1887

Abstract

All viruses with negative-sense RNA genomes encode a single-strand RNA-binding nucleoprotein (NP). The primary function of NP is to encapsidate the virus genome for the purposes of RNA transcription, replication and packaging. The purpose of this review is to illustrate using the influenza virus NP as a well-studied example that the molecule is much more than a structural RNA-binding protein, but also functions as a key adapter molecule between virus and host cell processes. It does so through the ability to interact with a wide variety of viral and cellular macromolecules, including RNA, itself, two subunits of the viral RNA-dependent RNA polymerase and the viral matrix protein. NP also interacts with cellular polypeptides, including actin, components of the nuclear import and export apparatus and a nuclear RNA helicase. The evidence for the existence of each of these activities and their possible roles in transcription, replication and intracellular trafficking of the virus genome is considered.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-83-4-723
2002-04-01
2019-10-19
Loading full text...

Full text loading...

/deliver/fulltext/jgv/83/4/0830723a.html?itemId=/content/journal/jgv/10.1099/0022-1317-83-4-723&mimeType=html&fmt=ahah

References

  1. Albo, C., Valencia, A. & Portela, A. ( 1995; ). Identification of an RNA binding region within the N-terminal third of the influenza A virus nucleoprotein. Journal of Virology 69, 3799-3806.
    [Google Scholar]
  2. Arrese, M. & Portela, A. ( 1996; ). Serine 3 is critical for phosphorylation at the N-terminal end of the nucleoprotein of influenza virus A/Victoria/3/75. Journal of Virology 70, 3385-3391.
    [Google Scholar]
  3. Avalos, R. T., Yu, Z. & Nayak, D. P. ( 1997; ). Association of influenza virus NP and M1 proteins with cellular cytoskeletal elements in influenza virus-infected cells. Journal of Virology 71, 2947-2958.
    [Google Scholar]
  4. Baudin, F., Bach, C., Cusack, S. & Ruigrok, R. W. H. ( 1994; ). Structure of influenza RNP. I. Influenza virus nucleoprotein melts secondary structure in panhandle RNA and exposes the bases to solvent. EMBO Journal 13, 3158-3165.
    [Google Scholar]
  5. Beaton, A. R. & Krug, R. M. ( 1986; ). Transcription antitermination during influenza viral template RNA synthesis requires the nucleocapsid proteins and the absence of a 5′ capped end. Proceedings of the National Academy of Sciences, USA 83, 6282-6286.[CrossRef]
    [Google Scholar]
  6. Bishop, D. H. L., Obijeski, J. F. & Simpson, R. W. ( 1971; ). Transcription of the influenza ribonucleic acid genome by a virion polymerase. I. Optimal conditions for in vitro activity of the ribonucleic acid-dependent ribonucleic acid polymerase. Journal of Virology 8, 66-73.
    [Google Scholar]
  7. Biswas, S. K., Boutz, P. L. & Nayak, D. P. ( 1998; ). Influenza virus nucleoprotein interacts with influenza virus polymerase proteins. Journal of Virology 72, 5493-5501.
    [Google Scholar]
  8. Breitenfeld, P. M. & Schafer, W. ( 1957; ). The formation of fowl plague antigens in infected cells, as studied with fluorescent antibodies. Virology 4, 328-345.[CrossRef]
    [Google Scholar]
  9. Bui, M., Wills, E. G., Helenius, A. & Whittaker, G. R. ( 2000; ). Role of the influenza virus M1 protein in nuclear export of viral ribonucleoproteins. Journal of Virology 74, 1781-1786.[CrossRef]
    [Google Scholar]
  10. Bullido, R., Gómez-Puertas, P., Albo, C. & Portela, A. ( 2000; ). Several protein regions contribute to determine the nuclear and cytoplasmic localization of the influenza A virus nucleoprotein. Journal of General Virology 81, 135-142.
    [Google Scholar]
  11. Cianci, C., Tiley, L. & Krystal, M. ( 1995; ). Differential activation of the influenza virus polymerase via template RNA binding. Journal of Virology 69, 3995-3999.
    [Google Scholar]
  12. Compans, R. W., Content, J. & Duesberg, P. H. ( 1972; ). Structure of the ribonucleoprotein of influenza virus. Journal of Virology 10, 795-800.
