Advertisement

Russian Journal of Genetics

, Volume 48, Issue 7, pp 671–678 | Cite as

Genetic diversity and evolution of the influenza C virus

  • A. S. SperanskayaEmail author
  • N. V. Melnikova
  • M. S. Belenikin
  • A. A. Dmitriev
  • N. Yu. Oparina
  • A. V. Kudryavtseva
Theoretical Papers and Reviews

Abstract

The influenza C virus is spread worldwide and causes diseases of the upper and (less frequently) lower respiratory tract in human. The virus is not pandemic, but it circulates together with pandemic influenza A and B viruses during winter months and has quite similar clinical manifestations. The influenza C virus is also encountered in animals (pigs and dogs) and is known to override the interspecific barriers of transmssion. The immune system of mammals often fails to recognize new antigenic variants of influenza C virus, which invariably arise in nature, resulting in outbreaks of diseases, although the structure of antigens in influenza C virus in general is much more stable than those of influenza viruses A and B. Variability of genetic information in natural isolates of viruses is determined by mutations, reassortment, and recombination. However, recombination events very rarely occur in genomes of negative-strand RNA viruses, including those of influenza, and virtually have no effect on their evolution. Unambiguous explanations for this phenomenon have thus far not been proposed. There is no proof of recombination processes in the influenza C virus genome. On the contrary, reassortant viruses derived from different strains of influenza C virus frequently appear in vitro and are likely to be common in nature. The genome of influenza C virus comprises seven segments. Based on the comparison of sequences in one of its genes (HEF), six genetic or antigenic lineages of this virus can be distinguished (Yamagata/26/81, Aichi/1/81, Mississippi/80, Taylor/1233/47, Sao Paulo/378/82, and Kanagawa/1/76). However, the available genetic data show that all the seven segments of the influenza C virus genome evolve independently.

