Summary
The nucleotide and deduced amino acid sequences of the haemagglutinin genes coding for the HA 1 domain of H3N8 equine influenza viruses isolated over wide regions of the world were analyzed in detail to determine their evolutionary relationships. We have constructed a phylogenetic model tree by the neighbour-joining method using nucleotide sequences of 15 haemagglutinin genes, including those of five viruses determined in the present study. This gene tree revealed the existence of two major evolutionary pathways during a twenty five-year period between 1963 to 1988, and each pathway appeared to consist of two distinct lineages of haemagglutinin genes. Furthermore, our analysis of nucleotide sequences showed that two distinct lineages of equine H3N8 viruses were involved in an equine influenza outbreak during the period of December 1971–January 1972 in Japan. The number of nucleotide changes between strains was proportional to the length of time (in years) between their isolation except for three of the HA genes. However, there are three exceptional strains isolated in 1971, 1987, and 1988, respectively. The haemagglutinin gene in these strains showed a small number of nucleotide substitutions after they branched off around 1963, suggesting an example of frozen replication. Although the estimated rate (0.0094/site/year) of synonymous (silent) substitutions of the haemagglutinin gene of equine H3N8 viruses was nearly the same as that of human H 1 and H 3 haemagglutinin genes, the rate of nonsynonymous (amino-acid changing) substitutions of the former equine virus gene was estimated to be 0.00041/site/year — that is about 5 times lower than that estimated for the human H 3 haemagglutinin gene. The present study is the first demonstration that multiple evolutionary lineages of equine H3N8 influenza virus circulated since 1963.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Air GM, Giggs AJ, Laver WG, Webster RG (1990) Evolutionary lineages in influenza B are not primarily governed by antibody selection. Proc Nat Acad Sci USA 87: 3884–3888
Both GW, Sleigh MJ (1981) Conservation and variation in the haemagglutinins of Hong Kong subtype influenza viruses during antigenic drift. J Virol 39: 663–672
Both GW, Sleigh MJ, Cox N, Kendal AP (1983) Antigenic drift in influenza virus H 3 haemagglutinin from 1968 to 1980: multiple evolutional pathway and sequential amino acid changes at key antigenic sites. J Virol 48: 52–60
Buonaguro DA, Nakada S, Desselberger U, Krystal M, Palese P (1985) Noncumulative sequence changes in the haemagglutinin genes of influenza C virus isolates. Virology 146: 221–232
Bunagurio DA, Nakada S, Fitch WM, Palese P (1986) Epidemiology of influenza C virus in man: multiple evolutionary lineages and low rate of change. Virology 153: 12–21
Burk F, Lamatsch O (1981) Surveillance for immunity against equine influenza virus infections. Comp Immun Microbiol Infect Dis 4: 267–278
Burrows R, Goodrige D, Denyer M, Hutchings G, Frank CJ (1982) Equine influenza infections in Great Britain, 1979. Vet Rec 110: 494–497
Daniels RS, Skehel JJ, Wiley DC (1985) Amino acid sequences of haemagglutinins of influenza viruses of the H 3 subtype isolated from horses. J Gen Virol 66: 457–464
Donis RO, Bean WJ, Webster RG (1989) Distinct lineages of influenza virus H 4 haemagglutinin genes in different regions of the world. Virology 169: 406–417
Fang R, Min Jou W, Huylebroeck D, Devos R, Fiers W (1981) Complete structure of A/duck/Ukraina/1/63 influenza haemagglutinin gene: animal viruses progenitor of human Hong Kong 1968 influenza haemagglutinin. Cell 25: 315–323
Gorman OT, Bean EJ, Kawaoka Y, Webster RG (1990) Evolution of the nucleoprotein gene of influenza A virus. J Virol 64: 1487–1497
Grunstein M, Schedle P, Kedes L (1976) Sequence analysis and evolution of sea urchin (Lytechinus pictus andStrongylocentrorus purpuratus) histone H 4 messenger RNAs. J Mol Biol 104: 351–369
Hayashida H, Itoh H, Kikuno R, Miyata T (1985) Evolution of influenza virus genes. Mol Biol Evol 2: 389–303
Hinshaw VS, Webster RG, Rodriguez RJ (1981) Influenza viruses: combinations of haemagglutinin and neuraminidase subtypes isolated from animals and other sources. Arch Virol 67: 191–201
Kanegae Y, Sugita S, Endo A, Ishida M, Senya S, Osaka K, Nerome K, Oya A (1990) Evolutionary pattern of the haemagglutinin gene of influenza B viruses isolated in Japan: cocirculating lineages in the same epidemic season. J Virol 64: 2860–2865
Kawaoka Y, Bean W, Webster RG (1989) Evolution of the haemagglutinin of equine H 3 influenza viruses. Virology 169: 283–292
Kawaoka Y, Webster RG (1989) Origin of the haemagglutinin on A/eq/Johannesburg/86 (H3N8): the first known equine influenza outbreak in South Africa. Arch Virol 106: 159–164
Kawaoka Y, Yamnikova S, Chambers TM, Lvov DK, Webster RG (1990) Molecular characterization of a new haemagglutinin, subtype H 14, of influenza A virus. Virology 179: 759–767