    [Google Scholar]
  13. Davey, J., Dimmock, N. J. & Colman, A. ( 1985; ). Identification of the sequence responsible for the nuclear accumulation of the influenza virus nucleoprotein in Xenopus oocytes. Cell 40, 667-675.[CrossRef]
    [Google Scholar]
  14. Digard, P., Elton, D., Bishop, K., Medcalf, E., Weeds, A. & Pope, B. ( 1999; ). Modulation of nuclear localization of the influenza virus nucleoprotein through interaction with actin filaments. Journal of Virology 73, 2222-2231.
    [Google Scholar]
  15. Duesberg, P. H. ( 1969; ). Distinct subunits of the ribonucleoprotein of influenza virus. Journal of Molecular Biology 42, 485-499.[CrossRef]
    [Google Scholar]
  16. Elton, D., Medcalf, L., Bishop, K. & Digard, P. ( 1999a; ). Oligomerization of the influenza virus nucleoprotein: identification of positive and negative sequence elements. Virology 260, 190-200.[CrossRef]
    [Google Scholar]
  17. Elton, D., Medcalf, L., Bishop, K., Harrison, D. & Digard, P. ( 1999b; ). Identification of amino acid residues of influenza virus nucleoprotein essential for RNA binding. Journal of Virology 73, 7357-7367.
    [Google Scholar]
  18. Elton, D., Simpson-Holley, M., Archer, K., Medcalf, L., Hallam, R., McCauley, J. & Digard, P. ( 2001; ). Interaction of the influenza virus nucleoprotein with the cellular CRM1-mediated nuclear export pathway. Journal of Virology 75, 408-419.[CrossRef]
    [Google Scholar]
  19. Fodor, E., Pritlove, D. C. & Brownlee, G. G. ( 1994; ). The influenza virus panhandle is involved in the initiation of transcription. Journal of Virology 68, 4092-4096.
    [Google Scholar]
  20. Fodor, E., Devenish, L., Engelhardt, O. G., Palese, P., Brownlee, G. G. & Garcia-Sastre, A. ( 1999; ). Rescue of influenza A virus from recombinant DNA. Journal of Virology 73, 9679-9682.
    [Google Scholar]
  21. Fornerod, M., Ohno, M., Yoshida, M. & Mattaj, I. W. ( 1997; ). CRM1 is an export receptor for leucine-rich nuclear export signals. Cell 90, 1051-1060.[CrossRef]
    [Google Scholar]
  22. Galarza, J. M., Sowa, A., Hill, V. M., Skorko, R. & Summers, D. F. ( 1992; ). Influenza A virus NP protein expressed in insect cells by a recombinant baculovirus is associated with a protein kinase activity and possesses single-stranded RNA binding activity. Virus Research 24, 91-106.[CrossRef]
    [Google Scholar]
  23. Gómez-Puertas, P., Albo, C., Pérez-Pastrana, E., Vivo, A. & Portela, A. ( 2000; ). Influenza virus matrix protein is the major driving force in virus budding. Journal of Virology 74, 11538-11547.[CrossRef]
    [Google Scholar]
  24. Gorlich, D., Prehn, S., Laskey, R. A. & Hartmann, E. ( 1994; ). Isolation of a protein that is essential for the first step of nuclear protein import. Cell 79, 767-778.[CrossRef]
    [Google Scholar]
  25. Hagen, M., Chung, T. D. Y., Butcher, J. A. & Krystal, M. ( 1994; ). Recombinant influenza virus polymerase: requirement of both 5′ and 3′ viral ends for endonuclease activity. Journal of Virology 68, 1509-1515.
    [Google Scholar]
  26. Hay, A. J., Lomniczi, B., Bellamy, A. R. & Skehel, J. J. ( 1977; ). Transcription of the influenza virus genome. Virology 83, 337-355.[CrossRef]
    [Google Scholar]
  27. Hay, A. J., Skehel, J. J. & McCauley, J. ( 1982; ). Characterization of influenza virus RNA complete transcripts. Virology 116, 517-522.[CrossRef]
    [Google Scholar]
  28. Herz, C., Stavnezer, E., Krug, R. M. & Gurney, T.Jr ( 1981; ). Influenza virus, an RNA virus, synthesizes its messenger RNA in the nucleus of infected cells. Cell 26, 391-400.[CrossRef]
    [Google Scholar]
  29. Honda, A., Ueda, K., Nagata, K. & Ishihama, A. ( 1988; ). RNA polymerase of influenza virus: role of NP in RNA chain elongation. Journal of Biochemistry 104, 1021-1026.
