Distinct domains of the influenza A virus M2 protein cytoplasmic tail mediate binding to the M1 protein and facilitate infectious virus production

Journal of Virology

Volumn 80, Issue 16, 2006, Pages 8178-8189

  McCown, Matthew F ^a,b   Pekosz, Andrew ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b ROCHE BIOSCIENCE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ION CHANNEL; PROTEIN M1; PROTEIN M2; UNCLASSIFIED DRUG; VIRUS PROTEIN; VIRUS RNA;

ANIMAL CELL; ARTICLE; BINDING SITE; CONTROLLED STUDY; CYTOPLASM; EMBRYO; GENETIC COMPLEMENTATION; GENETIC CONSERVATION; GENETICS; HUMAN; HUMAN CELL; INFLUENZA VIRUS A; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REVERSE GENETICS; VIRUS ASSEMBLY; VIRUS CELL INTERACTION; VIRUS INFECTIVITY; VIRUS MORPHOLOGY; VIRUS PARTICLE; VIRUS REPLICATION;

AMINO ACID SEQUENCE; ANIMALS; CELLS, CULTURED; CYTOPLASM; DNA, VIRAL; DOGS; HUMANS; INFLUENZA A VIRUS; INFLUENZA, HUMAN; MOLECULAR SEQUENCE DATA; PROTEIN INTERACTION MAPPING; PROTEIN STRUCTURE, TERTIARY; SEQUENCE DELETION; VIRAL MATRIX PROTEINS; VIRUS ASSEMBLY;

INFLUENZA A VIRUS;

EID: 33746810932     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00627-06     Document Type: Article

References (84)

