The highly conserved arginine residues at positions 76 through 78 of influenza a virus matrix protein M1 play an important role in viral replication by affecting the intracellular localization of M1

Journal of Virology

Volumn 86, Issue 3, 2012, Pages 1522-1530

  Das, Subash C ^a   Watanabe, Shinji ^b   Hatta, Masato ^a   Noda, Takeshi ^c   Neumann, Gabrielle ^a   Kawaoka, Makoto Ozawa ^a,b,c,d  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c UNIVERSITY OF TOKYO   (Japan)

^d The Universtiry of Tokyo   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; ASPARTIC ACID; INFLUENZA VIRUS A MATRIX PROTEIN; LYSINE; MATRIX PROTEIN; UNCLASSIFIED DRUG; VIRUS PROTEIN;

AMINO ACID SUBSTITUTION; ARTICLE; CELL MIGRATION; INFLUENZA VIRUS A; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SITE DIRECTED MUTAGENESIS; VIRION; VIROGENESIS; VIRUS MUTATION; VIRUS RELEASE; VIRUS REPLICATION;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMALS; ARGININE; CELLS, CULTURED; CONSERVED SEQUENCE; DOGS; INFLUENZA A VIRUS; MOLECULAR SEQUENCE DATA; MUTATION; SEQUENCE HOMOLOGY, AMINO ACID; VIRAL MATRIX PROTEINS; VIRUS REPLICATION;

CERCOPITHECINE HERPESVIRUS 1; INFLUENZA A VIRUS; ORTHOMYXOVIRIDAE;

EID: 84863400843     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.06230-11     Document Type: Article

References (56)