    [Google Scholar]
  30. Hsu, M.-T., Parvin, J. D., Gupta, S., Krystal, M. & Palese, P. ( 1987; ). Genomic RNAs of influenza viruses are held in a circular conformation in virions and in infected cells by a terminal panhandle. Proceedings of the National Academy of Sciences, USA 84, 8140-8144.[CrossRef]
    [Google Scholar]
  31. Huang, X., Liu, T., Muller, J., Levandowski, R. A. & Ye, Z. ( 2001; ). Effect of influenza virus matrix protein and viral RNA on ribonucleoprotein formation and nuclear export. Virology 287, 405-416.[CrossRef]
    [Google Scholar]
  32. Husain, M. & Gupta, C. M. ( 1997; ). Interactions of viral matrix protein and nucleoprotein with the host cell cytoskeletal actin in influenza viral infection. Current Science 73, 40-47.
    [Google Scholar]
  33. Jennings, P. A., Finch, J. T., Winter, G. & Robertson, J. S. ( 1983; ). Does the higher order structure of the influenza virus ribonucleoprotein guide sequence rearrangements in influenza viral RNA? Cell 34, 619-627.[CrossRef]
    [Google Scholar]
  34. Kingsbury, D. W. & Webster, R. G. ( 1969; ). Some properties of influenza virus nucleocapsids. Journal of Virology 4, 219-225.
    [Google Scholar]
  35. Kingsbury, D. W., Jones, I. M. & Murti, K. G. ( 1987; ). Assembly of influenza ribonucleoprotein in vitro using recombinant nucleoprotein. Virology 156, 396-403.[CrossRef]
    [Google Scholar]
  36. Kistner, O., Müller, H., Becht, H. & Scholtissek, C. ( 1985; ). Phosphopeptide fingerprints of nucleoproteins of various influenza A virus strains grown in different host cells. Journal of General Virology 66, 465-472.[CrossRef]
    [Google Scholar]
  37. Kistner, O., Müller, K. & Scholtissek, C. ( 1989; ). Differential phosphorylation of the nucleoprotein of influenza A viruses. Journal of General Virology 70, 2421-2431.[CrossRef]
    [Google Scholar]
  38. Klumpp, K., Ruigrok, R. W. H. & Baudin, F. ( 1997; ). Roles of the influenza virus polymerase and nucleoprotein in forming a functional RNP structure. EMBO Journal 16, 1248-1257.[CrossRef]
    [Google Scholar]
  39. Kobayashi, M., Toyoda, T., Adyshev, D. M., Azuma, Y. & Ishihama, A. ( 1994; ). Molecular dissection of influenza virus nucleoprotein: deletion mapping of the RNA binding domain. Journal of Virology 68, 8433-8436.
    [Google Scholar]
  40. Krug, R. M., Ueda, M. & Palese, P. ( 1975; ). Temperature-sensitive mutants of influenza WSN virus defective in virus-specific RNA synthesis. Journal of Virology 16, 790-796.
    [Google Scholar]
  41. Kudo, N., Wolff, B., Sekimoto, T., Schreiner, E. P., Yoneda, Y., Yanagida, M., Horinouchi, S. & Yoshida, M. ( 1998; ). Leptomycin B inhibition of signal-mediated nuclear export by direct binding to CRM1. Experimental Cell Research 242, 540-547.[CrossRef]
    [Google Scholar]
  42. Kurokawa, M., Ochiai, H., Nakajima, K. & Niwayama, S. ( 1990; ). Inhibitory effect of protein kinase C inhibitor on the replication of influenza type A virus. Journal of General Virology 71, 2149-2155.[CrossRef]
    [Google Scholar]
  43. Lin, B.-C. & Lai, C.-J. ( 1983; ). The influenza virus nucleoprotein synthesized from cloned DNA in a simian virus 40 vector is detected in the nucleus. Journal of Virology 45, 434-438.
    [Google Scholar]
  44. Londo, D. R., Davis, A. R. & Nayak, D. P. ( 1983; ). Complete nucleotide sequence of the nucleoprotein gene of influenza B virus. Journal of Virology 47, 642-648.
