1887

Abstract

From immunological and phylogenetic analyses of H3 influenza viruses isolated from pigs and ducks in the People’s Republic of China (China), Hong Kong, Taiwan and Japan, between 1968 and 1982, we arrived at the following conclusions. The H3 haemagglutinin and N2 neuraminidase genes from swine isolates can be segregated into four mammalian lineages, including: (i) the earliest human strains; (ii) early swine strains including Hong Kong isolates from 1976–1977; (iii) an intermediate strain between the early swine and recent human strains; and (iv) recent human strains. In this study we found an unusual swine strain (sw/Hong Kong/127/82) belonging to the third lineage which behaved like those of the early swine-like lineage in the haemagglutination inhibition test; but neuraminidase inhibition profiles with monoclonal antibodies indicated that this virus is related to late human strains. On the basis of pairwise comparisons of complete or partial nucleotide sequences the genes encoding the three polymerase proteins (PB2, PB1, PA), the nucleoprotein, the membrane protein and possibly the nonstructural proteins of sw/Hong Kong/127/82 are of the swine H1N1 lineage, whereas genes encoding the two surface glycoproteins belong to the human H3N2 lineage. In contrast, all RNA segments of one swine isolate (sw/Hong Kong/81/78) are similar to those of recent human H3N2 viruses. This study indicated that frequent interspecies infections between human and swine hosts appeared to occur during 1976–82. Although the evolutionary rates of human (0.0122/site/year), swine (0.0127/site/year) and avian (0.0193/site/year) virus genes are similar when based upon synonymous substitutions, nonsynonymous substitutions indicated that viral genes derived from human and swine viruses evolved about three times faster (0.0026–0.0027/site/year) than those of avian viruses (0.0008/site/year). Furthermore, the evolutionary mechanism by which human and swine H3 haemagglutinin genes evolve at a similar rate, based on nonsynonymous substitutions, appeared to be quite different from previous evidence which showed that human H1 haemagglutinin genes evolved three times faster than those of swine viruses. However, comparison of the number of nonsynonymous substitutions in the antigenic sites (A–E) of haemagglutinin molecules demonstrated that swine viruses evolve at a rate that is about one fifth to one tenth that of human viruses, reflecting the conservative nature of the antigenic structure in the former.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-76-3-613
1995-03-01
2022-08-11
Loading full text...

Full text loading...

/deliver/fulltext/jgv/76/3/JV0760030613.html?itemId=/content/journal/jgv/10.1099/0022-1317-76-3-613&mimeType=html&fmt=ahah

