Nuclear export of influenza viral ribonucleoprotein is temperature-dependently inhibited by dissociation of viral matrix protein

Virology

Volumn 306, Issue 2, 2003, Pages 244-253

  Sakaguchi, Atsushi ^a   Hirayama, Etsuko ^a   Hiraki, Akihiro ^a   Ishida, Yo Ichi ^a   Kim, Jeman ^a  

^a KYOTO PHARMACEUTICAL UNIVERSITY   (Japan)

Author keywords

Influenza virus; Nuclear export; Ribonucleoprotein; Temperature dependency; Viral matrix protein

Indexed keywords

MATRIX PROTEIN; NUCLEAR PROTEIN; RIBONUCLEOPROTEIN; RNA POLYMERASE; VIRUS PROTEIN;

ANIMAL CELL; ARTICLE; CELL FUNCTION; CELL MEMBRANE; CELL NUCLEUS; CYTOPATHOGENIC EFFECT; CYTOPLASM; DISSOCIATION; HOST CELL; IMMUNOFLUORESCENCE TEST; IMMUNOPRECIPITATION; INFLUENZA VIRUS; NONHUMAN; NUCLEOCYTOPLASMIC TRANSPORT; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN SYNTHESIS; PROTEIN TRANSPORT; TEMPERATURE DEPENDENCE; VIRUS REPLICATION;

INFLUENZA VIRUS;

EID: 0037440711     PISSN: 00426822     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0042-6822(02)00013-2     Document Type: Article

References (39)

