Experimentally based orientational refinement of membrane protein models: A structure for the influenza A M2 H+ channel

Journal of Molecular Biology

Volumn 286, Issue 3, 1999, Pages 951-962

  Kukol, Andreas ^a   D Adams, Paul ^b   Rice, Luke M ^b   Brunger, Axel T ^b   T Arkin, Isaiah ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b YALE UNIVERSITY   (United States)

Author keywords

Influenza; Infrared spectroscopy; Ion channel; M2 protein; Molecular dynamics

Indexed keywords

CARRIER PROTEIN; MEMBRANE PROTEIN;

ALPHA HELIX; ARTICLE; CIRCULAR DICHROISM; INFLUENZA VIRUS A; LIPID VESICLE; MEMBRANE CHANNEL; MOLECULAR DYNAMICS; MOLECULAR MODEL; NONHUMAN; PRIORITY JOURNAL; PROTON TRANSPORT; SPATIAL ORIENTATION; STRUCTURE ACTIVITY RELATION;

INFLUENZA A VIRUS; INFLUENZA VIRUS; RNA VIRUSES;

EID: 0033605318     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1998.2512     Document Type: Article

References (45)

1. Adams P., Arkin I., Engelman D., Brunger A. Computational searching and mutagenesis suggests a structure for the petameric transmembrane domain of phospholamban. Nature Struct. Biol. 2:1995;154-162.
2. Adams P., Engelman D., Brunger A. Improved prediction for the structure of the dimeric transmembrane domain of glycophorin A obtained through global searching. Proteins: Stuct. Funct. Genet. 26:1996;257-261.
3. Akiba T., Toyoshima C., Matsunaga T., Kawamoto M., T K., Fukuyama K., Namba K., Matsubara H. Three-dimensional structure of bovine cytochrome bc 1 complex by electron cryomicroscopy and helical image reconstruction. Nature Struct. Biol. 3:1996;553-561.
4. Anderson T., Hellgeth J., Lansbury P. Isotope edited infrared linear dichroism-determination of amide orientational relationships. J. Am. Chem. Soc. 31:1992;6540-6546.
5. Arkin I., Adams P., MacKenzie K., Lemmon M., Brunger A., Engelman D. Structural organization of the pentameric transmembrane alpha-helices of phospholamban, a cardiac ion channel. EMBO J. 13:1994;4757-4764.
6. Arkin I., Brunger A., Engelman D. Are there dominant membrane protein families with a given number of helices? Proteins: Struct. Funct. Genet. 28:1997a;465-466.
7. Arkin I., MacKenzie K., Brunger A. Site-directed dichroism as a method for obtaining rotational and orientational constraints for oriented polymers. J. Am. Chem. Soc. 119:1997b;8973-8190.
8. Braiman M., Rothschild K. Fourier transform infrared techniques for probing membrane protein structure. Annu. Rev. Biophys. Biophys. Chem. 17:1988;541-570.
9. Brunger A., Adams P., Clore G., Gros W., Grosse-Kunstleve R., Jiang J., Kuszewski J., Nilges M., Pannu N., Read R., Rice L., Simonson T., Warren G. Crystallography and NMR system: A new software system for macromolecular structure determination. Acta Crystallog. sect. D. 1999.
10. Bui M., Whittaker G., Helenius A. Effect of m1 protein and low pH on nuclear transport of influenza virus ribonucleoproteins. J. Virol. 70:1996;8391-8401.
11. Byler D., Susi H. Examination of the secondary structure of proteins by deconvolved FTIR spectra. Biopolymers. 25:1986;469-487.
12. +conduction and selectivity. Science. 280:1998;69-77.
13. Duff K., Ashley R. The transmembrane domain of influenza A M2 protein forms amantadine-sensitive proton channels in planar lipid bilayers. Virology. 190:1992;485-489.
14. Duff K., Kelly S., Price N., Bradshaw J. The secondary structure of influenza A M2 transmembrane domain. A circular dichroism study. FEBS Letters. 311:1992;256-258.
15. Duff K., Gilchrist P., Saxena A., Bradshaw J. Neutron diffraction reveals the site of amantadine blockade in the influenza A M2 ion channel. Virology. 202:1994;287-293.
16. Forrest L., DeGrado W., Dieckmann G., Sansom M. Two models of the influenza A M2 channel domain: verification by comparison. Fold. Design. 3:1998;443-448.
17. Grambas S., Bennett M., Hay A. Influence of amantadine resistance mutations on the pH regulatory function of the M2 protein of influenza A viruses. Virology. 191:1992;541-549.
18. Hagmar P., Norden B., Baty D., Chartier M., Takahashi M. Structure of DNA-RecA complexes studied by residue differential linear dichroism and fluorescence spectroscopy for a genetically engineered RecA protein. J. Mol. Biol. 226:1992;1193-1205.
19. Harrick N. Internal Reflection Spectroscopy. 1967;Interscience Publishers, New York.
20. Hay A., Wolstenholme A., Skehel J., Smith M. The molecular basis of the specific anti-influenza action of amantadine. EMBO J. 4:1985;3021-3024.