References

  1. Air G. M., Els M. C., Laver W. G., Webster R. G. 1985; Location of antigenic sites on the three-dimensional structure of the influenza N2 virus neuraminidase. Virology 145:237–248
    [Google Scholar]
  2. Air G. M., Gibbs A. J., Laver W. G., Webster R. G. 1990; Evolutionary changes in influenza B are not primarily governed by antibody selection. Proceedings of the National Academy of Sciences, USA 87:3884–3888
    [Google Scholar]
  3. Bean W. J., Schell M., Katz J., Kawaoka Y., Naeve C., Gorman O., Webster R. G. 1992; Evolution of the H3 influenza virus hemagglutinin from human and nonhuman hosts. Journal of Virology 66:1129–1138
    [Google Scholar]
  4. Bently D. R., Brownlee G. G. 1982; Sequence of N2 neuraminidase from influenza virus A/NT/60/68. Nucleic Acids Research 10:5033–5042
    [Google Scholar]
  5. Both G. W., Sleigh M. J. 1980; Complete nucleotide sequence of the hemagglutinin gene from human influenza virus of the Hong Kong subtype. Nucleic Acids Research 8:2561–2575
    [Google Scholar]
  6. Both G. W., Sleigh M. J. 1981; Conservation and variation in the hemagglutinins of Hong Kong subtype influenza viruses during antigenic drift. Journal of Virology 39:663–672
    [Google Scholar]
  7. Buonagurio D. A., Nakada S., Parvin J. D., Krystal M., Palese P., Fitch W. M. 1986; Evolution of human influenza A viruses over 50 years: rapid, uniform rate of change in NS gene. Science 232:980–982
    [Google Scholar]
  8. Castrucci M. R., Donatelli I., Sidoli L., Barigazzi G., Kawaoka Y., Webster R. G. 1993; Genetic reassortment between avian and human influenza A viruses in Italian pigs. Virology 193:503–506
    [Google Scholar]
  9. Castrucci M. R., Campitelli L., Ruggieri A., Barigazzi G., Sidoli L., Daniels R., Oxford J. S., Donatelli I. 1994; Antigenic and sequence analysis of H3 influenza virus haemagglutinins from pigs in Italy. Journal of General Virology 75:371–379
    [Google Scholar]
  10. Deshpande K. L., Naeve C. W., Webster R. G. 1985; The neuraminidase of the virulent and a virulent A/chicken/ Pennsylvania/83 (H5N2) influenza A viruses: sequence antigenic analyses. Virology 147:49–60
    [Google Scholar]
  11. Elleman T. C., Azad A. A., Ward C. W. 1982; Neuraminidase gene from the early Asian strain of human influenza virus A/RI/5/57(H2N2). Nucleic Acids Research 10:7005–7015
    [Google Scholar]
  12. Fang R., Min Jou W., Huylebroeck D., Devos R., Fiers W. 1981; Complete structure of A/Duck/Ukraine/63 influenza hemagglutinin gene: animal virus as progenitor of human H3 Hong Kong 1968 influenza hemagglutinin. Cell 25:315–323
    [Google Scholar]
  13. Gammelin M., Altmuller A., Reinhardt U., Mandler J., Harley V. R., Hudson P. J., Fitch W. M., Scholtissek C. 1990; Phylogenetic analysis of nucleoproteins suggests that human influenza A viruses emerged from a 19th century avian ancestor. Molecular Biology and Evolution 7:194–200
    [Google Scholar]
  14. Gojobori T., Ishii K., Nei M. 1982; Estimation of average number of nucleotide substitutions when the rate of substitution varies with nucleotide. Journal of Molecular Evolution 18:414–423
    [Google Scholar]
  15. Gorman O. T., Bean W. J., Kawaoka Y., Webster R. G. 1990; Evolution of the nucleoprotein genes of influenza A virus. Journal of Virology 64:1487–1497
    [Google Scholar]
  16. Ito T., Gorman O. T., Kawaoka Y., Bean W. J., Webster R. G. 1990; Evolutionary analysis of the influenza A virus M gene with comparison of the M1 and M2 proteins. Journal of Virology 65:5491–5498
    [Google Scholar]
  17. Kanegae Y., Sugita S., Endo A., Ishida M., Senya S., Osako K., Nerome K., Oya A. 1990; Evolutionary pattern of the hemagglutinin gene of influenza B viruses isolated in Japan: cocirculating lineages in the same epidemic season. Journal of Virology 64:2860–2865
    [Google Scholar]
  18. Kawaoka Y., Krauss S., Webster R. G. 1989; Avian-to-Human transmission of the PB1 gene of influenza A viruses in the 1957 and 1968 pandemics. Journal of Virology 63:4603–1608
    [Google Scholar]
  19. Kida H., Kawaoka Y., Naeve C. W., Webster R. G. 1987; Antigenic and genetic conservation of H3 influenza virus in wild ducks. Virology 159:109–119
    [Google Scholar]
  20. Kida H., Shortridge K. F., Webster R. G. 1988; Origin of the hemagglutinin gene of H3N2 influenza viruses from pigs in China. Virology 162:160–166
    [Google Scholar]
  21. Laver W. G., Webster R. G. 1973; Studies on the origin of pandemic influenza. III. Evidence implicating duck and equine influenza viruses as possible progenitors of the Hong Kong strain of human influenza. Virology 51:383–391
    [Google Scholar]
  22. Laver W. G., Air G. M., Dopheide T. A., Ward C. W. 1980; Amino acid sequence changes in the hemagglutinin of A/Hong Kong (H3N2) influenza virus during the period 1968–77. Science 283:454–457
    [Google Scholar]
  23. Lentz M. R., Air G. M., Laver W. G., Webster R. G. 1984; Sequence of neuraminidase gene of influenza virus A/Tokyo/3/67 and previously uncharacterized monoclonal variants. Virology 135:257–265
    [Google Scholar]
  24. Markoff L., Lai C. J. 1982; Sequence of the influenza A/Udorn/72 (H3N2) virus neuraminidase gene as determined from cloned full-length DNA. Virology 119:288–297
    [Google Scholar]
