Evolution and ecology of influenza A viruses.
Journal: 1992/June - Microbiological reviews
ISSN: 0146-0749
PUBMED: 1579108
Abstract:
In this review we examine the hypothesis that aquatic birds are the primordial source of all influenza viruses in other species and study the ecological features that permit the perpetuation of influenza viruses in aquatic avian species. Phylogenetic analysis of the nucleotide sequence of influenza A virus RNA segments coding for the spike proteins (HA, NA, and M2) and the internal proteins (PB2, PB1, PA, NP, M, and NS) from a wide range of hosts, geographical regions, and influenza A virus subtypes support the following conclusions. (i) Two partly overlapping reservoirs of influenza A viruses exist in migrating waterfowl and shorebirds throughout the world. These species harbor influenza viruses of all the known HA and NA subtypes. (ii) Influenza viruses have evolved into a number of host-specific lineages that are exemplified by the NP gene and include equine Prague/56, recent equine strains, classical swine and human strains, H13 gull strains, and all other avian strains. Other genes show similar patterns, but with extensive evidence of genetic reassortment. Geographical as well as host-specific lineages are evident. (iii) All of the influenza A viruses of mammalian sources originated from the avian gene pool, and it is possible that influenza B viruses also arose from the same source. (iv) The different virus lineages are predominantly host specific, but there are periodic exchanges of influenza virus genes or whole viruses between species, giving rise to pandemics of disease in humans, lower animals, and birds. (v) The influenza viruses currently circulating in humans and pigs in North America originated by transmission of all genes from the avian reservoir prior to the 1918 Spanish influenza pandemic; some of the genes have subsequently been replaced by others from the influenza gene pool in birds. (vi) The influenza virus gene pool in aquatic birds of the world is probably perpetuated by low-level transmission within that species throughout the year. (vii) There is evidence that most new human pandemic strains and variants have originated in southern China. (viii) There is speculation that pigs may serve as the intermediate host in genetic exchange between influenza viruses in avian and humans, but experimental evidence is lacking. (ix) Once the ecological properties of influenza viruses are understood, it may be possible to interdict the introduction of new influenza viruses into humans.
Relations:
Content
Citations
(1K+)
References
(161)
Diseases
(1)
Organisms
(4)
Processes
(2)
Affiliates
(1)
Similar articles
Articles by the same authors
Discussion board
Microbiol Rev 56(1): 152-179

Evolution and ecology of influenza A viruses.

Abstract

In this review we examine the hypothesis that aquatic birds are the primordial source of all influenza viruses in other species and study the ecological features that permit the perpetuation of influenza viruses in aquatic avian species. Phylogenetic analysis of the nucleotide sequence of influenza A virus RNA segments coding for the spike proteins (HA, NA, and M2) and the internal proteins (PB2, PB1, PA, NP, M, and NS) from a wide range of hosts, geographical regions, and influenza A virus subtypes support the following conclusions. (i) Two partly overlapping reservoirs of influenza A viruses exist in migrating waterfowl and shorebirds throughout the world. These species harbor influenza viruses of all the known HA and NA subtypes. (ii) Influenza viruses have evolved into a number of host-specific lineages that are exemplified by the NP gene and include equine Prague/56, recent equine strains, classical swine and human strains, H13 gull strains, and all other avian strains. Other genes show similar patterns, but with extensive evidence of genetic reassortment. Geographical as well as host-specific lineages are evident. (iii) All of the influenza A viruses of mammalian sources originated from the avian gene pool, and it is possible that influenza B viruses also arose from the same source. (iv) The different virus lineages are predominantly host specific, but there are periodic exchanges of influenza virus genes or whole viruses between species, giving rise to pandemics of disease in humans, lower animals, and birds. (v) The influenza viruses currently circulating in humans and pigs in North America originated by transmission of all genes from the avian reservoir prior to the 1918 Spanish influenza pandemic; some of the genes have subsequently been replaced by others from the influenza gene pool in birds. (vi) The influenza virus gene pool in aquatic birds of the world is probably perpetuated by low-level transmission within that species throughout the year. (vii) There is evidence that most new human pandemic strains and variants have originated in southern China. (viii) There is speculation that pigs may serve as the intermediate host in genetic exchange between influenza viruses in avian and humans, but experimental evidence is lacking. (ix) Once the ecological properties of influenza viruses are understood, it may be possible to interdict the introduction of new influenza viruses into humans.

