Analyze Diet
Archives of virology1992; 123(1-2); 73-87; doi: 10.1007/BF01317139

Evolutionary pattern of the H 3 haemagglutinin of equine influenza viruses: multiple evolutionary lineages and frozen replication.

Abstract: 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.
Publication Date: 1992-01-01 PubMed ID: 1550498DOI: 10.1007/BF01317139Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
  • Comparative Study
  • Journal Article
  • Research Support
  • Non-U.S. Gov't

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

This study examines the evolution of the H 3 haemagglutinin of equine influenza viruses, showing the existence of two major evolutionary pathways over a 25-year period, as well as the concept of ‘frozen replication’.

Evolutionary Relationships and Pathways of H3N8 Equine Influenza Viruses

  • The researchers analyzed the nucleotide and deduced amino acid sequences of the haemagglutinin genes coding for the HA 1 domain of H3N8 equine influenza viruses to determine their evolutionary relationships.
  • They constructed a phylogenetic model tree, a method used to illustrate the evolutionary relationships among various species based on shared attributes. This was done using nucleotide sequences of 15 haemagglutinin genes, which included those of five viruses determined in the study.
  • The model tree revealed the existence of two major evolutionary pathways during a 25-year period, from 1963 to 1988. Each pathway consisted of two distinct lineages of haemagglutinin genes.

Equine Influenza Outbreak and Frozen Replication

  • The study found that two distinct lineages of equine H3N8 viruses were involved in an equine influenza outbreak in Japan between December 1971 and January 1972.
  • The number of nucleotide changes between strains was usually proportional to the length of time (in years) between their isolation. However, exceptions occurred in strains isolated in 1971, 1987, and 1988.
  • These strains displayed a small number of nucleotide substitutions after they branched off around 1963. This was seen as an example of “frozen replication”, a phenomenon where the genomic changes pause or slow down significantly for certain periods.

Rate of Synonymous and Non-Synonymous Substitutions

  • The estimated rate 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.
  • However, the rate of nonsynonymous (amino-acid changing) substitutions of the equine virus gene was found to be about 5 times lower than that estimated for the human H 3 haemagglutinin gene.

Implications of the Study

  • This research is significant because it marks the first demonstration that multiple evolutionary lineages of the equine H3N8 influenza virus have circulated since 1963.
  • This deeper understanding of the evolution and mutation rate of the H3N8 virus can aid in predicting future variations and in the development of more effective vaccines.

Cite This Article

APA
Endo A, Pecoraro R, Sugita S, Nerome K. (1992). Evolutionary pattern of the H 3 haemagglutinin of equine influenza viruses: multiple evolutionary lineages and frozen replication. Arch Virol, 123(1-2), 73-87. https://doi.org/10.1007/BF01317139

Publication

ISSN: 0304-8608
NlmUniqueID: 7506870
Country: Austria
Language: English
Volume: 123
Issue: 1-2
Pages: 73-87

Researcher Affiliations

Endo, A
  • Department of Virology and Rickettsiology, National Institute of Health, Tokyo, Japan.
Pecoraro, R
    Sugita, S
      Nerome, K

        MeSH Terms

        • Amino Acid Sequence
        • Animals
        • Base Sequence
        • Biological Evolution
        • Chick Embryo
        • Cloning, Molecular
        • DNA, Viral
        • Genes, Viral
        • Hemagglutinin Glycoproteins, Influenza Virus
        • Hemagglutinins, Viral / genetics
        • Influenza A virus / classification
        • Influenza A virus / genetics
        • Molecular Sequence Data
        • Sequence Homology, Nucleic Acid