    [Google Scholar]
  45. Ma, K., Roy, A. M. M. & Whittaker, G. R. ( 2001; ). Nuclear export of influenza virus ribonucleoproteins: identification of an export intermediate at the nuclear periphery. Virology 282, 215-220.[CrossRef]
    [Google Scholar]
  46. Maeno, K. & Kilbourne, E. D. ( 1970; ). Developmental sequence and intracellular sites of synthesis of three structural protein antigens of influenza A2 virus. Journal of Virology 5, 153-164.
    [Google Scholar]
  47. Mahy, B. W. J. ( 1983; ). Mutants of influenza virus. In Genetics of Influenza Virus , pp. 192-254. Edited by P. Palese & D. W. Kingsbury. New York:Springer-Verlag.
  48. Mahy, B. W. J., Barret, T., Nichol, S. T., Penn, C. R. & Wolstenholme, A. J. ( 1981; ). Analysis of the functions of influenza virus genome RNA segments by the use of temperature-sensitive mutants of fowl plague virus. In The Replication of Negative Strand Viruses , pp. 379-387. Edited by D. H. L. Bishop & R. W. Compans. Amsterdam:Elsevier.
  49. Mandler, J., Müller, K. & Scholtissek, C. ( 1991; ). Mutants and revertants of an avian influenza A virus with temperature-sensitive defects in the nucleoprotein and PB2. Virology 181, 512-519.[CrossRef]
    [Google Scholar]
  50. Markushin, S. G. & Ghendon, Y. Z. ( 1984; ). Studies of fowl plague virus temperature-sensitive mutants with defects in synthesis of virion RNA. Journal of General Virology 65, 559-575.[CrossRef]
    [Google Scholar]
  51. 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.[CrossRef]
    [Google Scholar]
  52. Martı́n-Benito, J., Area, E., Ortega, J., Llorca, O., Valpuesta, J. M., Carrascosa, J. L. & Ortı́n, J. ( 2001; ). Three-dimensional reconstruction of a recombinant influenza virus ribonucleoprotein particle. EMBO Reports 2, 313-317.[CrossRef]
    [Google Scholar]
  53. Medcalf, E., Poole, E., Elton, D. & Digard, P. ( 1999; ). Temperature-sensitive lesions in two influenza A viruses defective for replicative transcription disrupt RNA-binding by the nucleoprotein. Journal of Virology 73, 7349-7356.
    [Google Scholar]
  54. Mena, I., Jambrina, E., Albo, C., Perales, B., Ortı́n, J., Arrese, M., Vallejo, D. & Portela, A. ( 1999; ). Mutational analysis of influenza A virus nucleoprotein: identification of mutations that affect RNA replication. Journal of Virology 73, 1186-1194.
    [Google Scholar]
  55. Momose, F., Handa, H. & Nagata, K. ( 1996; ). Identification of host factors that regulate the influenza virus RNA polymerase activity. Biochimie 78, 1103-1108.[CrossRef]
    [Google Scholar]
  56. Momose, F., Basler, C. F., O’Neill, R. E., Iwamatsu, A., Palese, P. & Nagata, K. ( 2001; ). Cellular splicing factor RAF-2p48/NPI-5/BAT1/UAP56 interacts with the influenza virus nucleoprotein and enhances viral RNA synthesis. Journal of Virology 75, 1899-1908.[CrossRef]
    [Google Scholar]
  57. Moroianu, J., Blobel, G. & Radu, A. ( 1995; ). Previously identified protein of uncertain function is karyopherin α and together with karyopherin β docks import substrate at nuclear pore complexes. Proceedings of the National Academy of Sciences, USA 92, 2008-2011.[CrossRef]
    [Google Scholar]
  58. Naffakh, N., Massin, P., Escriou, N., Crescenzo-Chaigne, B. & van der Werf, S. ( 2000; ). Genetic analysis of the compatibility between polymerase proteins from human and avian strains of influenza A viruses. Journal of General Virology 81, 1283-1291.