Full text

Full text is available as a scanned copy of the original print version. Get a printable copy (PDF file) of the complete article (6.2M), or click on a page image below to browse page by page. Links to PubMed are also available for Selected References.

Images in this article

Click on the image to see a larger version.

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Ackerman E, Longini IM, Jr, Seaholm SK, Hedin AS. Simulation of mechanisms of viral interference in influenza. Int J Epidemiol. 1990 Jun;19(2):444–454. [PubMed] [Google Scholar]
  • 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):3884–3888.[PMC free article] [PubMed] [Google Scholar]
  • Akoto-Amanfu E, Sivasubramanian N, Nayak DP. Primary structure of the polymerase acidic (PA) gene of an influenza B virus (B/Sing/222/79). Virology. 1987 Jul;159(1):147–153. [PubMed] [Google Scholar]
  • Alexander DJ. Influenza A isolations from exotic caged birds. Vet Rec. 1988 Oct 22;123(17):442–442. [PubMed] [Google Scholar]
  • Almond JW. A single gene determines the host range of influenza virus. Nature. 1977 Dec 15;270(5638):617–618. [PubMed] [Google Scholar]
  • Altmüller A, Fitch WM, Scholtissek C. Biological and genetic evolution of the nucleoprotein gene of human influenza A viruses. J Gen Virol. 1989 Aug;70(Pt 8):2111–2119. [PubMed] [Google Scholar]
  • Bean WJ, Schell M, Katz J, Kawaoka Y, Naeve C, Gorman O, Webster RG. Evolution of the H3 influenza virus hemagglutinin from human and nonhuman hosts. J Virol. 1992 Feb;66(2):1129–1138.[PMC free article] [PubMed] [Google Scholar]
  • Bean WJ. Correlation of influenza A virus nucleoprotein genes with host species. Virology. 1984 Mar;133(2):438–442. [PubMed] [Google Scholar]
  • Bean WJ, Kawaoka Y, Wood JM, Pearson JE, Webster RG. Characterization of virulent and avirulent A/chicken/Pennsylvania/83 influenza A viruses: potential role of defective interfering RNAs in nature. J Virol. 1985 Apr;54(1):151–160.[PMC free article] [PubMed] [Google Scholar]
  • Beare AS, Webster RG. Replication of avian influenza viruses in humans. Arch Virol. 1991;119(1-2):37–42. [PubMed] [Google Scholar]
  • Becker WB. The isolation and classification of Tern virus: influenza A-Tern South Africa--1961. J Hyg (Lond) 1966 Sep;64(3):309–320.[PMC free article] [PubMed] [Google Scholar]
  • 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.[PMC free article] [PubMed] [Google Scholar]
  • Briedis DJ, Lamb RA. Influenza B virus genome: sequences and structural organization of RNA segment 8 and the mRNAs coding for the NS1 and NS2 proteins. J Virol. 1982 Apr;42(1):186–193.[PMC free article] [PubMed] [Google Scholar]
  • Briedis DJ, Lamb RA, Choppin PW. Sequence of RNA segment 7 of the influenza B virus genome: partial amino acid homology between the membrane proteins (M1) of influenza A and B viruses and conservation of a second open reading frame. Virology. 1982 Jan 30;116(2):581–588. [PubMed] [Google Scholar]
  • Briedis DJ, Tobin M. Influenza B virus genome: complete nucleotide sequence of the influenza B/lee/40 virus genome RNA segment 5 encoding the nucleoprotein and comparison with the B/Singapore/222/79 nucleoprotein. Virology. 1984 Mar;133(2):448–455. [PubMed] [Google Scholar]
  • 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):221–232. [PubMed] [Google Scholar]
  • 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] [Google Scholar]
  • Buonagurio DA, Nakada S, Parvin JD, Krystal M, Palese P, Fitch WM. Evolution of human influenza A viruses over 50 years: rapid, uniform rate of change in NS gene. Science. 1986 May 23;232(4753):980–982. [PubMed] [Google Scholar]