        References

        This article includes 42 references
        1. Both GW, Sleigh MJ, Cox NJ, Kendal AP. Antigenic drift in influenza virus H3 hemagglutinin from 1968 to 1980: multiple evolutionary pathways and sequential amino acid changes at key antigenic sites.. J Virol 1983 Oct;48(1):52-60.
          pubmed: 6193288doi: 10.1128/JVI.48.1.52-60.1983google scholar: lookup
        2. Thomson GR, Mumford JA, Spooner PR, Burrows R, Powell DG. The outbreak of equine influenza in England: January 1976.. Vet Rec 1977 May 28;100(22):465-8.
          pubmed: 17942doi: 10.1136/vr.100.22.465google scholar: lookup
        3. van Oirschot JT, Masurel N, Huffels AD, Anker WJ. Equine influenza in the Netherlands during the winter of 1978-1979; antigenic drift of the A-equi 2 virus.. Vet Q 1981 Apr;3(2):80-4.
          pubmed: 7245173doi: 10.1080/01652176.1981.9693801google scholar: lookup
        4. Grunstein M, Schedl P, Kedes L. Sequence analysis and evolution of sea urchin (Lytechinus pictus and Strongylocentrotus purpuratus) histone H4 messenger RNAs.. J Mol Biol 1976 Jun 25;104(2):351-69.
          pubmed: 950666doi: 10.1016/0022-2836(76)90276-xgoogle scholar: lookup
        5. Kanegae Y, Sugita S, Endo A, Ishida M, Senya S, Osako K, Nerome K, Oya A. Evolutionary pattern of the hemagglutinin gene of influenza B viruses isolated in Japan: cocirculating lineages in the same epidemic season.. J Virol 1990 Jun;64(6):2860-5.
        6. Kida H, Shortridge KF, Webster RG. Origin of the hemagglutinin gene of H3N2 influenza viruses from pigs in China.. Virology 1988 Jan;162(1):160-6.
          pubmed: 3336940doi: 10.1016/0042-6822(88)90405-9google scholar: lookup
        7. Kawaoka Y, Webster RG. Origin of the hemagglutinin on A/Equine/Johannesburg/86 (H3N8): the first known equine influenza outbreak in South Africa.. Arch Virol 1989;106(1-2):159-64.
          pubmed: 2548457doi: 10.1007/BF01311048google scholar: lookup
        8. Jou WM, Verhoeyen M, Devos R, Saman E, Fang R, Huylebroeck D, Fiers W, Threlfall G, Barber C, Carey N, Emtage S. Complete structure of the hemagglutinin gene from the human influenza A/Victoria/3/75 (H3N2) strain as determined from cloned DNA.. Cell 1980 Mar;19(3):683-96.
          pubmed: 6153930doi: 10.1016/s0092-8674(80)80045-6google scholar: lookup
        9. Kimura M. Preponderance of synonymous changes as evidence for the neutral theory of molecular evolution.. Nature 1977 May 19;267(5608):275-6.
          pubmed: 865622doi: 10.1038/267275a0google scholar: lookup
        10. WADDELL GH, TEIGLAND MB, SIGEL MM. A NEW INFLUENZA VIRUS ASSOCIATED WITH EQUINE RESPIRATORY DISEASE.. J Am Vet Med Assoc 1963 Sep 15;143:587-90.
          pubmed: 14077956
        11. Daniels RS, Skehel JJ, Wiley DC. Amino acid sequences of haemagglutinins of influenza viruses of the H3 subtype isolated from horses.. J Gen Virol 1985 Mar;66 ( Pt 3):457-64.
          pubmed: 3973560doi: 10.1099/0022-1317-66-3-457google scholar: lookup
        12. Yamashita M, Krystal M, Fitch WM, Palese P. Influenza B virus evolution: co-circulating lineages and comparison of evolutionary pattern with those of influenza A and C viruses.. Virology 1988 Mar;163(1):112-22.
          pubmed: 3267218doi: 10.1016/0042-6822(88)90238-3google scholar: lookup
        13. Fang R, Min Jou W, Huylebroeck D, Devos R, Fiers W. Complete structure of A/duck/Ukraine/63 influenza hemagglutinin gene: animal virus as progenitor of human H3 Hong Kong 1968 influenza hemagglutinin.. Cell 1981 Aug;25(2):315-23.