Keywords

Influenza Influenza Virus Hongo Reassortant Virus Influenza Virus Resource 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Matsuzaki, Y., Katsushima, N., Nagai, Y., et al., Clinical Features of Influenza C Virus Infection in Children, J. Infect. Dis., 2006, vol. 193, no. 9, pp. 1229–1235.PubMedCrossRefGoogle Scholar
  2. 2.
    Matsuzaki, Y., Abiko, C., Mizuta, K., et al., A Nationwide Epidemic of Influenza C Virus Infection in Japan in 2004, J. Clin. Microbiol., 2007, vol. 45, no. 3, pp. 783–788.PubMedCrossRefGoogle Scholar
  3. 3.
    Gouarin, S., Vabret, A., Dina, J., et al., Study of Influenza C Virus Infection in France, J. Med. Virol., 2008, vol. 80, no. 8, pp. 1441–1446.PubMedCrossRefGoogle Scholar
  4. 4.
    Han, B.Z., Boni, M.F., and Li, S.S., No Observed Effect of Homologous Recombination on Influenza C Virus Evolution, Virol. J., 2010, vol. 7, p. 227.PubMedCrossRefGoogle Scholar
  5. 5.
    Gatherer, D., Tempo and Mode in the Molecular Evolution of Influenza C, PLoS Curr., 2010, vol. 2: RRN1199.Google Scholar
  6. 6.
    Ohwada, K., Kitame, F., and Homma, M., Experimental Infections of Dogs with Type C Influenza Virus, Microbiol. Immunol., 1986, vol. 30, no. 5, pp. 451–460.PubMedGoogle Scholar
  7. 7.
    Greenbaum, E., Morag, A., and Zakay-Rones, Z., Isolation of Influenza C Virus during an Outbreak of Influenza A and B Viruses, J. Clin. Microbiol., 1998, vol. 36, no. 5, pp. 1441–1442.PubMedGoogle Scholar
  8. 8.
    Yatsyshina, S.B., Minenko, A.N., Kushakova, T.E., et al., Pandemic Influenza A/H1N1(sw2009) in Russia: Epidemiology, Diagnostics, Clinic and Treatment, Ter. Arkh., 2010, no. 11, pp. 10–14.Google Scholar
  9. 9.
    Yatsyshina, S.B., Minenko, A.N., Praded, M.N., et al., Epidemiological Supervision under Influenza during 2009–2010 Pandemic, Mol. Diagn., 2010, vol. 4, pp. 230–244.Google Scholar
  10. 10.
    Yatsyshina, S.B., Praded, M.N., Minenko, A.N., et al., Elaboration and Approbation of the Reagent Kit for Acute Respiratory Diseases’ Diagnostics Using Multipraim-FL PCR, Mol. Diagn., 2010, vol. 4, pp. 244–247.Google Scholar
  11. 11.
    Yatsyshina, S.B., Minenko, A.N., Voloshina, P.V., et al., Molecular-Genetic Characteristics of Pandemic Influenza A/H1N1(sw2009) Viruses Identified in 2009–2010 in Russia, Zh. Mokrobiol. Epidemiol. Immunobiol., 2011, no. 1, pp. 26–34.Google Scholar
  12. 12.
    Bao, Y., Bolotov, P., Dernovoy, D., et al., The Influenza Virus Resource at the National Center for Biotechnology Information, J. Virol., 2008, vol. 82, no. 2, pp. 596–601.PubMedCrossRefGoogle Scholar
  13. 13.
    Matsuzaki, Y., Mizuta, K., Sugawara, K., et al., Frequent Reassortment among Influenza C Viruses, J. Virol., 2003, vol. 77, no. 2, pp. 871–881.PubMedCrossRefGoogle Scholar
  14. 14.
    Coiras, M.T., Prez-Brea, P., Garca, M.L., and Casas, I.J., Simultaneous Detection of Influenza A, B, and C Viruses, Respiratory Syncytial Virus, and Adenoviruses in Clinical Samples by Multiplex Reverse Transcription Nested-PCR Assay, Med. Virol., 2003, vol. 69, no. 1, pp. 1321–1344.Google Scholar
  15. 15.
    Nishimura, H., Hara, M., Sugawara, K., et al., Characterization of the Cord-Like Structures Emerging from the Surface of Influenza C Virus-Infected Cells, Virology, 1990, vol. 179, no. 1, pp. 179–188.PubMedCrossRefGoogle Scholar
  16. 16.
    Nakamura, K., The Ability of Influenza C Virus to Generate Cord-Like Structures Is Influenced by the Gene Coding for M Protein, Virology, 1994, vol. 200, no. 1, pp. 140–147.PubMedCrossRefGoogle Scholar