1. Bucher D., Popple S., Baer M., Mikhail A., Gong Y.F., Whitaker C., Paoletti E., Judd A. M protein (M1) of influenza virus antigenic analysis and intracellular localization with monoclonal antibodies . J. Virol. 63:1989;3622-3633.
2. Bui M., Wills E.G., Helenius A., Whittaker G.R. Role of the influenza virus M1 protein in nuclear export of viral ribonucleoproteins. J. Virol. 74:2000;1781-1786.
3. Bui M., Myers J.E., Whittaker G.R. Nucleo-cytoplasmic localization of influenza virus nucleoprotein depends on cell density and phosphorylation. Virus Res. 84:2002;37-44.
4. Cadd T.L., Skoging U., Liljestrom P. Budding of enveloped viruses from the plasma membrane. Bioessays. 19:1997;993-1000.
5. Chu C.M., Tian S.F., Ren G.F., Zhang Y.M., Zhang L.X., Liu G.Q. Occurrence of temperature-sensitive influenza A viruses in nature. J. Virol. 41:1982;353-359.
6. Elton D., Simpson-Holley M., Archer K., Medcalf L., Hallam R., McCauley J., Digard P. Interaction of the influenza virus nucleoprotein with the cellular CRM1-mediated nuclear export pathway. J. Virol. 75:2001;408-419.
7. Fornerod M., Ohno M., Yoshida M., Mattaj I.W. CRM1 is an export receptor for leucine-rich nuclear export signals. Cell. 90:1997;1051-1060.
8. Giesendorf B., Bosch F.X., Wahn K., Rott R. Temperature sensitivity in maturation of mammalian influenza A viruses. Virus Res. 1:1984;655-667.
9. Hamaguchi M., Maeno K., Yoshida T., Nagai Y., Iinuma M., Matsumoto T. Analysis of nuclear accumulation of influenza nucleoprotein antigen using a temperature-sensitive mutant. Microbiol. Immunol. 29:1985;1131-1137.
10. Hirayama E., Udaka Y., Kawai T., Kim J. Characterization of heterokaryons between skeletal myoblasts and somatic cells formed by fusion with HVJ (Sendai virus); effects on myogenic differentiation. Cell Struct. Funct. 26:2001;37-47.
11. Hyodo N., Kim J. Preparation and characterization of a monoclonal antibody that inhibits myoblast fusion of avian skeletal myoblasts. Exp. Cell Res. 212:1994;120-131.
12. Ishida, Y., Hiraki, A., Hirayama, E., Koga, Y., Kim, J., 2002. Temperature-sensitive viral infection: inhibition of hemagglutinating virus of Japan (Sendai virus)-infection at 41°C. Intervirology 45, 125-135.
13. Kendal A.P., Galphin J.C., Palmer E.L. Replication of influenza virus at elevated temperatures Production of virus-like particles with reduced matrix protein content . Virology. 76:1977;186-195.
14. Kielian M., Jungerwirth S. Mechanisms of enveloped virus entry into cells. Mol. Biol. & Med. 7:1990;17-31.
15. Kim J., Adachi T., Hirayama E., Yabubayashi T., Okada Y. Differentiation of quail myoblasts transformed with a temperature sensitive mutant of Rous sarcoma virus. I. Relationship between differentiation and tyrosine kinase of src gene product. Cell Struct. Funct. 17:1992;237-247.
16. Kim J., Adachi T., Saiuchi M., Asada A. Differentiation of quail myoblasts transformed with a temperature sensitive mutant of Rous sarcoma virus. II. Relationship of myoblast fusion with calcium and temperature. Cell Struct. Funct. 17:1992;249-255.
17. Kim J., Adachi T., Yoneda Y., Okada Y. Fusion of Mardin-Darby canine kidney cells by HVJ (Sendai virus) absence of direct association of virus particles with the site of membrane fusion . Eur. J. Cell Biol. 51:1990;128-134.
18. Kim J., Saiuchi M., Adachi T. Morphological characters and disturbance of myofibril assembly in avian myoblasts fused with HVJ (Sendai virus). Eur. J. Cell Biol. 66:1995;94-105.
19. Knudsen K.A., Horwitz A.F. Tandem events in myoblast fusion. Dev. Biol. 58:1977;328-338.
20. Kudo N., Wolff B., Sekimoto T., Schreiner E.P., Yoneda Y., Yanagida M., Horinouchi S., Yoshida M. Leptomycin B inhibition of signal-mediated nuclear export by direct binding to CRM1. Exp. Cell Res. 242:1998;540-547 doi:10.1006/excr.1998.4136.
21. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227:1970;680-685.
22. Lamb R.A., Krug R.M. Orthomyxoviridae: The viruses and their replication. Fields B.N., Knipe D.M., Howley P.M. Fields Virology. 1996;1353-1395 Lippincott-Raven, Philadelphia, PA.
23. Ma K., Roy A.M., Whittaker G.R. Nuclear export of influenza virus ribonucleoproteins identification of an export intermediate at the nuclear periphery . Virology. 282:2001;215-220 doi:10.1006/viro.2001.0833.
24. Martin K., Helenius A. Nuclear transport of influenza virus ribonucleoproteins the viral matrix protein (M1) promotes export and inhibits import . Cell. 67:1991;117-130.
25. Martin K., Helenius A. Transport of incoming influenza virus nucleocapsids into the nucleus. J. Virol. 65:1991;232-244.
26. Neumann G., Castrucci M.R., Kawaoka Y. Nuclear import and export of influenza virus nucleoprotein. J. Virol. 71:1997;9690-9700.
27. Neumann G., Hughes M.T., Kawaoka Y. Influenza A virus NS2 protein mediates vRNP nuclear export through NES-independent interaction with hCRM1. EMBO J. 19:2000;6751-6758.
28. Nishi K., Yoshida M., Fujiwara D., Nishikawa M., Horinouchi S., Beppu T. Leptomycin B targets a regulatory cascade of crm1, a fission yeast nuclear protein, involved in control of higher order chromosome structure and gene expression. J. Biol. Chem. 269:1994;6320-6324.
29. O'Neill R.E., Jaskunas R., Blobel G., Palese P., Moroianu J. Nuclear import of influenza virus RNA can be mediated by viral nucleoprotein and transport factors required for protein import. J. Biol. Chem. 270:1995;22701-22704.
30. O'Neill R.E., Talon J., Palese P. The influenza virus NEP (NS2 protein) mediates the nuclear export of viral ribonucleoproteins. EMBO J. 17:1998;288-296.
31. Oxford J.S., Corcoran T., Schild G.C. Naturally occurring temperature-sensitive influenza A viruses of the H1N1 and H3N2 subtypes. J. Gen. Virol. 48:1980;383-389.
32. Pleschka S., Wolff T., Ehrhardt C., Hobom G., Planz O., Rapp U.R., Ludwig S. Influenza virus propagation is impaired by inhibition of the Raf/MEK/ERK signaling cascade. Nat. Cell Biol. 3:2001;301-305.
33. Saiuchi M., Nunoura N., Kim J. Preparation of a monoclonal antibody and expression of its antigen associated with myogenic differentiation on spontaneous and artificial myotubes derived from avian myoblasts. Cell Struct. Funct. 18:1993;285-296.
34. Salk J.E. A simplified procedure for titrating hemagglutinating capacity of influenza-virus and the corresponding antibody. J. Immunol. 49:1944;87-98.
35. Scholtissek C., Rott R. Effect of temperature on the multiplication of an influenza virus. J. Gen. Virol. 5:1969;283-290.
36. Tachibana T., Hieda M., Sekimoto T., Yoneda Y. Exogenously injected nuclear import factor p10/NTF2 inhibits signal-mediated nuclear import and export of proteins in living cells. FEBS Lett. 397:1996;177-182.
37. Whittaker G., Bui M., Helenius A. Nuclear trafficking of influenza virus ribonucleoproteins in heterokaryons. J. Virol. 70:1996;2743-2756.
38. Yamaoka M., Homma M., Hotta H. MDCK cell cultures supplemented with high concentrations of trypsin exhibit remarkable susceptibility to influenza C virus. Arch. Virol. 140:1995;937-944.
39. Ye Z., Liu T., Offringa D.P., Mclnnis J., Levandowski R.A. Association of influenza virus matrix protein with ribonucleoproteins. J. Virol. 73:1999;7467-7473.