          pubmed: 6169439doi: 10.1016/0092-8674(81)90049-0google scholar: lookup
        14. Webster RG, Laver WG, Air GM, Schild GC. Molecular mechanisms of variation in influenza viruses.. Nature 1982 Mar 11;296(5853):115-21.
          pubmed: 6174870doi: 10.1038/296115a0google scholar: lookup
        15. Air GM, Gibbs AJ, Laver WG, Webster RG. Evolutionary changes in influenza B are not primarily governed by antibody selection.. Proc Natl Acad Sci U S A 1990 May;87(10):3884-8.
          pubmed: 2378639doi: 10.1073/pnas.87.10.3884google scholar: lookup
        16. Both GW, Sleigh MJ. Conservation and variation in the hemagglutinins of Hong Kong subtype influenza viruses during antigenic drift.. J Virol 1981 Sep;39(3):663-72.
          pubmed: 6169840doi: 10.1128/JVI.39.3.663-672.1981google scholar: lookup
        17. Buonagurio DA, Nakada S, Fitch WM, Palese P. Epidemiology of influenza C virus in man: multiple evolutionary lineages and low rate of change.. Virology 1986 Aug;153(1):12-21.
          pubmed: 2943076doi: 10.1016/0042-6822(86)90003-6google scholar: lookup
        18. Bürki F, Lamatsch O. Surveillance for immunity against equine influenza virus infections.. Comp Immunol Microbiol Infect Dis 1981;4(3-4):267-78.
          pubmed: 6174266doi: 10.1016/0147-9571(81)90012-6google scholar: lookup
        19. Rogers GN, Paulson JC, Daniels RS, Skehel JJ, Wilson IA, Wiley DC. Single amino acid substitutions in influenza haemagglutinin change receptor binding specificity.. Nature 1983 Jul 7-13;304(5921):76-8.
          pubmed: 6191220doi: 10.1038/304076a0google scholar: lookup
        20. Donis RO, Bean WJ, Kawaoka Y, Webster RG. Distinct lineages of influenza virus H4 hemagglutinin genes in different regions of the world.. Virology 1989 Apr;169(2):408-17.
          pubmed: 2705304doi: 10.1016/0042-6822(89)90166-9google scholar: lookup
        21. Wiley DC, Wilson IA, Skehel JJ. Structural identification of the antibody-binding sites of Hong Kong influenza haemagglutinin and their involvement in antigenic variation.. Nature 1981 Jan 29;289(5796):373-8.
          pubmed: 6162101doi: 10.1038/289373a0google scholar: lookup
        22. Verhoeyen M, Fang R, Jou WM, Devos R, Huylebroeck D, Saman E, Fiers W. Antigenic drift between the haemagglutinin of the Hong Kong influenza strains A/Aichi/2/68 and A/Victoria/3/75.. Nature 1980 Aug 21;286(5775):771-6.
          pubmed: 7402351doi: 10.1038/286771a0google scholar: lookup
        23. Hinshaw VS, Webster RG, Rodriguez RJ. Influenza A viruses: combinations of hemagglutinin and neuraminidase subtypes isolated from animals and other sources.. Arch Virol 1981;67(3):191-201.
          pubmed: 6164356doi: 10.1007/BF01318130google scholar: lookup
        24. Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees.. Mol Biol Evol 1987 Jul;4(4):406-25.
        25. Uppal PK, Yadav MP. Outbreak of equine influenza in India.. Vet Rec 1987 Dec 12;121(24):569-70.
          pubmed: 2829407
        26. SOVINOVA O, TUMOVA B, POUSKA F, NEMEC J. Isolation of a virus causing respiratory disease in horses.. Acta Virol 1958 Jan-Mar;2(1):52-61.
          pubmed: 13533033
        27. Gorman OT, Bean WJ, Kawaoka Y, Webster RG. Evolution of the nucleoprotein gene of influenza A virus.. J Virol 1990 Apr;64(4):1487-97.
        28. Burrows R, Goodridge D, Denyer M, Hutchings G, Frank CJ. Equine influenza infections in Great Britain, 1979.. Vet Rec 1982 May 22;110(21):494-7.
          pubmed: 6287694doi: 10.1136/vr.110.21.494google scholar: lookup