  • Chambers TM, Kawaoka Y, Webster RG. Protection of chickens from lethal influenza infection by vaccinia-expressed hemagglutinin. Virology. 1988 Dec;167(2):414–421. [PubMed] [Google Scholar]
  • Chambers TM, Yamnikova S, Kawaoka Y, Lvov DK, Webster RG. Antigenic and molecular characterization of subtype H13 hemagglutinin of influenza virus. Virology. 1989 Sep;172(1):180–188. [PubMed] [Google Scholar]
  • Coleman MT, Dowdle WR, Pereira HG, Schild GC, Chang WK. The Hong Kong-68 influenza A2 variant. Lancet. 1968 Dec 28;2(7583):1384–1386. [PubMed] [Google Scholar]
  • Cox NJ, Bai ZS, Kendal AP. Laboratory-based surveillance of influenza A(H1N1) and A(H3N2) viruses in 1980-81: antigenic and genomic analyses. Bull World Health Organ. 1983;61(1):143–152.[PMC free article] [PubMed] [Google Scholar]
  • Dacso CC, Couch RB, Six HR, Young JF, Quarles JM, Kasel JA. Sporadic occurrence of zoonotic swine influenza virus infections. J Clin Microbiol. 1984 Oct;20(4):833–835.[PMC free article] [PubMed] [Google Scholar]
  • 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):457–464. [PubMed] [Google Scholar]
  • De BK, Nayak DP. Defective interfering influenza viruses and host cells: establishment and maintenance of persistent influenza virus infection in MDBK and HeLa cells. J Virol. 1980 Dec;36(3):847–859.[PMC free article] [PubMed] [Google Scholar]
  • DeBorde DC, Naeve CW, Herlocher ML, Maassab HF. Nucleotide sequences of the PA and PB1 genes of B/Ann Arbor/1/66 virus: comparison with genes of B/Lee/40 and type A influenza viruses. Virus Res. 1987 Jul;8(1):33–41. [PubMed] [Google Scholar]
  • Desselberger U, Racaniello VR, Zazra JJ, Palese P. The 3' and 5'-terminal sequences of influenza A, B and C virus RNA segments are highly conserved and show partial inverted complementarity. Gene. 1980 Feb;8(3):315–328. [PubMed] [Google Scholar]
  • 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):408–417. [PubMed] [Google Scholar]
  • Downie JC, Laver WG. Isolation of a type A influenza virus from an Australian pelagic bird. Virology. 1973 Feb;51(2):259–269. [PubMed] [Google Scholar]
  • 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):315–323. [PubMed] [Google Scholar]
  • Frank AL, Taber LH, Wells JM. Individuals infected with two subtypes of influenza A virus in the same season. J Infect Dis. 1983 Jan;147(1):120–124. [PubMed] [Google Scholar]
  • Frielle DW, Huang DD, Youngner JS. Persistent infection with influenza A virus: evolution of virus mutants. Virology. 1984 Oct 15;138(1):103–117. [PubMed] [Google Scholar]
  • Gammelin M, Altmüller A, Reinhardt U, Mandler J, Harley VR, Hudson PJ, Fitch WM, Scholtissek C. Phylogenetic analysis of nucleoproteins suggests that human influenza A viruses emerged from a 19th-century avian ancestor. Mol Biol Evol. 1990 Mar;7(2):194–200. [PubMed] [Google Scholar]
  • Geraci JR, St Aubin DJ, Barker IK, Webster RG, Hinshaw VS, Bean WJ, Ruhnke HL, Prescott JH, Early G, Baker AS, et al. Mass mortality of harbor seals: pneumonia associated with influenza A virus. Science. 1982 Feb 26;215(4536):1129–1131. [PubMed] [Google Scholar]
  • Gething MJ, Bye J, Skehel J, Waterfield M. Cloning and DNA sequence of double-stranded copies of haemagglutinin genes from H2 and H3 strains elucidates antigenic shift and drift in human influenza virus. Nature. 1980 Sep 25;287(5780):301–306. [PubMed] [Google Scholar]
  • Gorman OT, Bean WJ, Kawaoka Y, Donatelli I, Guo YJ, Webster RG. Evolution of influenza A virus nucleoprotein genes: implications for the origins of H1N1 human and classical swine viruses. J Virol. 1991 Jul;65(7):3704–3714.[PMC free article] [PubMed] [Google Scholar]