1. Ali, A., R. T. Avalos, E. Ponimaskin, and D. P. Nayak. 2000. Influenza virus assembly: effect of influenza virus glycoproteins on the membrane association of M1 protein. J. Virol. 74:8709-8719.
2. Barman, S., A. Ali, E. K. Hui, L. Adhikary, and D. P. Nayak. 2001. Transport of viral proteins to the apical membranes and interaction of matrix protein with glycoproteins in the assembly of influenza viruses. Virus Res. 77:61-69.
3. Bavari, S., C. M. Bosio, E. Wiegand, G. Ruthel, A. B. Will, T. W. Geisbert, M. Hevey, C. Schmaljohn, A. Schmaljohn, and M. J. Aman. 2002. Lipid raft microdomains: a gateway for compartmentalized trafficking of Ebola and Marburg viruses. J. Exp. Med. 195:593-602.
4. Bourmakina, S. V., and A. Garcia-Sastre. 2005. The morphology and composition of influenza A virus particles are not affected by low levels of M1 and M2 proteins in infected cells. J. Virol. 79:7926-7932.
5. Bourmakina, S. V., and A. Garcia-Sastre. 2003. Reverse genetics studies on the filamentous morphology of influenza A virus. J. Gen. Virol. 84:517-527.
6. Bukrinskaya, A. G., N. K. Vorkunova, G. V. Kornilayeva, R. A. Narmanbetova, and G. K. Vorkunova. 1982. Influenza virus uncoating in infected cells and effect of rimantadine. J. Gen. Virol. 60:49-59.
7. Bukrinskaya, A. G., N. K. Vorkunova, and N. L. Pushkarskaya. 1982. Uncoating of a rimantadine-resistant variant of influenza virus in the presence of rimantadine. J. Gen. Virol. 60:61-66.
8. Burleigh, L. M., L. J. Calder, J. J. Skehel, and D. A. Steinhauer. 2005. Influenza A viruses with mutations in the M1 helix six domain display a wide variety of morphological phenotypes. J. Virol. 79:1262-1270.
9. Castrucci, M. R., M. Hughes, L. Calzoletti, I. Donatelli, K. Wells, A. Takada, and Y. Kawaoka. 1997. The cysteine residues of the M2 protein are not required for influenza A virus replication. Virology 238:128-134.
10. Chen, B. J., M. Takeda, and R. A. Lamb. 2005. Influenza virus hemagglutinin (H3 subtype) requires palmitoylation of its cytoplasmic tail for assembly: M1 proteins of two subtypes differ in their ability to support assembly. J. Virol. 79:13673-13684.
11. Cox, J. C., A. W. Hampson, and R. C. Hamilton. 1980. An immunofluorescence study of influenza virus filament formation. Arch. Virol. 63:275-284.
12. Delchambre, M., D. Gheysen, D. Thines, C. Thiriart, E. Jacobs, E. Verdin, M. Horth, A. Burny, and F. Bex. 1989. The GAG precursor of simian immunodeficiency virus assembles into virus-like particles. EMBO J. 8:2653-2660.
13. D'Souza, V., and M. F. Summers. 2005. How retroviruses select their genomes. Nat. Rev. Microbiol. 3:643-655.
14. Duff, K. C., and R. H. Ashley. 1992. The transmembrane domain of influenza A M2 protein forms amantadine-sensitive proton channels in planar lipid bilayers. Virology 190:485-489.
15. Elleman, C. J., and W. S. Barclay. 2004. The M1 matrix protein controls the filamentous phenotype of influenza A virus. Virology 321:144-153.
16. Enami, M., and K. Enami. 1996. Influenza virus hemagglutinin and neuraminidase glycoproteins stimulate the membrane association of the matrix protein. J. Virol. 70:6653-6657.
17. Fujii, K., Y. Fujii, T. Noda, Y. Muramoto, T. Watanabe, A. Takada, H. Goto, T. Horimoto, and Y. Kawaoka. 2005. Importance of both the coding and the segment-specific noncoding regions of the influenza A virus NS segment for its efficient incorporation into virions. J. Virol. 79:3766-3774.
18. Fujii, Y., H. Goto, T. Watanabe, T. Yoshida, and Y. Kawaoka. 2003. Selective incorporation of influenza virus RNA segments into virions. Proc. Natl. Acad. Sci. USA 100:2002-2007.
19. Gheysen, D., E. Jacobs, F. de Foresta, C. Thiriart, M. Francotte, D. Thines, and M. De Wilde. 1989. Assembly and release of HIV-1 precursor Pr55gag virus-like particles from recombinant baculovirus-infected insect cells. Cell 59:103-112.
20. Gomez-Puertas, P., C. Albo, E. Perez-Pastrana, A. Vivo, and A. Portela. 2000. Influenza virus matrix protein is the major driving force in virus budding. J. Virol. 74:11538-11547.