    [Google Scholar]
  59. Nakada, S., Creager, R. S., Krystal, M. & Palese, P. ( 1984; ). Complete nucleotide sequence of the influenza C/California/78 virus nucleoprotein gene. Virus Research 1, 433-441.[CrossRef]
    [Google Scholar]
  60. Neumann, G., Castrucci, M. R. & Kawaoka, Y. ( 1997; ). Nuclear import and export of influenza virus nucleoprotein. Journal of Virology 71, 9690-9700.
    [Google Scholar]
  61. Neumann, G., Watanabe, T., Ito, H., Watanabe, S., Goto, H., Gao, P., Hughes, M., Perez, D. R., Donis, R., Hoffmann, E., Hobom, G. & Kawaoka, Y. ( 1999; ). Generation of influenza A viruses entirely from cloned cDNAs. Proceedings of the National Academy of Sciences, USA 96, 9345-9350.[CrossRef]
    [Google Scholar]
  62. Neumann, G., Hughes, M. T. & Kawaoka, Y. ( 2000; ). Influenza A virus NS2 protein mediates vRNP nuclear export through NES-independent interaction with hCRM1. EMBO Journal 19, 6751-6758.[CrossRef]
    [Google Scholar]
  63. O’Neill, R. E. & Palese, P. ( 1995; ). NPI-1, the human homolog of SRP-1, interacts with influenza virus nucleoprotein. Virology 206, 116-125.[CrossRef]
    [Google Scholar]
  64. O’Neill, R. E., Jaskunas, R., Blobel, G., Palese, P. & Moroianu, J. ( 1995; ). Nuclear import of influenza virus RNA can be mediated by viral nucleoprotein and transport factors required for protein import. Journal of Biological Chemistry 270, 22701-22704.[CrossRef]
    [Google Scholar]
  65. O’Neill, R. E., Talon, J. & Palese, P. ( 1998; ). The influenza virus NEP (NS2 protein) mediates the nuclear export of viral ribonucleoproteins. EMBO Journal 17, 288-296.[CrossRef]
    [Google Scholar]
  66. Ortega, J., Martı́n-Benito, J., Zurcher, T., Valpuesta, J. M., Carrascosa, J. L. & Ortı́n, J. ( 2000; ). Ultrastructural and functional analyses of recombinant influenza virus ribonucleoproteins suggest dimerization of nucleoprotein during virus amplification. Journal of Virology 74, 156-163.[CrossRef]
    [Google Scholar]
  67. Osborne, J. C. & Elliott, R. M. ( 2000; ). RNA binding properties of bunyamwera virus nucleocapsid protein and selective binding to an element in the 5′ terminus of the negative-sense S segment. Journal of Virology 74, 9946-9952.[CrossRef]
    [Google Scholar]
  68. Palese, P., Wang, P., Wolff, T. & O’Neill, R. E. ( 1997; ). Host–viral protein–protein interactions in influenza virus replication. In Molecular Aspects of Host–Pathogen Interactions , pp. 327-340. Edited by M. A. McCrae, J. R. Saunders, C. J. Smyth & N. D. Stow. Cambridge:Cambridge University Press.
  69. Paragas, J., Talon, J., O’Neill, R. E., Anderson, D. K., Garcı́a-Sastre, A. & Palese, P. ( 2001; ). Influenza B and C virus NEP (NS2) proteins possess nuclear export activities. Journal of Virology 75, 7375-7383.[CrossRef]
    [Google Scholar]
  70. Plotch, S. J., Bouloy, M., Ulmanen, I. & Krug, R. M. ( 1981; ). A unique cap(m7GpppXm)-dependent influenza virion endonuclease cleaves capped RNAs to generate the primers that initiate viral RNA transcription. Cell 23, 847-858.[CrossRef]
    [Google Scholar]
  71. Pons, M. W., Schulze, I. T., Hirst, G. K. & Hauser, R. ( 1969; ). Isolation and characterization of the ribonucleoprotein of influenza virus. Virology 39, 250-259.[CrossRef]
    [Google Scholar]
  72. Poon, L. L. M., Pritlove, D. C., Sharps, J. & Brownlee, G. G. ( 1998; ). The RNA polymerase of influenza virus, bound to the 5′ end of virion RNA, acts in cis to polyadenylate mRNA. Journal of Virology 72, 8214-8219.