  • Gorman OT, Bean WJ, Kawaoka Y, Webster RG. Evolution of the nucleoprotein gene of influenza A virus. J Virol. 1990 Apr;64(4):1487–1497.[PMC free article] [PubMed] [Google Scholar]
  • Gorman OT, Donis RO, Kawaoka Y, Webster RG. Evolution of influenza A virus PB2 genes: implications for evolution of the ribonucleoprotein complex and origin of human influenza A virus. J Virol. 1990 Oct;64(10):4893–4902.[PMC free article] [PubMed] [Google Scholar]
  • Guo YJ, Jin FG, Wang P, Wang M, Zhu JM. Isolation of influenza C virus from pigs and experimental infection of pigs with influenza C virus. J Gen Virol. 1983 Jan;64(Pt 1):177–182. [PubMed] [Google Scholar]
  • Haesebrouck F, Biront P, Pensaert MB, Leunen J. Epizootics of respiratory tract disease in swine in Belgium due to H3N2 influenza virus and experimental reproduction of disease. Am J Vet Res. 1985 Sep;46(9):1926–1928. [PubMed] [Google Scholar]
  • Halvorson D, Karunakaran D, Senne D, Kelleher C, Bailey C, Abraham A, Hinshaw V, Newman J. Epizootiology of avian influenza--simultaneous monitoring of sentinel ducks and turkeys in Minnesota. Avian Dis. 1983 Jan-Mar;27(1):77–85. [PubMed] [Google Scholar]
  • Henderson IM, Hendy MD, Penny D. Influenza viruses, comets and the science of evolutionary trees. J Theor Biol. 1989 Oct 9;140(3):289–303. [PubMed] [Google Scholar]
  • Henderson IM, Penny D, Hendy MD. Models for the origin of influenza viruses. Nature. 1987 Mar 5;326(6108):22–22. [PubMed] [Google Scholar]
  • Hinshaw VS, Bean WJ, Geraci J, Fiorelli P, Early G, Webster RG. Characterization of two influenza A viruses from a pilot whale. J Virol. 1986 May;58(2):655–656.[PMC free article] [PubMed] [Google Scholar]
  • Hinshaw VS, Bean WJ, Jr, Webster RG, Easterday BC. The prevalence of influenza viruses in swine and the antigenic and genetic relatedness of influenza viruses from man and swine. Virology. 1978 Jan;84(1):51–62. [PubMed] [Google Scholar]
  • Hinshaw VS, Bean WJ, Webster RG, Rehg JE, Fiorelli P, Early G, Geraci JR, St Aubin DJ. Are seals frequently infected with avian influenza viruses? J Virol. 1984 Sep;51(3):863–865.[PMC free article] [PubMed] [Google Scholar]
  • Webster RG, Hinshaw VS, Laver WG. Selection and analysis of antigenic variants of the neuraminidase of N2 influenza viruses with monoclonal antibodies. Virology. 1982 Feb;117(1):93–104. [PubMed] [Google Scholar]
  • Hinshaw VS, Webster RG, Bean WJ, Downie J, Senne DA. Swine influenza-like viruses in turkeys: potential source of virus for humans? Science. 1983 Apr 8;220(4593):206–208. [PubMed] [Google Scholar]
  • Hinshaw VS, Webster RG, Turner B. Novel influenza A viruses isolated from Canadian feral ducks: including strains antigenically related to swine influenza (Hsw1N1) viruses. J Gen Virol. 1978 Oct;41(1):115–127. [PubMed] [Google Scholar]
  • Hinshaw VS, Wood JM, Webster RG, Deibel R, Turner B. Circulation of influenza viruses and paramyxoviruses in waterfowl originating from two different areas of North America. Bull World Health Organ. 1985;63(4):711–719.[PMC free article] [PubMed] [Google Scholar]
  • Holland J, Spindler K, Horodyski F, Grabau E, Nichol S, VandePol S. Rapid evolution of RNA genomes. Science. 1982 Mar 26;215(4540):1577–1585. [PubMed] [Google Scholar]
  • Hope-Simpson RE. Epidemic mechanisms of type A influenza. J Hyg (Lond) 1979 Aug;83(1):11–26.[PMC free article] [PubMed] [Google Scholar]
  • Hope-Simpson RE. The role of season in the epidemiology of influenza. J Hyg (Lond) 1981 Feb;86(1):35–47.[PMC free article] [PubMed] [Google Scholar]