21. Gomez-Puertas, P., I. Mena, M. Castillo, A. Vivo, E. Perez-Pastrana, and A. Portela. 1999. Efficient formation of influenza virus-like particles: dependence on the expression levels of viral proteins. J. Gen. Virol. 80(Pt 7):1635-1645.
22. Hatta, M., H. Goto, and Y. Kawaoka. 2004. Influenza B virus requires BM2 protein for replication. J. Virol. 78:5576-5583.
23. Hay, A. J., A. J. Wolstenholme, J. J. Skehel, and M. H. Smith. 1985. The molecular basis of the specific anti-influenza action of amantadine. EMBO J. 4:3021-3024.
24. Holsinger, L. J., M. A. Shaughnessy, A. Micko, L. H. Pinto, and R. A. Lamb. 1995. Analysis of the posttranslational modifications of the influenza virus M2 protein. J. Virol. 69:1219-1225.
25. Hughey, P. G., P. C. Roberts, L. J. Holsinger, S. L. Zebedee, R. A. Lamb, and R. W. Compans. 1995. Effects of antibody to the influenza A virus M2 protein on M2 surface expression and virus assembly. Virology 212:411-421.
26. Hui, E. K.-W., S. Barman, D. H.-P. Tang, B. France, and D. P. Nayak. 2006. YRKL sequence of influenza virus M1 functions as the L domain motif and interacts with VPS28 and Cdc42. J. Virol. 80:2291-2308.
27. Hui, E. K.-W., S. Barman, T. Y. Yang, and D. P. Nayak. 2003. Basic residues of the helix six domain of influenza virus M1 involved in nuclear translocation of M1 can be replaced by PTAP and YPDL late assembly domain motifs. J. Virol. 77:7078-7092.
28. Imai, M., S. Watanabe, A. Ninomiya, M. Obuchi, and T. Odagiri. 2004. Influenza B virus BM2 protein is a crucial component for incorporation of viral ribonucleoprotein complex into virions during virus assembly. J. Virol. 78:11007-11015.
29. Jin, H., G. P. Leser, J. Zhang, and R. A. Lamb. 1997. Influenza virus hemagglutinin and neuraminidase cytoplasmic tails control particle shape. EMBO J. 16:1236-1247.
30. Lamb, R. A., and R. M. Krug. 2001. Orthomyxoviridae: the viruses and their replication, p. 1487-1532. In D. M. Knipe and P. M. Howley (ed.), Fields virology, 4th ed. Lippincott, Williams, & Wilkins, Philadelphia, Pa.
31. Latham, T., and J. M. Galarza. 2001. Formation of wild-type and chimeric influenza virus-like particles following simultaneous expression of only four structural proteins. J. Virol. 75:6154-6165.
32. Leser, G. P., and R. A. Lamb. 2005. Influenza virus assembly and budding in raft-derived microdomains: a quantitative analysis of the surface distribution of HA, NA and M2 proteins. Virology 342:215-227.
33. Li, Y., L. Luo, M. Schubert, R. R. Wagner, and C. Y. Kang. 1993. Viral liposomes released from insect cells infected with recombinant baculovirus expressing the matrix protein of vesicular stomatitis virus. J. Virol. 67:4415-4420.
34. Liang, Y., Y. Hong, and T. G. Parslow. 2005. cis-acting packaging signals in the influenza virus PB1, PB2, and PA genomic RNA segments. J. Virol. 79:10348-10355.
35. Licata, J. M., R. F. Johnson, Z. Han, and R. N. Harty. 2004. Contribution of Ebola virus glycoprotein, nucleoprotein, and VP24 to budding of VP40 virus-like particles. J. Virol. 78:7344-7351.
36. Licata, J. M., M. Simpson-Holley, N. T. Wright, Z. Han, J. Paragas, and R. N. Harty. 2003. Overlapping motifs (PTAP and PPEY) within the Ebola virus VP40 protein function independently as late budding domains: involvement of host proteins TSG101 and VPS-4. J. Virol. 77:1812-1819.
37. Martin, K., and A. Helenius. 1991. Nuclear transport of influenza virus ribonucleoproteins: the viral matrix protein (M1) promotes export and inhibits import. Cell 67:117-130.
38. Martin, K., and A. Helenius. 1991. Transport of incoming influenza virus nucleocapsids into the nucleus. J. Virol. 65:232-244.
39. McCown, M., M. S. Diamond, and A. Pekosz. 2003. The utility of siRNA transcripts produced by RNA polymerase I in down regulating viral gene expression and replication of negative- and positive-strand RNA viruses. Virology 313:514-524.
40. McCown, M. F., and A. Pekosz. 2005. The influenza A virus M2 cytoplasmic tail is required for infectious virus production and efficient genome packaging. J. Virol. 79:3595-3605.
