1887

Abstract

Influenza C virus-like particles (VLPs) have been generated from cloned cDNAs. A cDNA of the green fluorescent protein (GFP) gene in antisense orientation was flanked by the 5′ and 3′ non-coding regions of RNA segment 5 of the influenza C virus. The cDNA cassette was inserted between an RNA polymerase I promoter and terminator of the Pol I vector. This plasmid DNA was transfected into 293T cells together with plasmids encoding virus proteins of C/Ann Arbor/1/50 or C/Yamagata/1/88. Transfer of the supernatants of the transfected 293T cells to HMV-II cells resulted in GFP expression in the HMV-II cells. The quantification of the GFP-positive HMV-II cells indicated the presence of approximately 10 VLPs (ml supernatant). Cords 50−300 μm in length were observed on transfected 293T cells, although the cords were not observed when the plasmid for M1 protein of C/Ann Arbor/1/50 was replaced with that of C/Taylor/1233/47. A series of transfection experiments with plasmids encoding M1 mutants of C/Ann Arbor/1/50 or C/Taylor/1233/47 showed that an amino acid at residue 24 of the M1 protein is responsible for cord formation. This finding provides direct evidence for a previous hypothesis that M1 protein is involved in the formation of cord-like structures protruding from the C/Yamagata/1/88-infected cells. Evidence was obtained by electron microscopy that transfected cells bearing cords produced filamentous VLPs, suggesting the potential role of the M1 protein in determining the filamentous/spherical morphology of influenza C virus.

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2004-07-01
2020-01-27
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References

  1. Bourmakina, S. V. & García-Sastre, A. ( 2003; ). Reverse genetics studies on the filamentous morphology of influenza A virus. J Gen Virol 84, 517–527.[CrossRef]
    [Google Scholar]
  2. Compans, R. W., Bishop, D. H. & Meier-Ewert, H. ( 1977; ). Structural components of influenza C virions. J Virol 21, 658–665.
    [Google Scholar]
  3. Flewett, T. H. & Apostolov, K. ( 1967; ). A reticular structure in the wall of influenza C virus. J Gen Virol 1, 297–304.
    [Google Scholar]
  4. Fodor, E., Devenish, L., Engelhardt, O. G., Palese, P., Brownlee, G. G. & García-Sastre, A. ( 1999; ). Rescue of influenza A virus from recombinant DNA. J Virol 73, 9679–9682.
    [Google Scholar]
  5. Gómez-Puertas, P., Mena, I., Castillo, M., Vivo, A., Pérez-Pastrana, E. & Portela, A. ( 1999; ). Efficient formation of influenza virus-like particles: dependence on the expression levels of viral proteins. J Gen Virol 80, 1635–1645.
    [Google Scholar]
  6. Grambas, S., Bennett, M. S. & Hay, A. J. ( 1992; ). Influence of amantadine resistance mutations on the pH regulatory function of the M2 protein of influenza A viruses. Virology 191, 541–549.[CrossRef]
    [Google Scholar]
  7. Hatta, M. & Kawaoka, Y. ( 2003; ). The NB protein of influenza B virus is not necessary for virus replication in vitro. J Virol 77, 6050–6054.[CrossRef]
    [Google Scholar]
  8. Herrler, G. & Klenk, H. D. ( 1991; ). Structure and function of the HEF glycoprotein of influenza C virus. Adv Virus Res 40, 213–234.