        29. Kimmel AR, Berger SL. Preparation of cDNA and the generation of cDNA libraries: overview.. Methods Enzymol 1987;152:307-16.
          pubmed: 3657577doi: 10.1016/0076-6879(87)52035-3google scholar: lookup
        30. Powell DG, Thomson GR, Spooner P, Plowright W, Burrows R, Schild GC. The outbreak of equine influenza in England April-May 1973.. Vet Rec 1974 Mar 30;94(13):282-7.
          pubmed: 4826197doi: 10.1136/vr.94.13.282google scholar: lookup
        31. Nerome K, Sakamoto S, Yano N, Yamamoto T, Kobayashi S, Webster RG, Oya A. Antigenic characteristics and genome composition of a naturally occurring recombinant influenza virus isolated from a pig in Japan.. J Gen Virol 1983 Dec;64 ( Pt 12):2611-20.
          pubmed: 6198440doi: 10.1099/0022-1317-64-12-2611google scholar: lookup
        32. Rota PA, Wallis TR, Harmon MW, Rota JS, Kendal AP, Nerome K. Cocirculation of two distinct evolutionary lineages of influenza type B virus since 1983.. Virology 1990 Mar;175(1):59-68.
          pubmed: 2309452doi: 10.1016/0042-6822(90)90186-ugoogle scholar: lookup
        33. Nei M, Gojobori T. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions.. Mol Biol Evol 1986 Sep;3(5):418-26.
        34. Kida H, Kawaoka Y, Naeve CW, Webster RG. Antigenic and genetic conservation of H3 influenza virus in wild ducks.. Virology 1987 Jul;159(1):109-19.
          pubmed: 2440178doi: 10.1016/0042-6822(87)90353-9google scholar: lookup
        35. Kawaoka Y, Bean WJ, Webster RG. Evolution of the hemagglutinin of equine H3 influenza viruses.. Virology 1989 Apr;169(2):283-92.
          pubmed: 2705299doi: 10.1016/0042-6822(89)90153-0google scholar: lookup
        36. Kawaoka Y, Yamnikova S, Chambers TM, Lvov DK, Webster RG. Molecular characterization of a new hemagglutinin, subtype H14, of influenza A virus.. Virology 1990 Dec;179(2):759-67.
          pubmed: 2238469doi: 10.1016/0042-6822(90)90143-fgoogle scholar: lookup
        37. Buonagurio DA, Nakada S, Desselberger U, Krystal M, Palese P. Noncumulative sequence changes in the hemagglutinin genes of influenza C virus isolates.. Virology 1985 Oct 30;146(2):221-32.
          pubmed: 3855244doi: 10.1016/0042-6822(85)90006-6google scholar: lookup
        38. Laver WG, Webster RG. Studies on the origin of pandemic influenza. 3. Evidence implicating duck and equine influenza viruses as possible progenitors of the Hong Kong strain of human influenza.. Virology 1973 Feb;51(2):383-91.
          pubmed: 4632653doi: 10.1016/0042-6822(73)90437-6google scholar: lookup
        39. Ward CW, Dopheide TA. Evolution of the Hong Kong influenza A sub-type. Structural relationships between the haemagglutinin from A/duck/Ukraine/1/63 (Hav 7) and the Hong Kong (H3) haemagglutinins.. Biochem J 1981 Apr 1;195(1):337-40.
          pubmed: 7306060doi: 10.1042/bj1950337google scholar: lookup
        40. Shortridge KF, Webster RG, Butterfield WK, Campbell CH. Persistence of Hong Kong influenza virus variants in pigs.. Science 1977 Jun 24;196(4297):1454-5.
          pubmed: 867041doi: 10.1126/science.867041google scholar: lookup
        41. Salser W, Isaacson JS. Mutation rates in globin genes: the genetic load and Haldane's dilemma.. Prog Nucleic Acid Res Mol Biol 1976;19:205-20.
          pubmed: 1019345doi: 10.1016/s0079-6603(08)60919-8google scholar: lookup
        42. Scholtissek C, Rohde W, Von Hoyningen V, Rott R. On the origin of the human influenza virus subtypes H2N2 and H3N2.. Virology 1978 Jun 1;87(1):13-20.
          pubmed: 664248doi: 10.1016/0042-6822(78)90153-8google scholar: lookup