    [Google Scholar]
  73. Poon, L. L. M., Pritlove, D. C., Fodor, E. & Brownlee, G. G. ( 1999; ). Direct evidence that the poly(A) tail of influenza A virus mRNA is synthesized by reiterative copying of a U track in the virion RNA template. Journal of Virology 73, 3473-3476.
    [Google Scholar]
  74. Pritlove, D. C., Poon, L. L. M., Fodor, E., Sharps, J. & Brownlee, G. G. ( 1998; ). Polyadenylation of influenza virus mRNA transcribed in vitro from model virion RNA templates: requirement for 5′ conserved sequences. Journal of Virology 72, 1280-1286.
    [Google Scholar]
  75. Privalsky, M. L. & Penhoet, E. E. ( 1978; ). Influenza virus proteins: identity, synthesis, and modification analyzed by two-dimensional gel electrophoresis. Proceedings of the National Academy of Sciences, USA 75, 3625-3629.[CrossRef]
    [Google Scholar]
  76. Rees, P. J. & Dimmock, N. J. ( 1981; ). Electrophoretic separation of influenza virus ribonucleoproteins. Journal of General Virology 53, 125-132.[CrossRef]
    [Google Scholar]
  77. Robertson, J. S., Schubert, M. & Lazzarini, R. A. ( 1981; ). Polyadenylation sites for influenza virus mRNA. Journal of Virology 38, 157-163.
    [Google Scholar]
  78. Ruigrok, R. W. H. & Baudin, F. ( 1995; ). Structure of influenza virus ribonucleoprotein particles. II. Purified RNA-free influenza virus ribonucleoprotein forms structures that are indistinguishable from the intact influenza virus ribonucleoprotein particles. Journal of General Virology 76, 1009-1014.[CrossRef]
    [Google Scholar]
  79. Scholtissek, C. ( 1978; ). The genome of influenza virus. Current Topics in Microbiology and Immunology 80, 139-169.
    [Google Scholar]
  80. Scholtissek, C. & Becht, H. ( 1971; ). Binding of ribonucleic acids to the RNP-antigen protein of influenza viruses. Journal of General Virology 10, 11-16.[CrossRef]
    [Google Scholar]
  81. Seong, B. L., Kobayshi, M., Nagata, K., Brownlee, G. G. & Ishihama, A. ( 1992; ). Comparison of two reconstituted systems for in vitro transcription and replication of influenza virus. Journal of Biochemistry 111, 496-499.
    [Google Scholar]
  82. Severson, W. E., Xu, X. & Jonsson, C. B. ( 2001; ). Cis-acting signals in encapsidation of Hantaan virus S-segment viral genomic RNA by its N protein. Journal of Virology 75, 2646-2652.[CrossRef]
    [Google Scholar]
  83. Shapiro, G. I. & Krug, R. M. ( 1988; ). Influenza virus RNA replication in vitro: synthesis of viral template RNAs and virion RNAs in the absence of an added primer. Journal of Virology 62, 2285-2290.
    [Google Scholar]
  84. Shaw, M. W. & Lamb, R. A. ( 1984; ). A specific sub-set of host-cell mRNAs prime influenza virus mRNA synthesis. Virus Research 1, 455-467.[CrossRef]
    [Google Scholar]
  85. Shimizu, K., Handa, H., Nakada, S. & Nagata, K. ( 1994; ). Regulation of influenza virus RNA polymerase activity by cellular and viral factors. Nucleic Acids Research 22, 5047-5053.[CrossRef]
    [Google Scholar]
  86. Shu, L. L., Bean, W. J. & Webster, R. G. ( 1993; ). Analysis of the evolution and variation of the human influenza A virus nucleoprotein gene from 1933 to 1990. Journal of Virology 67, 2723-2729.
    [Google Scholar]
  87. Simpson, R. W. & Hirst, G. K. ( 1968; ). Temperature-sensitive mutants of influenza A virus: isolation of mutants and preliminary observations on genetic recombination and complementation. Virology 35, 41-49.[CrossRef]
    [Google Scholar]
  88. Skorko, R., Summers, D. F. & Galarza, J. M. ( 1991; ). Influenza A virus in vitro transcription: roles of NS1 and NP proteins in regulating RNA synthesis. Virology 180, 668-677.[CrossRef]
    [Google Scholar]
  89. Thierry, F. & Danos, O. ( 1982; ). Use of specific single stranded DNA probes cloned in M13 to study the RNA synthesis of four temperature-sensitive mutants of HK/68 influenza virus. Nucleic Acids Research 10, 2925-2938.[CrossRef]
    [Google Scholar]
  90. Tiley, L. S., Hagen, M., Matthews, J. T. & Krystal, M. ( 1994; ). Sequence-specific binding of the influenza virus RNA polymerase to sequences located at the 5′ ends of the viral RNAs. Journal of Virology 68, 5108-5116.