  17. 17.
    Muraki, Y. and Hongo, S., The Molecular Virology and Reverse Genetics of Influenza C Virus, Jpn. J. Dis., 2010, vol. 63, no. 3, pp. 157–165.Google Scholar
  18. 18.
    Herrler, G., Durkop, I., Becht, H., and Klenk, H.D., The Glycoprotein of Influenza C Virus Is the Haemagglutinin, Esterase and Fusion Factor, J. Gen. Virol., 1988, vol. 69, no. 4, pp. 839–846.PubMedCrossRefGoogle Scholar
  19. 19.
    Rosenthal, P.B., Zhang, X., Formanowski, F., et al., Structure of the Haemagglutinin-Esterase-Fusion Glycoprotein of Influenza C Virus, Nature, 1998, vol. 396, no. 6706, pp. 92–96.PubMedCrossRefGoogle Scholar
  20. 20.
    Oeffner, F., Klenk, H.D., and Herrler, G., The Cytoplasmic Tail of the Influenza C Virus Glycoprotein HEF Negatively Affects Transport to the Cell Surface, J. Gen. Virol., 1999, vol. 80, no. 2, pp. 363–369.PubMedGoogle Scholar
  21. 21.
    Sugawara, K., Nishimura, H., Hongo, S., et al., Construction of an Antigenic Map of the Haemagglutinin-Esterase Protein of Influenza C Virus, J. Gen. Virol., 1993, vol. 74, no. 8, pp. 1661–1666.PubMedCrossRefGoogle Scholar
  22. 22.
    Hongo, S., Sugawara, K., Homma, M., and Nakamura, K., The Functions of Oligosaccharide Chains Associated with Influenza C Viral Glycoproteins: 1. The Formation of Influenza C Virus Particles in the Absence of Glycosylation, Arch. Virol., 1986, vol. 89, nos. 1–4, pp. 171–187.PubMedCrossRefGoogle Scholar
  23. 23.
    Hongo, S., Sugawara, K., Homma, M., and Nakamura, K., The Functions of Oligosaccharide Chains Associated with Influenza C Viral Glycoproteins: 2. The Role of Carbohydrates in the Antigenic Properties of Influenza C Viral Glycoproteins, Arch. Virol., 1986, vol. 89, nos. 1–4, pp. 189–201.PubMedCrossRefGoogle Scholar
  24. 24.
    Sugahara, K., Hongo, S., Sugawara, K., et al., Role of Individual Oligosaccharide Chains in Antigenic Properties, Intracellular Transport, and Biological Activities of Influenza C Virus Hemagglutinin-Esterase Protein, Virology, 2001, vol. 285, no. 1, pp. 153–164.PubMedCrossRefGoogle Scholar
  25. 25.
    Sugawara, K., Kitame, F., Nishimura, H., and Nakamura, K., Operational and Topological Analyses of Antigenic Sites on Influenza C Virus Glycoprotein and Their Dependence on Glycosylation, J. Gen. Virol., 1988, vol. 69, pp. 537–547.PubMedCrossRefGoogle Scholar
  26. 26.
    Pekosz, A. and Lamb, R.A., Identification of a Membrane Targeting and Degradation Signal in the p42 Protein of Influenza C Virus, J. Virol., 2000, vol. 74, no. 22, pp. 10480–10488.PubMedCrossRefGoogle Scholar
  27. 27.
    Muraki, Y., Washioka, H., Sugawara, K., et al., Identification of an Amino Acid Residue on Influenza C Virus M1 Protein Responsible for Formation of the Cord-Like Structures of the Virus, J. Gen. Virol., 2004, vol. 85, no. 7, pp. 1885–1893.PubMedCrossRefGoogle Scholar
  28. 28.
    Muraki, Y., Murata, T., Takashita, E., et al., A Mutation on Influenza C Virus M1 Protein Affects Virion Morphology by Altering the Membrane Affinity of the Protein, J. Virol., 2007, vol. 81, no. 16, pp. 8766–8773.PubMedCrossRefGoogle Scholar
  29. 29.
    Hongo, S., Ishii, K., Mori, K., et al., Detection of Ion Channel Activity in Xenopus laevis Oocytes Expressing Influenza C Virus CM2 Protein, Arch. Virol., 2004, vol. 149, no. 1, pp. 35–50.PubMedCrossRefGoogle Scholar
  30. 30.
    Betakova, T. and Kollerova, E., pH Modulating Activity of Ion Channels of Influenza A, B, and C Viruses, Acta Virol., 2006, vol. 50, no. 3, pp. 187–193.PubMedGoogle Scholar