  25. Martinez C., Rio L. D., Portela A., Domingo E., Ortín J. 1983; Evolution of the influenza virus neuraminidase gene during drift of the N2 subtype. Virology 130:539–545
    [Google Scholar]
  26. Min Jou W., Verhoeyen M., Devos R., Saman E., Fang R., Huylebroeck D., Fiers W. 1980; Complete structure of the hemagglutinin gene from the human influenza A/Victoria/3/75 (H3N2) strain as determined from cloned DNA. Cell 19:683–696
    [Google Scholar]
  27. Nakajima S., Takeuchi Y., Nakajima K. 1988; Location on the evolutionary tree of influenza H3 hemagglutinin genes of Japanese strains isolated during 1985–6 season. Epidemiology and Infection 100:301–310
    [Google Scholar]
  28. Nei M., Gojobori T. 1986; Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Molecular Biology and Evolution 3:418–126
    [Google Scholar]
  29. Nerome K., Ishida M., Nakayama M., Oya A., Kanai C., Suwicha K. 1981; Antigenic and genetic analysis of A/Hong Kong (H3N2) influenza viruses isolated from swine and man. Journal of General Virology 56:441–445
    [Google Scholar]
  30. Nerome K., Ishida M., Oya A., Kanai C., Suwicha K. 1982; Isolation of an influenza H1N1 virus from a pig. Virology 117:485–189
    [Google Scholar]
  31. Nerome K., Sakamoto S., Yano N., Yamamoto T., Kobayashi T., Webster R. G., Oya A. 1983; Antigenic characteristics and genome composition of a naturally occurring recombinant influenza virus isolated from a pig in Japan. Journal of General Virology 64:2611–2620
    [Google Scholar]
  32. Nerome K., Yoshioka Y., Sakamoto S., Yasuhara H., Oya A. 1985; Characteristics of swine recombinant influenza virus isolated in 1990: recombination between swine and the earliest Hong Kong (H3N2) viruses. Vaccine 3:267–273
    [Google Scholar]
  33. Nerome K., Kanegae Y., Yoshioka Y., Itamura S., Ishida M., Gojobori T., Oya A. 1991; Evolutionary pathways of N2 neuraminidase of swine and human influenza A viruses: origin of the neuraminidase genes of two reassortants (H1N2) isolated from pigs. Journal of General Virology 72:693–698
    [Google Scholar]
  34. Newton S. E., Air G. M., Webster R. G., Laver W. G. 1983; Sequence of the hemagglutinin gene of influenza virus A/Memphis/1/71 and previously uncharacterized monoclonal antibody-derived variants. Virology 128:495–501
    [Google Scholar]
  35. Okazaki K., Kawaoka Y., Webster R. G. 1989; Evolutionary pathways of the PA genes of influenza viruses. Virology 172:601–608
    [Google Scholar]
  36. Palese P., Schulman J. L. 1976; Differences in RNA patterns of influenza A virus. Journal of Virology 17:876–884
    [Google Scholar]
  37. Rompuy L. V., Min Jou W., Huylebroeck D., Fiers W. 1982; Complete nucleotide sequence of a human influenza neuraminidase gene of sub-type N2 (A/Victoria/3/75). Journal of Molecular Evolution 3:57–74
    [Google Scholar]
  38. Saitou N., Nei M. 1987; The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4:406–425
    [Google Scholar]
  39. Sanger F., Nicklen S., Coulson A. R. 1977; DNA sequencing with chain-terminating inhibitors. Proceedings of the National Academy of Sciences, USA 74:5463–5467
    [Google Scholar]
  40. Scholtissek C., Rohde W., von Hoyningen V., Rott R. 1978; On the origin of the human influenza virus subtype H2N2 and H3N2. Virology 87:13–20
    [Google Scholar]
  41. Schultz U., Fitch W. M., Ludwig S., Mandler J., Scholtissek C. 1991; Evolution of pig influenza viruses. Virology 183:61–73
    [Google Scholar]
  42. Shortridge K. F., Webster R. G., Butterfield W. K., Campbell C. H. 1976; Persistence of Hong Kong influenza virus variants in pigs. Science 196:1454–1455
    [Google Scholar]
  43. Shortridge K. F., Webster R. G. 1979; Geographical distribution of swine (swHlNl) and Hong Kong (H3N2) influenza virus variants in pigs in Southeast Asia. Intervirology 11:9–15
    [Google Scholar]
  44. Shortridge K. F., King A. P., Webster R. G. 1987; Monoclonal antibodies for characterizing H3N2 influenza viruses that persist in pigs in China. Journal of Infectious Diseases 155:577–581
    [Google Scholar]
  45. Sleigh M. J., Both G. W., Underwood P. A., Bender V. J. 1981; Antigenic drift in the hemagglutinin of Hong Kong influenza subtype: Correlation of amino acid changes in viral antigenicity. Journal of Virology 37:845–853
    [Google Scholar]
  46. Verhoeyen M., Fang R., Min Jou W., Devos R., Huylebroeck D., Saman E., Fiers W. 1980; Antigenic drift between the hemagglutinin of the Hong Kong influenza strains A/Aichi/2/68 and A/Victoria/3/75. Nature 286:771–776
    [Google Scholar]
  47. WHO Report 1973; Influenza virus neuraminidase and neuraminidase inhibition test procedures. Bulletin of the World Health Organization 48:199–202
    [Google Scholar]
  48. Wiley D. C., Wilson I. A., Skehel J. J. 1981; Structural identification of the antibody-binding sites of Hong Kong influenza hemagglutinin and their involvement in antigeneic variation. Nature 289:373–378
    [Google Scholar]
  49. Wright S. M., Kawaoka Y., Sharp G. B., Senne D. A., Webster R. G. 1992; Interspecies transmission and reassortment of influenza A viruses in pigs and turkeys in the United States. American Journal of Epidemiology 136:488–497
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/0022-1317-76-3-613
Loading
/content/journal/jgv/10.1099/0022-1317-76-3-613
Loading

Data & Media loading...

Most cited this month Most Cited RSS feed

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