Structural basis for the function and inhibition of an influenza virus proton channel

Nature

Volumn 451, Issue 7178, 2008, Pages 596-599

  Stouffer, Amanda L ^a,b,d   Acharya, Rudresh ^a   Salom, David ^a,e   Levine, Anna S ^a,f   Di Costanzo, Luigi ^b   Soto, Cinque S ^a   Tereshko, Valentina ^c   Nanda, Vikas ^a,g   Stayrook, Steven ^a   DeGrado, William F ^a,b  

^a School of Veterinary Medicine   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c UNIVERSITY OF CHICAGO   (United States)

^d ETH ZURICH   (Switzerland)

^e Polgenix Inc   (United States)

^f BROWN UNIVERSITY   (United States)

^g UNIVERSITY OF MEDICINE AND DENTISTRY OF NEW JERSEY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMANTADINE; HISTIDINE; ION CHANNEL; MUSCARINIC M2 RECEPTOR ANTAGONIST; PROTON; TRYPTOPHAN;

ACIDIFICATION; CRYSTAL STRUCTURE; DRUG RESISTANCE; INFLUENZA; INHIBITION; MUTATION; PH; PROTEIN; VIRUS;

ARTICLE; CRYSTAL STRUCTURE; DRUG BINDING; DRUG BINDING SITE; INFLUENZA VIRUS; MEMBRANE STRUCTURE; PH; PKA; PRIORITY JOURNAL; PROTEIN FUNCTION; VIRUS INHIBITION; VIRUS MUTATION;

AVES; INFLUENZA A VIRUS; ORTHOMYXOVIRIDAE; SUIDAE;

EID: 38749151911     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature06528     Document Type: Article

References (42)

