., Viboud C., Grenfell B.T., Dushoff J., Jennings L., Smit M., Macken C., Hata M., Gog J., Miller M.A., et al. The genesis and spread of reassortment human influenza A/H3N2 viruses conferring adamantane resistance. Mol. Biol. Evol. 24 (2007) 1811-1820
49. Steinhauer D.A., Wharton S.A., Skehel J.J., Wiley D.C., and Hay A.J. Amantadine selection of a mutant influenza virus containing an acid-stable hemagglutinin glycoprotein: evidence for virus-specific regulation of the pH of glycoprotein transport vesicles. Proc. Natl. Acad. Sci. USA 88 (1991) 11525-11529
50. Stouffer A.L., Nanda V., Lear J.D., and DeGrado W.F. Sequence determinants of a transmembrane proton channel: an inverse relationship between stability and function. J. Mol. Biol. 347 (2005) 169-179
51. Stouffer A.L., DeGrado W.F., and Lear J.D. Analytical ultracentrifugation studies of the influenza M2 homotetramerization equilibrium in detergent solutions. Prog. Colloid Polym. Sci. 131 (2006) 108-115
52. Stouffer A.L., Acharya R., Salom D., Levine A.S., Di Costanzo L., Soto C.S., Tereshko V., Nanda V., Stayrook S., and DeGrado W.F. Structural basis for the function and inhibition of an influenza virus proton channel. Nature 451 (2008) 596-599
53. Suzuki H., Saito R., Masuda H., Oshitani H., Sato M., and Sato I. Emergence of amantadine-resistant influenza A viruses: epidemiological study. J. Infect. Chemother. 9 (2003) 195-200
54. Tamm L.K., Hong H., and Liang B. Folding and assembly of β-barrel membrane proteins. Biochim. Biophys. Acta 1666 (2004) 250-263
55. Tang Y., Zaitseva F., Lamb R.A., and Pinto L.H. The gate of the influenza virus M2 proton channel is formed by a single tryptophan residue. J. Biol. Chem. 277 (2002) 39880-39886
56. Venkataraman P., Lamb R.A., and Pinto L.H. Chemical rescue of histidine selectivity filter mutants of the M2 ion channel of influenza A virus. J. Biol. Chem. 280 (2005) 21463-21472
57. Wang C., Takeuchi K., Pinto L.H., and Lamb R.A. Ion channel activity of influenza A virus M2 protein: characterization of the amantadine block. J. Virol. 67 (1993) 5585-5594
58. Wang C., Lamb R.A., and Pinto L.H. Activation of the M2 ion channel of influenza virus: a role for the transmembrane domain histidine residue. Biophys. J. 69 (1995) 1363-1371
59. Wu Y., and Voth G.A. A computational study of the closed and open states of the influenza A M2 proton channel. Biophys. J. 89 (2005) 2402-2411