Structure and mechanism of the M2 proton channel of influenza A virus

Nature

Volumn 451, Issue 7178, 2008, Pages 591-595

  Schnell, Jason R ^a   Chou, James J ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ASPARTIC ACID; MEMBRANE PROTEIN; PROTEIN M2; PROTON; RIMANTADINE; TETRAMER; TRYPTOPHAN; WATER;

ACIDIFICATION; CYTOPLASM; INFLUENZA; MEMBRANE; MUTATION; PROTEIN; VIRUS;

ANTIVIRAL RESISTANCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONFORMATION; DISSOCIATION; DRUG BINDING; GENE MUTATION; HYDROPHILICITY; INFLUENZA VIRUS A; MEMBRANE CHANNEL; MOLECULAR INTERACTION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PH; PRIORITY JOURNAL; PROTEIN STRUCTURE; PROTON TRANSPORT;

INFLUENZA A VIRUS; ORTHOMYXOVIRIDAE;

EID: 38749106195     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature06531     Document Type: Article

References (39)

1. Lamb, R. A., Holsinger, L. J. & Pinto, L. H. Receptor-Mediated Virus Entry into Cells (ed., Wimmer, E.) 303-321 (Cold Spring Harbor Laboratory Press, Cold Spring Harbor, 1994).
2. Helenius, A. Unpacking the incoming influenza-virus. Cell 69, 577-578 (1992).
3. Ciampor, F. et al. Evidence that the amantadine-induced, M2-mediated conversion of influenza A virus hemagglutinin to the low pH conformation occurs in an acidic trans Golgi compartment. Virology 188, 14-24 (1992).
4. Hay, A. J., Wolstenholme, A. J., Skehel, J. J. & Smith, M. H. The molecular basis of the specific anti-influenza action of amantadine. EMBO J. 4, 3021-3024 (1985).
5. Wang, C., Takeuchi, K., Pinto, L. H. & Lamb, R. A. Ion channel activity of influenza A virus M2 protein: characterization of the amantadine block. J. Virol. 67, 5585-5594 (1993).
6. Pinto, L. H., Holsinger, L. J. & Lamb, R. A. Influenza virus M2 protein has ion channel activity. Cell 69, 517-528 (1992).
7. Chizhmakov, I. V. et al. Selective proton permeability and pH regulation of the influenza virus M2 channel expressed in mouse erythroleukaemia cells. J. Physiol. (Lond.) 494, 329-336 (1996).
8. Sugrue, R. J. & Hay, A. J. Structural characteristics of the M2 protein of influenza A viruses: evidence that it forms a tetrameric channel. Virology 180, 617-624 (1991).
9. Holsinger, L. J. & Lamb, R. A. Influenza virus M2 integral membrane protein is a homotetramer Stabilized by formation of disulfide bonds. Virology 183, 32-43 (1991).
10. Tang, Y., Zaitseva, F., Lamb, R. A. & Pinto, L. H. The gate of the influenza virus M2 proton channel is formed by a single tryptophan residue. J. Biol. Chem. 277, 39880-39886 (2002).
11. Pinto, L. H. et al. 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, 11301-11306 (1997).
12. + channel. Protein Sci. 10, 2241-2250 (2001).
13. + channel. J. Mol. Biol. 286, 951-962 (1999).
14. Betakova, T., Ciampor, F. & Hay, A. J. Influence of residue 44 on the activity of the M2 proton channel of influenza A virus. J. Gen. Virol. 86, 181-184 (2005).
15. Sugrue, R. J., Belshe, R. B. & Hay, A. J. Palmitoylation of the influenza A virus M2 protein. Virology 179, 51-56 (1990).
16. Aldrich, P. E. et al. Antiviral agents. 2. Structure-activity relationships of compounds related to 1-adamantanamine. J. Med. Chem. 14, 535-543 (1971).
17. Loria, J. P., Rance, M. & Palmer, A. G. A relaxation-compensated Carr-Purcell-Meiboom-Gill sequence for characterizing chemical exchange by NMR spectroscopy. J. Am. Chem. Soc. 121, 2331-2332 (1999).
18. Tobler, K., Kelly, M. L., Pinto, L. H. & Lamb, R. A. Effect of cytoplasmic tail truncations on the activity of the M(2) ion channel of influenza A virus. J. Virol. 73, 9695-9701 (1999).