41. Mena, I., A. Vivo, E. Perez, and A. Portela. 1996. Rescue of a synthetic chloramphenicol acetyltransferase RNA into influenza virus-like particles obtained from recombinant plasmids. J. Virol. 70:5016-5024.
42. Morgenstern, J. P., and H. Land. 1990. Advanced mammalian gene transfer: high titre retroviral vectors with multiple drug selection markers and a complementary helper-free packaging cell line. Nucleic Acids Res. 18:3587-3596.
43. Morita, E., and W. I. Sundquist. 2004. Retrovirus budding. Annu. Rev. Cell Dev. Biol. 20:395-425.
44. Mosley, V. M., and R. W. G. Wyckoff. 1946. Electron micrography of the virus of influenza. Nature 157:263.
45. Mould, J. A., R. G. Paterson, M. Takeda, Y. Ohigashi, P. Venkataraman, R. A. Lamb, and L. H. Pinto. 2003. Influenza B virus BM2 protein has ion channel activity that conducts protons across membranes. Dev. Cell 5:175-184.
46. Muramoto, Y., A. Takada, K. Fujii, T. Noda, K. Iwatsuki-Horimoto, S. Watanabe, T. Horimoto, H. Kida, and Y. Kawaoka. 2006. Hierarchy among viral RNA (vRNA) segments in their role in vRNA incorporation into influenza A virions. J. Virol. 80:2318-2325.
47. Muriaux, D., S. Costes, K. Nagashima, J. Mirro, E. Cho, S. Lockett, and A. Rein. 2004. Role of murine leukemia virus nucleocapsid protein in virus assembly. J. Virol. 78:12378-12385.
48. Muriaux, D., J. Mirro, D. Harvin, and A. Rein. 2001. RNA is a structural element in retrovirus particles. Proc. Natl. Acad. Sci. USA 98:5246-5251.
49. Neumann, G., T. Watanabe, H. Ito, S. Watanabe, H. Goto, P. Gao, M. Hughes, D. R. Perez, R. Donis, E. Hoffmann, G. Hobom, and Y. Kawaoka. 1999. Generation of influenza A viruses entirely from cloned cDNAs. Proc. Natl. Acad. Sci. USA 96:9345-9350.
50. Neumann, G., T. Watanabe, and Y. Kawaoka. 2000. Plasmid-driven formation of influenza virus-like particles. J. Virol. 74:547-551.
51. Noda, T., H. Sagara, E. Suzuki, A. Takada, H. Kida, and Y. Kawaoka. 2002. Ebola virus VP40 drives the formation of virus-like filamentous particles along with GP. J. Virol. 76:4855-4865.
52. Noda, T., H. Sagara, A. Yen, A. Takada, H. Kida, R. H. Cheng, and Y. Kawaoka. 2006. Architecture of ribonucleoprotein complexes in influenza A virus particles. Nature 439:490-492.
53. Park, E. K., M. R. Castrucci, A. Portner, and Y. Kawaoka. 1998. The M2 ectodomain is important for its incorporation into influenza A virions. J. Virol. 72:2449-2455.
54. Paterson, R. G., and R. A. Lamb. 1993. The molecular biology of influenza viruses and paramyxoviruses, p. 35-73. In A. J. Davison and R. M. Elliott (ed.), Molecular virology: a practical approach. Oxford University Press, Oxford, United Kingdom.
55. Patnaik, A., V. Chau, and J. W. Wills. 2000. Ubiquitin is part of the retrovirus budding machinery. Proc. Natl. Acad. Sci. USA 97:13069-13074.
56. Pinto, L. H., L. J. Holsinger, and R. A. Lamb. 1992. Influenza virus M2 protein has ion channel activity. Cell 69:517-528.
57. Roberts, P. C., R. A. Lamb, and R. W. Compans. 1998. The M1 and M2 proteins of influenza A virus are important determinants in filamentous particle formation. Virology 240:127-137.
58. Robison, C. S., and M. A. Whitt. 2000. The membrane-proximal stem region of vesicular stomatitis virus G protein confers efficient virus assembly. J. Virol. 74:2239-2246.
59. Sakaguchi, T., G. P. Leser, and R. A. Lamb. 1996. The ion channel activity of the influenza virus M2 protein affects transport through the Golgi apparatus. J. Cell Biol. 133:733-747.
60. Scheiffele, P., A. Rietveld, T. Wilk, and K. Simons. 1999. Influenza viruses select ordered lipid domains during budding from the plasma membrane. J. Biol. Chem. 274:2038-2044.
61. Schmitt, A. P., and R. A. Lamb. 2004. Escaping from the cell: assembly and budding of negative-strand RNA viruses. Curr. Top. Microbiol. Immunol. 283:145-196.
62. Schmitt, A. P., and R. A. Lamb. 2005. Influenza virus assembly and budding at the viral budozone. Adv. Virus Res. 64:383-416.
63. Schmitt, A. P., G. P. Leser, E. Morita, W. I. Sundquist, and R. A. Lamb. 2005. Evidence for a new viral late-domain core sequence, FPIV, necessary for budding of a paramyxovirus. J. Virol. 79:2988-2997.