1. Deyde, V. M. et al. Surveillance of resistance to adamantanes among influenza A(H3N2) and A(H1N1) viruses isolated worldwide. J. Infect. Dis. 196, 249-257 (2007).
2. 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).
3. Grambas, S., Bennett, M. S. & Hay, A. J. Influence of amantadine resistance mutations on the pH regulatory function of the M2 protein of influenza A viruses. Virology 191, 541-549 (1992).
4. Bright, R. A., Shay, D. K., Shu, B., Cox, N. J. & Klimov, A. I. Adamantane resistance among influenza A viruses isolated early during the 2005-2006 influenza season in the United States. J. Am. Med. Assoc. 295, 891-894 (2006).
5. 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).
6. Sansom, M. S. P., Kerr, I. D., Smith, G. R. & Son, H. S. The influenza A virus M2 channel: a molecular modeling and simulation study. Virology 233, 163-173 (1997).
7. Zhong, Q. F., Newns, D. M., Pattnaik, P., Lear, J. D. & Klein, M. L. Two possible conducting states of the influenza A virus M2 ion channel. FEBS Lett. 473, 195-198 (2000).
8. Ayton, G. S. & Voth, G. A. Multiscale simulation of transmembrane proteins. J. Struct. Biol. 157, 570-578 (2007).
9. Hu, F., Fu, R. & Cross, T. A. The chemical and dynamic influence of the drug amantadine on the M2 proton channel transmembrane domain. Biophys. J. 93, 276-283 (2007).
10. Hu, J. et al. 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 (2006).
11. Takeuchi, H., Okada, A. & Miura, T. Roles of the histidine and tryptophan side chains in the M2 proton channel from influenza A virus. FEBS Lett. 552, 35-38 (2003).
12. Duff, K. C. & Ashley, R. H. The transmembrane domain of influenza A M2 protein forms amantadine-sensitive proton channels in planar lipid bilayers. Virology 190, 485-489 (1992).
13. Salom, D., Hill, B. R., Lear, J. D. & DeGrado, W. F. pH-dependent tetramerization and amantadine binding of the transmembrane helix of M2 from the influenza A virus. Biochemistry 39, 14160-14170 (2000).
14. Cady, S. D., Goodman, C., Tatko, C. D., DeGrado, W. F. & Hong, M. Determining the orientation of uniaxially rotating membrane proteins using unoriented samples: a 2H, 13C, AND 15N solid-state NMR investigation of the dynamics and orientation of a transmembrane helical bundle. J. Am. Chem. Soc. 129, 5719-5729 (2007).
15. Stouffer, A. L., Nanda, V., Lear, J. D. & DeGrado, W. F. Sequence determinants of a transmembrane proton channel: an inverse relationship between stability and function. J. Mol. Biol. 347, 169-179 (2005).
16. + channel. Protein Sci. 10, 2241-2250 (2001).
17. MacKinnon, R. Potassium channels. FEBS Lett. 555, 62-65 (2003).
18. 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).
19. Czabotar, P. E., Martin, S. R. & Hay, A. J. Studies of structural changes in the M2 proton channel of influenza A virus by tryptophan fluorescence. Virus Res. 99, 57-61 (2004).
20. Bright, R. A. et al. Incidence of adamantane resistance among influenza A (H3N2) viruses isolated worldwide from 1994 to 2005: a cause for concern. Lancet 366, 1175-1181 (2005).
21. De Clercq, E. Antiviral agents active against influenza A viruses. Nature Rev. Drug Discov. 5, 1015-1025 (2006).
22. Senes, A., Engel, D. E. & DeGrado, W. F. Folding of helical membrane proteins: the role of polar, GxxxG-like and proline motifs. Curr. Opin. Struct. Biol. 14, 465-479 (2004).
23. + channel helical bundle combining precise orientational and distance restraints from solid state NMR-1. Biochemistry 41, 13170-13177 (2002).
24. Bauer, C. M., Pinto, L. H., Cross, T. A. & Lamb, R. A. The influenza virus M2 ion channel protein: probing the structure of the transmembrane domain in intact cells by using engineered disulfide cross-linking. Virology 254, 196-209 (1999).
25. Hu, J. et al. Backbone structure of the amantadine-blocked trans-membrane domain M2 proton channel from influenza A virus. Biophys. J. 92, 4335-4343 (2007).
26. Jiang, Y. et al. Crystal structure and mechanism of a calcium-gated potassium channel. Nature 417, 515-522 (2002).
27. 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).
28. Mould, J. A. et al. Mechanism for proton conduction of the M2 ion channel of influenza A Virus. J. Biol. Chem. 275, 8592-8599 (2000).
29. Gandhi, C. S. et al. Cu(II) inhibition of the proton translocation machinery of the influenza A virus M2 protein. J. Biol. Chem. 274, 5474-5482 (1999).
30. Holsinger, L. J., Nichani, D., Pinto, L. H. & Lamb, R. A. Influenza A virus M2 ion channel protein: a structure-function analysis. J. Virol. 68, 1551-1563 (1994).
31. Schnell, J. R. & Chou, J. J. Structure and mechanism of the M2 proton channel of influenza A virus. Nature doi:10.1038/nature06531 (this issue).
32. Choma, C., Gratowski, H., Lear, J. D. & DeGrado, W. F. Asparagine-mediated self-association of a model transmembrane helix. Nature Struct. Biol. 7, 161-166 (2000).
33. Otwinowski, Z. & Minor, W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326 (1997).
34. Matthews, B. W. Solvent content of protein crystals. J. Mol. Biol. 33, 491-497 (1968).
35. Read, R. J. Pushing the boundaries of molecular replacement with maximum likelihood. Acta Crystallogr. D57, 1373-1382 (2001).
36. Collaborative Computational Project Number 4. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D50, 760-763 (1994).
37. Murshudov, G. N., Vagin, A. A. & Dodson, E. J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D53, 240-255 (1997).
38. Brünger, A. T. et al. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D54, 905-921 (1998).
39. Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D60, 2126-2132 (2004).
40. SMART, SAINT, SADABS, and XPREP Software Reference Manual (Bruker, AXS Inc., Madison, Wisconsin, 2000).
41. Schweiters, C. D., Kuszewski, J. J., Tjandra, N. & Clore, G. M. The Xplor-NIH NMR molecular structure determination package. J. Magn. Reson. 160, 66-74 (2003).
42. Christopher, A. J., Swanson, R. & Baldwin, T. O. Algorithms for finding the axis of a helix: fast rotational and parametric least-squares methods. Comput. Chem. 20, 339-345 (1996).