  31. 31.
    Alamgir, A.S., Matsuzaki, Y., Hongo, S., et al., Phylogenetic Analysis of Influenza C Virus Nonstructural (NS) Protein Genes and Identification of the NS2 Protein, J. Gen. Virol., 2000, vol. 81, no. 8, pp. 1933–1940.PubMedGoogle Scholar
  32. 32.
    Marschall, M., Helten, A., Hechtfischer, A., et al., The ORF, Regulated Synthesis, and Persistence-Specific Variation of Influenza C Viral NS1 Protein, Virology, 1999, vol. 253, no. 2, pp. 208–218.PubMedCrossRefGoogle Scholar
  33. 33.
    Muraki, Y., Furukawa, T., Kohno, Y., et al., Influenza C Virus NS1 Protein Upregulates the Splicing of Viral mRNAs, J. Virol., 2010, vol. 84, no. 4, pp. 1957–1966.PubMedCrossRefGoogle Scholar
  34. 34.
    Kohno, Y., Muraki, Y., Matsuzaki, Y., et al., Intracellular Localization of Influenza C Virus NS2 Protein (NEP) in Infected Cells and Its Incorporation into Virions, Arch. Virol., 2009, vol. 154, no. 2, pp. 235–243.PubMedCrossRefGoogle Scholar
  35. 35.
    Paragas, J., Talon, J., O’Neill, R.E., et al., Influenza B and C Virus NEP (NS2) Proteins Possess Nuclear Export Activities, J. Virol., 2001, vol. 75, no. 16, pp. 7375–7383.PubMedCrossRefGoogle Scholar
  36. 36.
    Joosting, A.C., Head, B., Bynoe, M.L., and Tyrrell, D.A., Production of Common Colds in Human Volunteers by Influenza C Virus, Br. Med. J., 1968, vol. 4, no. 5624, pp. 153–154.PubMedCrossRefGoogle Scholar
  37. 37.
    Kudryavtseva, A.V. and Yatsyshina, S.B., A Study of Influenza C Virus Circulation among Moscow Patients with Acute Respiratory Disease, Mol. Diagn., 2010, vol. 4, pp. 184–186.Google Scholar
  38. 38.
    Domingo, E. and Holland, J.J., RNA Virus Mutations and Fitness for Survival, Annu. Rev. Microbiol., 1997, vol. 51, pp. 151–178.PubMedCrossRefGoogle Scholar
  39. 39.
    Worobey, M. and Holmes, E.C., Evolutionary Aspects of Recombination in RNA Viruses, J. Gen. Virol., 1999, vol. 80, no. 10, pp. 2535–2543.PubMedGoogle Scholar
  40. 40.
    Chare, E.R., Gould, E.A., and Holmes, E.C., Phylogenetic Analysis Reveals a Low Rate of Homologous Recombination in Negative-Sense RNA Viruses, J. Gen. Virol., 2003, vol. 84, no. 10, pp. 2691–2703.PubMedCrossRefGoogle Scholar
  41. 41.
    Boni, M.F., Zhou, Y., Taubenberger, J.K., and Holmes, E.C., Homologous Recombination Is Very Rare or Absent in Human Influenza A Virus, J. Virol., 2008, vol. 10, pp. 4807–4811.CrossRefGoogle Scholar
  42. 42.
    Gibbs, M.J., Armstrong, J.S., and Gibbs, A.J., Recombination in the Hemagglutinin Gene of the 1918 “Spanish Flu”, Science, 2001, vol. 293, no. 5536, pp. 1842–1845.PubMedCrossRefGoogle Scholar
  43. 43.
    Ohyama, S., Adachi, K., Sugawara, K., et al., Antigenic and Genetic Analyses of Eight Influenza C Strains Isolated in Various Areas of Japan during 1985–9, Epidemiol. Infect., 1992, vol. 108, no. 2, pp. 353–365.PubMedCrossRefGoogle Scholar
  44. 44.
    Kawamura, H., Tashiro, M., Kitame, F., et al., Genetic Variation among Human Strains of Influenza C Virus Isolated in Japan, Virus Res., 1986, vol. 4, no. 3, pp. 275–288.PubMedCrossRefGoogle Scholar
  45. 45.
    Matsuzaki, Y., Muraki, Y., Sugawara, K., et al., Cocirculation of Two Distinct Groups of Influenza C Virus in Yamagata City, Japan, Virology, 1994, vol. 202, no. 2, pp. 796–802.PubMedCrossRefGoogle Scholar
  46. 46.
    Peng, G., Hongo, S., Muraki, Y., et al., Genetic Reassortment of Influenza C Viruses in Man, J. Gen. Virol., 1994, vol. 75, no. 12, pp. 3619–3622.PubMedCrossRefGoogle Scholar
  47. 47.