64. Schroeder, C., H. Heider, E. Moncke-Buchner, and T. I. Lin. 2005. The influenza virus ion channel and maturation cofactor M2 is a cholesterol-binding protein. Eur. Biophys. J. 34:52-66.
65. Schubert, U., D. E. Ott, E. N. Chertova, R. Welker, V. Tessmer, M. F. Princiotta, J. R. Bennink, H. G. Krausslich, and J. W. Yewdell. 2000. Proteasome inhibition interferes with gag polyprotein processing, release, and maturation of HIV-1 and HIV-2. Proc. Natl. Acad. Sci. USA 97:13057-13062.
66. Simpson-Holley, M., D. Ellis, D. Fisher, D. Elton, J. McCauley, and P. Digard. 2002. A functional link between the actin cytoskeleton and lipid rafts during budding of filamentous influenza virions. Virology 301:212-225.
67. Steinhauer, D. A., S. A. Wharton, J. J. Skehel, D. C. Wiley, and A. J. Hay. 1991. 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: 11525-11529.
68. Strack, B., A. Calistri, M. A. Accola, G. Palu, and H. G. Gottlinger. 2000. A role for ubiquitin ligase recruitment in retrovirus release. Proc. Natl. Acad. Sci. USA 97:13063-13068.
69. Sugrue, R. J., G. Bahadur, M. C. Zambon, M. Hall-Smith, A. R. Douglas, and A. J. Hay. 1990. Specific structural alteration of the influenza haemagglutinin by amantadine. EMBO J. 9:3469-3476.
70. Sugrue, R. J., R. B. Belshe, and A. J. Hay. 1990. Palmitoylation of the influenza A virus M2 protein. Virology 179:51-56.
71. Swenson, D. L., K. L. Warfield, K. Kuehl, T. Larsen, M. C. Hevey, A. Schmaljohn, S. Bavari, and M. J. Aman. 2004. Generation of Marburg virus-like particles by co-expression of glycoprotein and matrix protein. FEMS Immunol. Med. Microbiol. 40:27-31.
72. Takeda, M., G. P. Leser, C. J. Russell, and R. A. Lamb. 2003. Influenza virus hemagglutinin concentrates in lipid raft microdomains for efficient viral fusion. Proc. Natl. Acad. Sci. USA 100:14610-14617.
73. 2 ion channel activity is essential for efficient replication in tissue culture. J. Virol. 76:1391-1399.
74. Thomas, J. M., M. P. Stevens, N. Percy, and W. S. Barclay. 1998. Phosphorylation of the M2 protein of influenza A virus is not essential for virus viability. Virology 252:54-64.
75. Tobler, K., M. L. Kelly, L. H. Pinto, and R. A. Lamb. 1999. Effect of cytoplasmic tail truncations on the activity of the M2 ion channel of influenza A virus. J. Virol. 73:9695-9701.
76. Veil, M., H. D. Klenk, A. Kendal, and R. Rott. 1991. The M2 protein of influenza A virus is acylated. J. Gen. Virol. 72(Pt 6):1461-1465.
77. Wang, C., K. Takeuchi, L. H. Pinto, and R. A. Lamb. 1993. Ion channel activity of influenza A virus M2 protein: characterization of the amantadine block. J. Virol. 67:5585-5594.
78. Ward, C. L., M. H. Dempsey, C. J. Ring, R. E. Kempson, L. Zhang, D. Gor, B. W. Snowden, and M. Tisdale. 2004. Design and performance testing of quantitative real time PCR assays for influenza A and B viral load measurement. J. Clin. Virol. 29:179-188.
79. Watanabe, T., S. Watanabe, H. Ito, H. Kida, and Y. Kawaoka. 2001. Influenza A virus can undergo multiple cycles of replication without M2 ion channel activity. J. Virol. 75:5656-5662.
80. Watanabe, T., S. Watanabe, T. Noda, Y. Fujii, and Y. Kawaoka. 2003. Exploitation of nucleic acid packaging signals to generate a novel influenza virus-based vector stably expressing two foreign genes. J. Virol. 77:10575-10583.
81. Zebedee, S. L., and R. A. Lamb. 1989. Growth restriction of influenza A virus by M2 protein antibody is genetically linked to the M1 protein. Proc. Natl. Acad. Sci. USA 86:1061-1065.
82. Zebedee, S. L., and R. A. Lamb. 1988. Influenza A virus M2 protein: monoclonal antibody restriction of virus growth and detection of M2 in virions. J. Virol. 62:2762-2772.
83. Zhang, J., A. Pekosz, and R. A. Lamb. 2000. Influenza virus assembly and lipid raft microdomains: a role for the cytoplasmic tails of the spike glycoproteins. J. Virol. 74:4634-4644.
84. Zhirnov, O. P. 1992. Isolation of matrix protein M1 from influenza viruses by acid-dependent extraction with nonionic detergent. Virology 186:324-330.