21. Holsinger L., Lamb R. Influenza virus M2 integral membrane protein is a homotetramer stabilized by formation of disulfide bonds. Virology. 183:1991;32-43.
22. Holsinger L., Nichani D., Pinto L., Lamb R. Influenza A virus M2 ion channel protein: a structure-function analysis. J. Virol. 68:1994;1551-1563.
23. Iwata S., Ostermeier C., Michel H. Structure at 2.8 Å resolution of cytochrome c oxidase from paraoccus denitrificans. Nature. 376:1995;660-669.
24. Jorgensen W., Tirado-Rives J. The OPLS potential function for proteins, energy minimization for crystals of cyclic peptides and crambin. J. Am. Chem. Soc. 110:1988;1657-1666.
25. Kauppinen J., Moffatt D., Mantsch H., Cameron D. Fourier self-deconvolution: a method for resolving intrinsically overlapped bands. Appl. Spectrosc. 35:1982;271-276.
26. Kovacs F., Cross T. Transmembrane four-helix bundle of influenza A M2 protein channel: structural implications from helix tilt and orientation. Biophys. J. 73:1997;2511-2517.
27. Kraulis P. Molscript: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystalog. 24:1991;946-950.
28. Lamb R., Pinto L. Do vpu and vpr of human immunodeficiency virus type 1 and nb of influenza b virus have ion channel activities in the viral life cycles? Virology. 229:1997;1-11.
29. Lamb R., Zebedee S., Richardson C. Influenza virus M2 protein is an integral membrane protein expressed on the infected-cell surface. Cell. 40:1985;627-633.
30. Lemmon M., Flanagan J., Treutlein H., Zhang J., Engelman D. Sequence specificity in the dimerization of transmembrane alpha-helices. Biochemistry. 31:1992;12719-12725.
31. Lemmon M., Treutlein H., Adams P., Brunger A., Engelman D. A dimerization motif for transmembrane alpha-helices. Nature Struct. Biol. 1:1994;157-163.
32. Ludlam C., Arkin I., Liu X., Rothman M., Rath P., Aimoto S., Engelman D., Rothschild K. FTIR spectroscopy and site-directed isotope labelling as a probe of the local secondary structure of in the transmembrane domain of phospholamban. Biophys. J. 70:1996;1728-1736.
33. MacKenzie K., Prestegard J., Engelman D. A transmembrane helix dimer: structure and implications. Science. 276:1997;131-133.
34. Norden B., Elvingson C., Kubista M., Sjoberg B., Ryberg H., Ryberg M., Mortensen K., Takahashi M. Structure of RecA-DNA complexes studied by combination of linear dichroism and small-angle neutron scattering measurements on flow-oriented samples. J. Mol. Biol. 226:1992;1175-1191.
35. Pinto L., Dieckmann G., Gandhi C., Papworth C., Braman J., Shaughnessy M., Lear J., Lamb R., DeGrado W. 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.
36. Sansom M., Kerr I. Influenza virus M2 protein: a molecular modelling study of the ion channel. Protein Eng. 6:1993;65-74.
37. Sansom M., Kerr I., Smith G., Son H. The influenza A virus M2 channel: a molecular modeling and simulation study. Virology. 233:1997;163-173.
38. Shimbo K., Brassard D., Lamb R., Pinto L. Ion selectivity and activation of the M2 ion channel of influenza virus. Biophys. J. 70:1996;1335-1346.
39. Sugrue R., Hay A. Structural characteristics of the M2 protein of influenza A viruses: evidence that it forms a tetrameric channel. Virology. 180:1991;617-624.
40. Tadesse L., Nazarbaghi R., Walters L. Isotopically enhanced infrared spectroscopy: a novel method for examining the secondary structure at specific sites in conformationally heterogenous peptides. J. Am. Chem. Soc. 113:1991;7036-7037.
41. Treutlein H., Lemmon M., Engelman D., Brunger A. The glycophorin A transmembrane domain dimer: sequence-specific propensity for a right-handed supercoil of helices. Biochemistry. 31:1992;12726-12732.
42. Tsuboi M. Infrared dichroism and molecular conformation of a-form poy-g-benzyl-l-glutamat. J. Polym. Sci. 59:1962;139-153.
43. Tsukihara T., Aoyama H., Yamashita T., Tomizaki T., Yamaguchi H., Shinzawa-Itoh K., Nakashima R., R Y., Yoshikawa S. The whole structure of the 13-subunit oxidized cytochrome c oxidase at 2.8 Å resolution. Science. 272:1996;1136-1144.
44. Wang C., Takeuchi K., Pinto L., Lamb R. Ion channel activity of influenza A virus M2 protein: characterization of the amantadine block. J. Virol. 67:1993;5585-5594.
45. Wang C., Lamb R., Pinto L. Activation of the M2 ion channel of influenza virus: a role for the transmembrane domain histidine residue. Biophys. J. 69:1995;1363-1371.