  • Hope-Simpson RE, Golubev DB. A new concept of the epidemic process of influenza A virus. Epidemiol Infect. 1987 Aug;99(1):5–54.[PMC free article] [PubMed] [Google Scholar]
  • Hoyle F, Wickramasinghe NC. Sunspots and influenza. Nature. 1990 Jan 25;343(6256):304–304. [PubMed] [Google Scholar]
  • Ibrahim HM, Awang IP, Alexander DJ, Manvell RJ, Aini I, Ibrahim AL. Isolations of influenza A viruses from passerine birds in Malaysia. Vet Rec. 1990 Nov 24;127(21):528–528. [PubMed] [Google Scholar]
  • Israël A. Productive and abortive infection of L cells by fowl plague virus (FPV): comparison of in vivo and in vitro translation products of the virus mRNAs. J Gen Virol. 1980 Apr;47(2):473–483. [PubMed] [Google Scholar]
  • Ito T, Gorman OT, Kawaoka Y, Bean WJ, Webster RG. Evolutionary analysis of the influenza A virus M gene with comparison of the M1 and M2 proteins. J Virol. 1991 Oct;65(10):5491–5498.[PMC free article] [PubMed] [Google Scholar]
  • Katagiri S, Ohizumi A, Homma M. An outbreak of type C influenza in a children's home. J Infect Dis. 1983 Jul;148(1):51–56. [PubMed] [Google Scholar]
  • Katz JM, Naeve CW, Webster RG. Host cell-mediated variation in H3N2 influenza viruses. Virology. 1987 Feb;156(2):386–395. [PubMed] [Google Scholar]
  • Kawaoka Y, Chambers TM, Sladen WL, Webster RG. Is the gene pool of influenza viruses in shorebirds and gulls different from that in wild ducks? Virology. 1988 Mar;163(1):247–250. [PubMed] [Google Scholar]
  • Kawaoka Y, Krauss S, Webster RG. Avian-to-human transmission of the PB1 gene of influenza A viruses in the 1957 and 1968 pandemics. J Virol. 1989 Nov;63(11):4603–4608.[PMC free article] [PubMed] [Google Scholar]
  • 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):159–164. [PubMed] [Google Scholar]
  • 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):759–767. [PubMed] [Google Scholar]
  • Kemdirim S, Palefsky J, Briedis DJ. Influenza B virus PB1 protein; nucleotide sequence of the genome RNA segment predicts a high degree of structural homology with the corresponding influenza A virus polymerase protein. Virology. 1986 Jul 15;152(1):126–135. [PubMed] [Google Scholar]
  • Kendal AP, Kiley MP. Characterization of influenza virus neuraminidases: peptide changes associated with antigenic divergence between early and late N2 neuraminidases. J Virol. 1973 Dec;12(6):1482–1490.[PMC free article] [PubMed] [Google Scholar]
  • Kendal AP, Minuse E, Maassab HF, Hennessy AV, Davenport FM. Influenza neuraminidase antibody patterns of man. Am J Epidemiol. 1973 Aug;98(2):96–103. [PubMed] [Google Scholar]
  • Khatchikian D, Orlich M, Rott R. Increased viral pathogenicity after insertion of a 28S ribosomal RNA sequence into the haemagglutinin gene of an influenza virus. Nature. 1989 Jul 13;340(6229):156–157. [PubMed] [Google Scholar]
  • Kida H, Shortridge KF, Webster RG. Origin of the hemagglutinin gene of H3N2 influenza viruses from pigs in China. Virology. 1988 Jan;162(1):160–166. [PubMed] [Google Scholar]
  • Kistner O, Müller H, Becht H, Scholtissek C. Phosphopeptide fingerprints of nucleoproteins of various influenza A virus strains grown in different host cells. J Gen Virol. 1985 Mar;66(Pt 3):465–472. [PubMed] [Google Scholar]
  • Kistner O, Müller K, Scholtissek C. Differential phosphorylation of the nucleoprotein of influenza A viruses. J Gen Virol. 1989 Sep;70(Pt 9):2421–2431. [PubMed] [Google Scholar]
  • Klingeborn B, Englund L, Rott R, Juntti N, Rockborn G. An avian influenza A virus killing a mammalian species--the mink. Brief report. Arch Virol. 1985;86(3-4):347–351. [PubMed] [Google Scholar]