    [Google Scholar]
  91. Tordo, N., De Haan, P., Goldbach, R. & Poch, O. ( 1992; ). Evolution of negative-stranded RNA genomes. Seminars in Virology 3, 341-357.
    [Google Scholar]
  92. Wagner, R. R. & Rose, J. K. ( 1995; ). Rhabdoviridae: the viruses and their replication. In Fields Virology , pp. 1121-1135. Edited by B. N. Fields, D. M. Knipe & P. M. Howley. Philadelphia:Lippincott–Raven.
  93. Wakefield, L. & Brownlee, G. G. ( 1989; ). RNA-binding properties of influenza virus matrix protein M1. Nucleic Acids Research 17, 8569-8580.[CrossRef]
    [Google Scholar]
  94. Wang, P., Palese, P. & O’Neill, R. E. ( 1997; ). The NPI-1/NPI-3 (karyopherin α) binding site on the influenza A virus nucleoprotein NP is a nonconventional nuclear localization signal. Journal of Virology 71, 1850-1856.
    [Google Scholar]
  95. Watanabe, K., Takizawa, N., Katoh, M., Hoshida, K., Kobayashi, N. & Nagata, K. ( 2001; ). Inhibition of nuclear export of ribonucleoprotein complexes of influenza virus by leptomycin B. Virus Research 77, 31-42.[CrossRef]
    [Google Scholar]
  96. Weber, F., Kochs, G., Gruber, S. & Haller, O. ( 1998; ). A classical bipartite nuclear localization signal on Thogoto and influenza A virus nucleoproteins. Virology 250, 9-18.[CrossRef]
    [Google Scholar]
  97. Whittaker, G., Kemler, I. & Helenius, A. ( 1995; ). Hyperphosphorylation of mutant influenza virus matrix protein, M1, causes its retention in the nucleus. Journal of Virology 69, 439-445.
    [Google Scholar]
  98. Whittaker, G., Bui, M. & Helenius, A. ( 1996; ). Nuclear trafficking of influenza virus ribonucleoproteins in heterokaryons. Journal of Virology 70, 2743-2756.
    [Google Scholar]
  99. Wolstenholme, A. J., Barrett, T., Nichol, S. T. & Mahy, B. W. ( 1980; ). Influenza virus-specific RNA and protein syntheses in cells infected with temperature-sensitive mutants defective in the genome segment encoding nonstructural proteins. Journal of Virology 35, 1-7.
    [Google Scholar]
  100. Yamanaka, K., Ishihama, A. & Nagata, K. ( 1990; ). Reconstitution of influenza virus RNA–nucleoprotein complexes structurally resembling native viral ribonucleoprotein cores. Journal of Biological Chemistry 265, 11151-11155.
    [Google Scholar]
  101. Yasuda, J., Nakada, S., Kato, A., Toyoda, T. & Ishihama, A. ( 1993; ). Molecular assembly of influenza virus: association of the NS2 protein with virion matrix. Virology 196, 249-255.[CrossRef]
    [Google Scholar]
  102. Ye, Z., Liu, T., Offringa, D. P., McInnis, J. & Levandowski, R. A. ( 1999; ). Association of influenza virus matrix protein with ribonucleoproteins. Journal of Virology 73, 7467-7473.
    [Google Scholar]
  103. Young, R. J. & Content, J. ( 1971; ). 5′-terminus of influenza virus RNA. Nature New Biology 230, 140-142.
    [Google Scholar]
  104. Zvonarjev, A. Y. & Ghendon, Y. Z. ( 1980; ). Influence of membrane (M) protein on influenza A virus virion transcriptase activity in vitro and its susceptibility to rimantadine. Journal of Virology 33, 583-586.
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/0022-1317-83-4-723
Loading
/content/journal/jgv/10.1099/0022-1317-83-4-723
Loading

Data & Media loading...

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error