1. Arzt S, et al. 2001. Combined results from solution studies on intact influenza virus M1 protein and from a new crystal form of its N-terminal domain show that M1 is an elongated monomer. Virology 279:439-446.
2. Baudin F, Petit I, Weissenhorn W, Ruigrok RW. 2001. In vitro dissection of the membrane and RNP binding activities of influenza virus M1 protein. Virology 281:102-108.
3. Bruce EA, Digard P, Stuart AD. 2010. The Rab11 pathway is required for influenzaAvirus budding and filament formation. J. Virol. 84:5848-5859.
4. Bui M, Whittaker G, Helenius A. 1996. Effect of M1 protein and low pH on nuclear transport of influenza virus ribonucleoproteins. J. Virol. 70: 8391-8401.
5. Bui M, Wills EG, Helenius A, Whittaker GR. 2000. Role of the influenza virus M1 protein in nuclear export of viral ribonucleoproteins. J. Virol. 74:1781-1786.
6. Burleigh LM, Calder LJ, Skehel JJ, Steinhauer DA. 2005. Influenza a viruses with mutations in the m1 helix six domain display a wide variety of morphological phenotypes. J. Virol. 79:1262-1270.
7. Chen BJ, Leser GP, Morita E, Lamb RA. 2007. Influenza virus hemagglutinin and neuraminidase, but not the matrix protein, are required for assembly and budding of plasmid-derived virus-like particles. J. Virol. 81:7111-7123.
8. Dhiman N, et al. 2010. Evidence for amino acid changes in a 57-base-pair region of the highly conserved matrix gene of pandemic (H1N1) 2009 influenza A virus. J. Clin. Microbiol. 48:3817-3819.
9. Eierhoff T, Ludwig S, Ehrhardt C. 2009. The influenza A virus matrix protein as a marker to monitor initial virus internalisation. Biol. Chem. 390:509 -515.
10. Eisfeld AJ, Kawakami E, Watanabe T, Neumann G, Kawaoka Y. 2011. RAB11A is essential for influenza genome transport to the plasma membrane. J. Virol. 85:6117- 6126.
11. Elster C, Larsen K, Gagnon J, Ruigrok RW, Baudin F. 1997. Influenza virus M1 protein binds to RNA through its nuclear localization signal. J. Gen. Virol. 78(Pt 7):1589-1596.
12. Gomez-Puertas P, Albo C, Perez-Pastrana E, Vivo A, Portela A. 2000. Influenza virus matrix protein is the major driving force in virus budding. J. Virol. 74:11538 -11547.
13. Gregoriades A. 1980. Interaction of influenza M protein with viral lipid and phosphatidylcholine vesicles. J. Virol. 36:470-479.
14. Harris A, Forouhar F, Qiu S, Sha B, Luo M. 2001. The crystal structure of the influenza matrix protein M1 at neutral pH: M1-M1 protein interfaces can rotate in the oligomeric structures of M1. Virology 289:34-44.
15. Helenius A. 1992. Unpacking the incoming influenza virus. Cell 69: 577-578.
16. Herz C, Stavnezer E, Krug R, Gurney T Jr. 1981. Influenza virus, an RNA virus, synthesizes its messenger RNA in the nucleus of infected cells. Cell 26:391-400.
17. Huang X, Liu T, Muller J, Levandowski RA, Ye Z. 2001. Effect of influenza virus matrix protein and viral RNA on ribonucleoprotein formation and nuclear export. Virology 287:405-416.
18. Kobasa D, Rodgers ME, Wells K, Kawaoka Y. 1997. Neuraminidase hemadsorption activity, conserved in avian influenza A viruses, does not influence viral replication in ducks. J. Virol. 71:6706-6713.
19. Lamb RA, Lai CJ, Choppin PW. 1981. Sequences of mRNAs derived from genome RNA segment 7 of influenza virus: colinear and interrupted mRNAs code for overlapping proteins. Proc. Natl. Acad. Sci. U. S. A. 78:4170-4174.
20. Lamb RA, Zebedee SL, Richardson CD. 1985. Influenza virus M2 protein is an integral membrane protein expressed on the infected-cell surface. Cell 40:627- 633.
21. Latham T, Galarza JM. 2001. Formation of wild-type and chimeric influenza virus-like particles following simultaneous expression of only four structural proteins. J. Virol. 75:6154-6165.
22. Li Z, et al. 2009. Mutational analysis of conserved amino acids in the influenza A virus nucleoprotein. J. Virol. 83:4153-4162.
23. Liu T, Ye Z. 2004. Introduction of a temperature-sensitive phenotype into influenza A/WSN/33 virus by altering the basic amino acid domain of influenza virus matrix protein. J. Virol. 78:9585-9591.
24. Liu X, et al. 2009. Cyclophilin A interacts with influenza A virus M1 protein and impairs the early stage of the viral replication. Cell Microbiol. 11:730-741.
25. Martin K, Helenius A. 1991. Nuclear transport of influenza virus ribonucleoproteins: the viral matrix protein (M1) promotes export and inhibits import. Cell 67:117-130.
26. Martin K, Helenius A. 1991. Transport of incoming influenza virus nucleocapsids into the nucleus. J. Virol. 65:232-244.
27. Mena I, Vivo A, Perez E, Portela A. 1996. Rescue of a synthetic chloramphenicol acetyltransferase RNA into influenza virus-like particles obtained from recombinant plasmids. J. Virol. 70:5016 -5024.