        Citations

        This article has been cited 14 times.
        1. Oladunni FS, Oseni SO, Martinez-Sobrido L, Chambers TM. Equine Influenza Virus and Vaccines.. Viruses 2021 Aug 20;13(8).
          doi: 10.3390/v13081657pubmed: 34452521google scholar: lookup
        2. Miño S, Mojsiejczuk L, Guo W, Zhang H, Qi T, Du C, Zhang X, Wang J, Campos R, Wang X. Equine Influenza Virus in Asia: Phylogeographic Pattern and Molecular Features Reveal Circulation of an Autochthonous Lineage.. J Virol 2019 Jul 1;93(13).
          doi: 10.1128/JVI.00116-19pubmed: 31019053google scholar: lookup
        3. Kwaśnik M, Góra IM, Żmudziński JF, Rola J, Polak MP, Rożek W. Genetic Analysis of the M Gene of Equine Influenza Virus Strains Isolated in Poland, in the Context of the Asian-like Group Formation.. J Vet Res 2018 Dec;62(4):405-412.
          doi: 10.2478/jvetres-2018-0057pubmed: 30729195google scholar: lookup
        4. Alves Beuttemmüller E, Woodward A, Rash A, Dos Santos Ferraz LE, Fernandes Alfieri A, Alfieri AA, Elton D. Characterisation of the epidemic strain of H3N8 equine influenza virus responsible for outbreaks in South America in 2012.. Virol J 2016 Mar 19;13:45.
          doi: 10.1186/s12985-016-0503-9pubmed: 26993620google scholar: lookup
        5. Nagy A, Cerníková L, Jiřincová H, Havlíčková M, Horníčková J. Local-scale diversity and between-year "frozen evolution" of avian influenza A viruses in nature.. PLoS One 2014;9(7):e103053.
          doi: 10.1371/journal.pone.0103053pubmed: 25075739google scholar: lookup
        6. Sugita S, Oki H, Hasegawa T, Ishida N. Estimation models for the morbidity of the horses infected with equine influenza virus.. J Equine Sci 2008;19(3):63-6.
          doi: 10.1294/jes.19.63pubmed: 24833957google scholar: lookup
        7. Pouwels HG, Van de Zande SM, Horspool LJ, Hoeijmakers MJ. Efficacy of a non-updated, Matrix-C-based equine influenza subunit-tetanus vaccine following Florida sublineage clade 2 challenge.. Vet Rec 2014 Jun 21;174(25):633.
          doi: 10.1136/vr.101993pubmed: 24795071google scholar: lookup
        8. Lu G, Guo W, Qi T, Ma J, Zhao S, Tian Z, Pan J, Zhu C, Wang X, Xiang W. Genetic analysis of the PB1-F2 gene of equine influenza virus.. Virus Genes 2013 Oct;47(2):250-8.
          doi: 10.1007/s11262-013-0935-xpubmed: 23780220google scholar: lookup
        9. Bountouri M, Fragkiadaki E, Ntafis V, Kanellos T, Xylouri E. Phylogenetic and molecular characterization of equine H3N8 influenza viruses from Greece (2003 and 2007): evidence for reassortment between evolutionary lineages.. Virol J 2011 Jul 14;8:350.
          doi: 10.1186/1743-422X-8-350pubmed: 21756308google scholar: lookup
        10. Murcia PR, Wood JL, Holmes EC. Genome-scale evolution and phylodynamics of equine H3N8 influenza A virus.. J Virol 2011 Jun;85(11):5312-22.
          doi: 10.1128/JVI.02619-10pubmed: 21430049google scholar: lookup
        11. Koelle K, Khatri P, Kamradt M, Kepler TB. A two-tiered model for simulating the ecological and evolutionary dynamics of rapidly evolving viruses, with an application to influenza.. J R Soc Interface 2010 Sep 6;7(50):1257-74.
          doi: 10.1098/rsif.2010.0007pubmed: 20335193google scholar: lookup
        12. Adeyefa CA, James ML, McCauley JW. Antigenic and genetic analysis of equine influenza viruses from tropical Africa in 1991.. Epidemiol Infect 1996 Oct;117(2):367-74.
          doi: 10.1017/s0950268800001552pubmed: 8870635google scholar: lookup
        13. Ballagi-Pordány A, Wehmann E, Herczeg J, Belák S, Lomniczi B. Identification and grouping of Newcastle disease virus strains by restriction site analysis of a region from the F gene.. Arch Virol 1996;141(2):243-61.
          doi: 10.1007/BF01718397pubmed: 8634018google scholar: lookup
        14. Binns MM, Daly JM, Chirnside ED, Mumford JA, Wood JM, Richards CM, Daniels RS. Genetic and antigenic analysis of an equine influenza H 3 isolate from the 1989 epidemic.. Arch Virol 1993;130(1-2):33-43.
          doi: 10.1007/BF01318994pubmed: 8503788google scholar: lookup