    [Google Scholar]
  9. Herrler, G., Nagele, A., Meier-Ewert, H., Bhown, A. S. & Compans, R. W. ( 1981; ). Isolation and structural analysis of influenza C virion glycoproteins. Virology 113, 439–451.[CrossRef]
    [Google Scholar]
  10. Hoffmann, E., Neumann, G., Kawaoka, Y., Hobom, G. & Webster, R. G. ( 2000; ). A DNA transfection system for generation of influenza A virus from eight plasmids. Proc Natl Acad Sci U S A 97, 6108–6113.[CrossRef]
    [Google Scholar]
  11. Hoffmann, E., Mahmood, K., Ya, C.-F., Webster, R. G., Greenberg, H. B. & Kemble, G. ( 2002; ). Rescue of influenza B virus from eight plasmids. Proc Natl Acad Sci U S A 99, 11411–11416.[CrossRef]
    [Google Scholar]
  12. Hongo, S., Sugawara, K., Nishimura, H., Muraki, Y., Kitame, F. & Nakamura, K. ( 1994; ). Identification of a second protein encoded by influenza C virus RNA segment 6. J Gen Virol 75, 3503–3510.[CrossRef]
    [Google Scholar]
  13. Hongo, S., Peng, G., Sugawara, K., Muraki, Y., Matsuzaki, Y., Tada, Y., Kitame, F. & Nakamura, K. ( 1998; ). Identification of a 374 amino acid protein encoded by RNA segment 6 of influenza C virus. J Gen Virol 79, 2207–2213.
    [Google Scholar]
  14. Hongo, S., Sugawara, K., Muraki, Y., Matsuzaki, Y., Takashita, E., Kitame, F. & Nakamura, K. ( 1999; ). Influenza C virus CM2 protein is produced from a 374 amino acid protein (P42) by signal peptidase cleavage. J Virol 73, 46–50.
    [Google Scholar]
  15. Hongo, S., Ishii, K., Mori, K., Takashita, E., Muraki, Y., Matsuzaki, Y. & Sugawara, K. ( 2004; ). Detection of ion channel activity in Xenopus laevis oocytes expressing influenza C virus CM2 protein. Arch Virol 149, 35–50.
    [Google Scholar]
  16. Jackson, D., Cadman, A., Zurcher, T. & Barclay, W. S. ( 2002; ). A reverse genetics approach for recovery of recombinant influenza B viruses entirely from cDNA. J Virol 76, 11744–11747.[CrossRef]
    [Google Scholar]
  17. Kimura, H., Abiko, C., Gao, P. & 8 other authors ( 1997; ). Interspecies transmission of influenza C virus between humans and pigs. Virus Res 48, 71–79.[CrossRef]
    [Google Scholar]
  18. Lamb, R. A. & Krug, R. M. ( 2001; ). Orthomyxoviridae: the viruses and their replication. In Fields Virology, 4th edn, vol. 1, pp. 1487–1531. Edited by D. M. Knipe & P. M. Howley. Philadelphia: Lippincott Williams & Wilkins.
  19. Matsuzaki, Y., Sugawara, K., Mizuta, K., Tsuchiya, E., Muraki, Y., Hongo, S., Suzuki, H. & Nakamura, K. ( 2002; ). Antigenic and genetic characterization of influenza C viruses which caused two outbreaks in Yamagata City, Japan, in 1996 and 1998. J Clin Microbiol 40, 422–429.[CrossRef]
    [Google Scholar]