Kida H, Kawaoka Y, Naeve C, Webster RG (1987) Antigenic and genetic conservation of H 3 influenza virus in wild ducks. Virology 159: 109–119
Kida H, Shortridge KF, Webster RG (1988) Origin of the haemagglutinin gene of H3N2 influenza from pigs in China. Virology 162: 160–166
Kimmel AR, Berger SL (1987) Preparation of cDNA and generation of cDNA libraries. In: Abelson JN, Simon MI (eds) Methods in enzymology, vol 152. Academic Press, London, pp 307–316
Kimura M (1977) Preponderance of synonymous changes as evidence for the neutral theory of molecular evolution. Nature 267: 275–276
Kumanomido T, Okuda Y, Akiyama T, Hirasawa K, Tabuchi E (1972) Studies on outbreak of equine influenza in Japan in 1971-virus isolation. Exp Res Equine Health Lab Tokyo 9: 35–43
Laver WG, Webster RG (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
Min Jou W, Verhoeyen M, Devos R, Saman E, Fang R, Huylebroeck D, Fiers W (1980) Complete structure of the haemagglutinin gene from the human influenza A/Victoria/3/75 (H3N2) strain as determined from cloned DNA. Cell 19: 683–696
Nei M (1975) Molecular population genetics and evolution. Elsevier/North-Holland, New York
Nei M, Gojubori T (1986) Simple methods for estimating the number of synonymous and nonsynonymous substitutions. Mol Biol Evol 3: 418–426
Nerome K, Sakamoto S, Yano N, Yamamoto T, Kobayashi S, Webster RG, Oya A (1983) Antigenic characteristics and genomic composition of naturally occurring recombinant influenza virus isolated from a pig in Japan. J Gen Virol 64: 2611–2620
Powell DG, Spooner P, Thompson GR, Plowright W, Burrow R, Schild GC (1974) The outbreak of equine influenza in England 1973. Vet Rec 94: 282–287
Powell DG (1975) Equine infections respiratory disease. Vet Rec 96: 300–304
Rogers GN, Paulson JC, Daniels RS, Skehel JJ, Wilson IA, Wiley DC (1983) Single amino acid substitutions in influenza haemagglutinin change receptor binding specificity. Nature: 76–78
Rota PA, Walls TR, Harmon MW, Rota JS, Kendal AP, Nerome K (1990) Cocirculation of two distinct evolutionary lineages of influenza type B virus since 1983. Virology 175: 59–68
Saitou M, Nei M (1987) The neighbour-joining method: a new method for reconstructing phylogenic trees. Mol Biol Evol 4: 406–425
Salser W, Isaacson JS (1976) Mutation rates in globin genes: the genetic load and haldane's dilemma. Prog Nucleic Acids Res Mol Biol 19: 205–220
Sambrook J, Fritsch EF, Maniatis T (1989) Commonly used plasmid vector. In: Sambrook J, Fritsch EF, Maniatis T (eds) Molecular cloning, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, p 1.14
Scholtissek C, Rohde W, Von Hoyningen V, Rott R (1978) On the origin of the human influenza virus subtypes H2N2 and H3N2. Virology 87: 13–20
Shortridge KF, Webster RG, Bufferfield WK, Campbell CH (1976) Persistence of Hong Kong influenza virus variants. Science 196: 1454–1455
Sovinova O, Tumova B, Pouska F, Nemec J (1958) Isolation of a virus causing respiratory disease in horses. Acta Virol 2: 52–60
Stuart-Harris CH, Schild GC (1976) Influenza viruses of lower animals and birds. In: Stuart-Harris CH, Schild GC (eds) Influenza, the viruses and disease. Edward Arnold, London, pp 83–85
Thompson GR, Mumford JA, Spooner PR, Burrow R, Powell DG (1977) The outbreak of equine influenza in England, January 1976. Vet Rec 100: 465–468
Uppal PK, Yadav MP (1987) Outbreak of equine influenza in India. Vet Rec 121: 569–570
Van Oirshot JT, Masuel N, Huffels ADNHJ, Auker WJJ (1981) Equine influenza in the Netherlands during the winter of 1978–1979: antigenic drift of the A-equi 2 virus. Vet Q 3: 80–84
Verhoyen M, Fang R, Min Jou W, Devos R, Huylebroeck D, Saman E, Friers W (1980) Antigenic drift between the haemagglutinin of the Hong Kong influenza strains A/Aichi/2/68 and A/Victoria/3/75. Nature 286: 771–776
Waddel GH, Teigland MB, Sigel MM (1963) A new influenza virus associated with equine respiratory disease. J Am Vet Med Assoc 143: 587–594
Ward CW, Dopheide TA (1981) Evolution of the Hong Kong influenza A subtype. Structural relationship between the haemagglutinin from A/duck/Ukraina/63 (Hav 7) and the Hong Kong (H 3) haemagglutinins. Biochem J 195: 337–340
Webster RG, Laver WG, Air GM, Schild GC (1982) Molecular mechanisms of variation in influenza viruses. Nature 296: 115–121
Wiley DC, Wilson IA, Skehel JJ (1981) Structural identification of the antibody-binding sites of Hong Kong influenza haemagglutinin and their involvement in antigenic variation. Nature 289: 373–378
Yamashita M, Krystal M, Fitch WM, Palese P (1988) Influenza B virus evolution: cocirculating lineages and comparison of evolutionary pattern with those of influenza A and C viruses. Virology 163: 112–122
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Endo, A., Pecoraro, R., Sugita, S. et al. Evolutionary pattern of the H 3 haemagglutinin of equine influenza viruses: multiple evolutionary lineages and frozen replication. Archives of Virology 123, 73–87 (1992). https://doi.org/10.1007/BF01317139
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF01317139