19. Pinto, L. H. & Lamb, R. A. Understanding the mechanism of action of the anti-influenza virus drug amantadine. Trends Microbiol. 3, 271 (1995).
20. Astrahan, P., Kass, I., Cooper, M. A. & Arkin, I. T. A novel method of resistance for influenza against a channel-blocking antiviral drug. Proteins 55, 251-257 (2004).
21. Subczynski, W. K., Wojas, J., Pezeshk, V. & Pezeshk, A. Partitioning and localization of spin-labeled amantadine in lipid bilayers: an EPR Study. J. Pharm. Sci. 87, 1249-1254 (1998).
22. Wang, J. F., Schnell, J. R. & Chou, J. J. Amantadine partition and localization in phospholipids membrane: a solution NMR study. Biochem. Biophys. Res. Commun. 324, 212-217 (2004).
23. Griffin, S. D. et al. The p7 protein of hepatitis C virus forms an ion channel that is blocked by the antiviral drug, Amantadine. FEBS Lett. 535, 34-38 (2003).
24. Plugge, B. et al. A potassium channel protein encoded by chlorella virus PBCV-1. Science 287, 1641-1644 (2000).
25. Svensson, T. H. Dopamine release and direct dopamine receptor activation in the central nervous system by D-145, an amantadine derivative. Eur. J. Pharmacol. 23, 232-238 (1973).
26. + channel through multiple binding sites. Neuron 18, 665-673 (1997).
27. Lee, S.-Y. & MacKinnon, R. A membrane-access mechanism of ion channel inhibition by voltage sensor toxins from spider venom. Nature 430, 232-235 (2004).
28. Stouffer, A. L. et al. Structural basis for the function and pharmaceutical inhibition of an influenza virus proton channel. Nature doi:10.1038/nature06528 (this issue).
29. Call, M. E. et al. The structure of the ζζ transmembrane dimer reveals features essential for its assembly with the T cell receptor. Cell 127, 355-368 (2006).
30. Chou, J. J., Baber, J. L. & Bax, A. Characterization of phospholipids mixed micelles by translational diffusion. J. Biomol. NMR 29, 299-308 (2004).
31. Oxenoid, K. & Chou, J. J. The structure of phospholamban pentamer reveals a channel-like architecture in membranes. Proc. Natl Acad. Sci. USA 102, 10870-10875 (2005).
32. Blacklow, S. C. & Kim, P. S. Protein folding and calcium binding defects arising from familial hypercholesterolemia mutations of the LDL receptor. Nature Struct. Biol. 3, 758-762 (1996).
33. Bax, A. et al. Measurement of homo- and heteronuclear J couplings from quantitative J correlation. Methods Enzymol. 239, 79-105 (1994).
34. MacKenzie, K. R., Prestegard, J. H. & Engelman, D. M. Leucine side-chain rotamers in a glycophorin A transmembrane peptide as revealed by three-bond carbon-carbon couplings and 13C chemical shifts. J. Biomol. NMR 7, 256-260 (1996).
35. Chou, J. J., Gaemers, S., Howder, B., Louis, J. M. & Bax, A. A simple apparatus for generating stretched polyacrylamide gels, yielding uniform alignment of proteins and detergent micelles. J. Biomol. NMR 21, 377-382 (2001).
36. Schwieters, C. D., Kuszewski, J., Tjandra, N. & Clore, G. M. The Xplor-NIH NMR molecular structure determination package. J. Magn. Reson. 160, 66-74 (2002).
37. Cornilescu, G., Delaglio, F. & Bax, A. Protein backbone angle restraints from searching a database for chemical shift and sequence homology. J. Biomol. NMR 13, 289-302 (1999).
38. Zweckstetter, M. & Bax, A. Prediction of sterically induced alignment in a dilute liquid crystalline phase: aid to protein structure determination by NMR. J. Am. Chem. Soc. 122, 3791-3792 (2000).
39. Allerhand, A. & Thiele, E. Analysis of Carr-Purcell spin-echo NMR experiments on multiple-spin systems. II. The effect of chemical exchange. J. Chem. Phys. 45, 902-916 (1966).