28. Neumann G, Hughes MT, Kawaoka Y. 2000. Influenza A virus NS2 protein mediates vRNP nuclear export through NES-independent interaction with hCRM1. EMBO J. 19:6751- 6758.
29. Neumann G, et al. 1999. Generation of influenza A viruses entirely from cloned cDNAs. Proc. Natl. Acad. Sci. U. S. A. 96:9345-9350.
30. Neumann G, Watanabe T, Kawaoka Y. 2000. Plasmid-driven formation of influenza virus-like particles. J. Virol. 74:547-551.
31. Niwa H, Yamamura K, Miyazaki J. 1991. Efficient selection for highexpression transfectants with a novel eukaryotic vector. Gene 108: 193-199.
32. Noda T, et al. 2006. Architecture of ribonucleoprotein complexes in influenza A virus particles. Nature 439:490-492.
33. O'Neill RE, Talon J, Palese P. 1998. The influenza virus NEP (NS2 protein) mediates the nuclear export of viral ribonucleoproteins.EMBOJ. 17:288-296.
34. Ozawa M, et al. 2007. Contributions of two nuclear localization signals of influenza A virus nucleoprotein to viral replication. J. Virol. 81:30-41.
35. Patterson S, Gross J, Oxford JS. 1988. The intracellular distribution of influenza virus matrix protein and nucleoprotein in infected cells and their relationship to haemagglutinin in the plasma membrane. J. Gen. Virol. 69(Pt 8):1859-1872.
36. Perez DR, Donis RO. 1998. The matrix 1 protein of influenza A virus inhibits the transcriptase activity of a model influenza reporter genome in vivo. Virology 249:52- 61.
37. Pinto LH, Holsinger LJ, Lamb RA. 1992. Influenza virus M2 protein has ion channel activity. Cell 69:517-528.
38. Rees PJ, Dimmock NJ. 1981. Electrophoretic separation of influenza virus ribonucleoproteins. J. Gen. Virol. 53:125-132.
39. Rey O, Nayak DP. 1992. Nuclear retention of M1 protein in a temperature-sensitive mutant of influenza (A/WSN/33) virus does not affect nuclear export of viral ribonucleoproteins. J. Virol. 66:5815-5824.
40. Robb NC, Smith M, Vreede FT, Fodor E. 2009. NS2/NEP protein regulates transcription and replication of the influenza virus RNA genome. J. Gen. Virol. 90:1398-1407.
41. Robertson BH, Bennett JC, Compans RW. 1982. Selective dansylation of M protein within intact influenza virions. J. Virol. 44:871-876.
42. Sarkar G, Sommer SS. 1990. The "megaprimer" method of site-directed mutagenesis. Biotechniques 8:404-407.
43. Sha B, Luo M. 1997. Structure of a bifunctional membrane-RNA binding protein, influenza virus matrix protein M1. Nat. Struct. Biol. 4:239-244.
44. Shimizu T, Takizawa N, Watanabe K, Nagata K, Kobayashi N. 2011. Crucial role of the influenza virus NS2 (NEP) C-terminal domain in M1 binding and nuclear export of vRNP. FEBS Lett. 585:41- 46.
45. Sugrue RJ, Hay AJ. 1991. Structural characteristics of the M2 protein of influenza A viruses: evidence that it forms a tetrameric channel. Virology 180:617- 624.
46. Wakefield L, Brownlee GG. 1989. RNA-binding properties of influenza A virus matrix protein M1. Nucleic Acids Res. 17:8569-8580.
47. Wang D, et al. 2010. The lack of an inherent membrane targeting signal is responsible for the failure of the matrix (M1) protein of influenza A virus to bud into virus-like particles. J. Virol. 84:4673-4681.
48. Watanabe K, Handa H, Mizumoto K, Nagata K. 1996. Mechanism for inhibition of influenza virusRNApolymerase activity by matrix protein. J. Virol. 70:241-247.
49. Whittaker G, Bui M, Helenius A. 1996. Nuclear trafficking of influenza virus ribonuleoproteins in heterokaryons. J. Virol. 70:2743-2756.
50. Whittaker G, Bui M, Helenius A. 1996. The role of nuclear import and export in influenza virus infection. Trends Cell Biol. 6:67-71.
51. Whittaker G, Kemler I, Helenius A. 1995. Hyperphosphorylation of mutant influenza virus matrix protein, M1, causes its retention in the nucleus. J. Virol. 69:439-445.
52. Ye Z, Liu T, Offringa DP, McInnis J, Levandowski RA. 1999. Association of influenza virus matrix protein with ribonucleoproteins. J. Virol. 73:7467-7473.
53. Ye Z, Robinson D, Wagner RR. 1995. Nucleus-targeting domain of the matrix protein (M1) of influenza virus. J. Virol. 69:1964 -1970.
54. Ye ZP, Baylor NW, Wagner RR. 1989. Transcription-inhibition and RNA-binding domains of influenza A virus matrix protein mapped with anti-idiotypic antibodies and synthetic peptides. J. Virol. 63:3586-3594.
55. Ye ZP, Pal R, Fox JW, Wagner RR. 1987. Functional and antigenic domains of the matrix (M1) protein of influenza A virus. J. Virol. 61: 239-246.
56. Zvonarjev AY, Ghendon YZ. 1980. Influence of membrane (M) protein on influenza A virus virion transcriptase activity in vitro and its susceptibility to rimantadine. J. Virol. 33:583-586.