  20. Mena, I., Vivo, A., Pérez, 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.
    [Google Scholar]
  21. Neumann, G., Watanabe, T., Ito, H. & 9 other authors ( 1999; ). Generation of influenza A viruses entirely from cloned cDNAs. Proc Natl Acad Sci U S A 96, 9345–9350.[CrossRef]
    [Google Scholar]
  22. Neumann, G., Watanabe, T. & Kawaoka, Y. ( 2000; ). Plasmid-driven formation of influenza virus-like particles. J Virol 74, 547–551.[CrossRef]
    [Google Scholar]
  23. Nishimura, H., Sugawara, K., Kitame, F., Nakamura, K., Katsushima, N., Moriuchi, H. & Numazaki, Y. ( 1989; ). A human melanoma cell line highly susceptible to influenza C virus. J Gen Virol 70, 1653–1661.[CrossRef]
    [Google Scholar]
  24. Nishimura, H., Hara, M., Sugawara, K., Kitame, F., Takiguchi, K., Umetsu, Y., Tonosaki, A. & Nakamura, K. ( 1990; ). Characterization of the cord-like structures emerging from the surface of influenza C virus-infected cells. Virology 179, 179–188.[CrossRef]
    [Google Scholar]
  25. Nishimura, H., Hongo, S., Sugawara, K., Muraki, Y., Kitame, F., Washioka, H., Tonosaki, A. & Nakamura, K. ( 1994; ). The ability of influenza C virus to generate cord-like structures is influenced by the gene coding for M protein. Virology 200, 140–147.[CrossRef]
    [Google Scholar]
  26. Paragas, J., Talon, J., O'Neill, R. E., Anderson, D. K., García-Sastre, A. & Palese, P. ( 2001; ). Influenza B and C virus NEP (NS2) proteins possess nuclear export activities. J Virol 75, 7375–7383.[CrossRef]
    [Google Scholar]
  27. Roberts, P. C., Lamb, R. A. & Compans, R. W. ( 1998; ). The M1 and M2 proteins of influenza A virus are important determinants in filamentous particle formation. Virology 240, 127–137.[CrossRef]
    [Google Scholar]
  28. Sha, B. & Luo, M. ( 1997; ). Structure of a bifunctional membrane-RNA binding protein, influenza virus matrix protein M1. Nat Struct Biol 4, 239–244.[CrossRef]
    [Google Scholar]
  29. Smirnov, Y. A., Kuznetsova, M. A. & Kaverin, N. V. ( 1991; ). The genetic aspects of influenza virus filamentous particle formation. Arch Virol 118, 279–284.[CrossRef]
    [Google Scholar]
  30. Sugawara, K., Nishimura, H., Hongo, S., Kitame, F. & Nakamura, K. ( 1991; ). Antigenic characterization of the nucleoprotein and matrix protein of influenza C virus with monoclonal antibodies. J Gen Virol 72, 103–109.[CrossRef]
    [Google Scholar]
  31. Sugawara, K., Nishimura, H., Hongo, S., Muraki, Y., Kitame, F. & Nakamura, K. ( 1993; ). Construction of an antigenic map of the haemagglutinin–esterase protein of influenza C virus. J Gen Virol 74, 1661–1666.[CrossRef]
    [Google Scholar]
  32. Tada, Y., Hongo, S., Muraki, Y., Sugawara, K., Kitame, F. & Nakamura, K. ( 1997; ). Evolutionary analysis of influenza C virus M genes. Virus Genes 15, 53–59.[CrossRef]
    [Google Scholar]
  33. Takebe, Y., Seiki, M., Fujisawa, J., Hoy, P., Yokota, K., Arai, K., Yoshida, M. & Arai, N. ( 1988; ). SR alpha promoter: an efficient and versatile mammalian cDNA expression system composed of the simian virus 40 early promoter and the R-U5 segment of human T-cell leukemia virus type 1 long terminal repeat. Mol Cell Biol 8, 466–472.
    [Google Scholar]
  34. Wagner, E., Engelhardt, O. G., Weber, F., Haller, O. & Kochs, G. ( 2000; ). Formation of virus-like particles from cloned cDNAs of Thogoto virus. J Gen Virol 81, 2849–2853.
    [Google Scholar]
  35. Wagner, E., Engelhardt, O. G., Gruber, S., Haller, O. & Kochs, G. ( 2001; ). Rescue of recombinant Thogoto virus from cloned cDNA. J Virol 75, 9282–9286.[CrossRef]
    [Google Scholar]
  36. Waterson, A. P., Hurrell, J. M. & Jensen, K. E. ( 1963; ). The fine structure of influenza A, B and C viruses. Arch Gesamte Virusforsch 12, 487–495.[CrossRef]
    [Google Scholar]
  37. Yamashita, M., Krystal, M. & Palese, P. ( 1988; ). Evidence that the matrix protein of influenza C virus is coded for by a spliced mRNA. J Virol 62, 3348–3355.
    [Google Scholar]
  38. Yokota, M., Nakamura, K., Sugawara, K. & Homma, M. ( 1983; ). The synthesis of polypeptides in influenza C virus-infected cells. Virology 130, 105–117.[CrossRef]
    [Google Scholar]
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