    Peng, G., Hongo, S., Kimura, H., et al., Frequent Occurrence of Genetic Reassortment between Influenza C Virus Strains in Nature, J. Gen. Virol., 1996, vol. 77, no. 7, pp. 1489–1492.PubMedCrossRefGoogle Scholar
  48. 48.
    Tada, Y., Hongo, S., Muraki, Y., et al., Evolutionary Analysis of Influenza C Virus M Genes, Virus Genes, 1997, vol. 15, no. 1, pp. 53–59.PubMedCrossRefGoogle Scholar
  49. 49.
    Matsuzaki, Y., Sugawara, K., Mizuta, K., et al., Antigenic and Genetic Characterization of Influenza C Viruses Which Caused Two Outbreaks in Yamagata City, Japan, in 1996 and 1998, J. Clin. Microbiol., 2002, vol. 40, no. 2, pp. 422–429.PubMedCrossRefGoogle Scholar
  50. 50.
    Gao, Q., Brydon, E.W., and Palese, P., A Seven-Segmented Influenza A Virus Expressing the Influenza C Virus Glycoprotein HEF, J. Virol., 2008, vol. 82, no. 13, pp. 6419–6426.PubMedCrossRefGoogle Scholar
  51. 51.
    Muraki, Y., Hongo, S., Sugawara, K., et al., Evolution of the Haemagglutinin-Esterase Gene of Influenza C Virus, J. Gen. Virol., 1996, vol. 77, no. 4, pp. 673–679.PubMedCrossRefGoogle Scholar
  52. 52.
    Matsuzaki, Y., Mizuta, K., Kimura, H., et al., Characterization of Antigenically Unique Influenza C Virus Strains Isolated in Yamagata and Sendai Cities, Japan, during 1992–1993, J. Gen. Virol., 2000, vol. 81, no. 6, pp. 1447–1452.PubMedGoogle Scholar
  53. 53.
    Chakraverty, P., The Detection and Multiplication of Influenza C Virus in Tissue Culture, J. Gen. Virol., 1974, vol. 25, no. 3, pp. 421–425.PubMedCrossRefGoogle Scholar
  54. 54.
    Sugawara, K., Nishimura, H., Hongo, S., et al., Antigenic Characterization of the Nucleoprotein and Matrix Protein of Influenza C Virus with Monoclonal Antibodies, J. Gen. Virol., 1991, vol. 72, no. 1, pp. 103–109.PubMedCrossRefGoogle Scholar
  55. 55.
    Elliott, R.M., Yuanji, G., and Desselberger, U., Protein and Nucleic Acid Analyses of Influenza C Viruses Isolated from Pigs and Man, Vaccine, 1985, suppl. 3, pp. 182–188.Google Scholar
  56. 56.
    Brown, I.H., Harris, P.A., and Alexander, D.J., Serological Studies of Influenza Viruses in Pigs in Great Britain 1991–2, Epidemiol. Infect., 1995, vol. 114, no. 3, pp. 511–520.PubMedCrossRefGoogle Scholar
  57. 57.
    Guo, Y.J., Jin, F.G., Wang, P., et al., Isolation of Influenza C Virus from Pigs and Experimental Infection of Pigs with Influenza C Virus, J. Gen. Virol., 1983, vol. 64, no. 1, pp. 177–182.PubMedCrossRefGoogle Scholar
  58. 58.
    Yamaoka, M., Hotta, H., Itoh, M., and Homma, M., Prevalence of Antibody to Influenza C Virus among Pigs in Hyogo Prefecture, Japan, J. Gen. Virol., 1991, vol. 72, no. 3, pp. 711–714.PubMedCrossRefGoogle Scholar
  59. 59.
    Kimura, Y., Abiko, C., Peng, G., et al., Interspecies Transmission between Humans and Pigs, Virus Res., 1997, vol. 48, pp. 71–79.PubMedCrossRefGoogle Scholar
  60. 60.
    Takao, S., Matsuzaki, Y., Shimazu, Y., et al., Isolation of Influenza C Virus during the 1999/2000-Influenza Season in Hiroshima Prefecture, Japan, Jpn. J. Infect. Dis., 2000, vol. 53, no. 4, pp. 173–174.PubMedGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2012

Authors and Affiliations

  • A. S. Speranskaya
    • 1
    • 2
    Email author
  • N. V. Melnikova
    • 1
  • M. S. Belenikin
    • 1
  • A. A. Dmitriev
    • 1
  • N. Yu. Oparina
    • 1
  • A. V. Kudryavtseva
    • 1
  1. 1.Engelgardt Institute of Molecular BiologyRussian Academy of SciencesMoscowRussia
  2. 2.Department of Higher PlantsMoscow State UniversityMoscowRussia

Personalised recommendations