  • Krystal M, Elliott RM, Benz EW, Jr, Young JF, Palese P. Evolution of influenza A and B viruses: conservation of structural features in the hemagglutinin genes. Proc Natl Acad Sci U S A. 1982 Aug;79(15):4800–4804.[PMC free article] [PubMed] [Google Scholar]
  • Kundin WD. Hong Kong A-2 influenza virus infection among swine during a human epidemic in Taiwan. Nature. 1970 Nov 28;228(5274):857–857. [PubMed] [Google Scholar]
  • 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):383–391. [PubMed] [Google Scholar]
  • Lipkind M, Bürger H, Rott R, Scholtissek C. Genetic characterization of influenza A viruses isolated from birds in Israel. A contribution to the ecology of avian influenza viruses. Zentralbl Veterinarmed B. 1984 Dec;31(10):721–728. [PubMed] [Google Scholar]
  • Londo DR, Davis AR, Nayak DP. Complete nucleotide sequence of the nucleoprotein gene of influenza B virus. J Virol. 1983 Sep;47(3):642–648.[PMC free article] [PubMed] [Google Scholar]
  • Lvov DK, Zdanov VM, Sazonov AA, Braude NA, Vladimirtceva EA, Agafonova LV, Skljanskaja EI, Kaverin NV, Reznik VI, Pysina TV, et al. Comparison of influenza viruses isolated from man and from whales. Bull World Health Organ. 1978;56(6):923–930.[PMC free article] [PubMed] [Google Scholar]
  • Lyons D, Murphy G. Influenza causing sunspots? Nature. 1990 Mar 1;344(6261):10–10. [PubMed] [Google Scholar]
  • Mackenzie JS, Edwards EC, Holmes RM, Hinshaw VS. Isolation of ortho- and paramyxoviruses from wild birds in Western Australia, and the characterization of novel influenza A viruses. Aust J Exp Biol Med Sci. 1984 Feb;62(Pt 1):89–99. [PubMed] [Google Scholar]
  • Masurel N, Heijtink RA. Recycling of H1N1 influenza A virus in man--a haemagglutinin antibody study. J Hyg (Lond) 1983 Jun;90(3):397–402.[PMC free article] [PubMed] [Google Scholar]
  • Matsuoka Y, Kida H, Yanagowa R. Isolation of an influenza virus subtype Hav4Navl from a budgerigar. Microbiol Immunol. 1979;23(1):35–38. [PubMed] [Google Scholar]
  • Matsuura Y, Yanagawa R, Noda H. Experimental infection of mink with influenza A viruses. Brief report. Arch Virol. 1979;62(1):71–76. [PubMed] [Google Scholar]
  • McMichael AJ, Gotch FM, Dongworth DW, Clark A, Potter CW. Declining T-cell immunity to influenza, 1977-82. Lancet. 1983 Oct 1;2(8353):762–764. [PubMed] [Google Scholar]
  • Monto AS, Maassab HF. Serologic responses to nonprevalent influenza A viruses during intercyclic periods. Am J Epidemiol. 1981 Mar;113(3):236–244. [PubMed] [Google Scholar]
  • MULDER J, MASUREL N. Pre-epidemic antibody against 1957 strain of Asiatic influenza in serum of older people living in the Netherlands. Lancet. 1958 Apr 19;1(7025):810–814. [PubMed] [Google Scholar]
  • Murphy BR, Harper J, Sly DL, London WT, Miller NT, Webster RG. Evaluation of the A/Seal/Mass/1/80 virus in squirrel monkeys. Infect Immun. 1983 Oct;42(1):424–426.[PMC free article] [PubMed] [Google Scholar]
  • Naeve CW, Hinshaw VS, Webster RG. Mutations in the hemagglutinin receptor-binding site can change the biological properties of an influenza virus. J Virol. 1984 Aug;51(2):567–569.[PMC free article] [PubMed] [Google Scholar]
  • Nakada S, Creager RS, Krystal M, Palese P. Complete nucleotide sequence of the influenza C/California/78 virus nucleoprotein gene. Virus Res. 1984 Sep;1(6):433–441. [PubMed] [Google Scholar]
  • Nakajima K, Desselberger U, Palese P. Recent human influenza A (H1N1) viruses are closely related genetically to strains isolated in 1950. Nature. 1978 Jul 27;274(5669):334–339. [PubMed] [Google Scholar]
  • Nakajima K, Nakajima S, Sugiura A. The possible origin of H3N2 influenza virus. Virology. 1982 Jul 30;120(2):504–509. [PubMed] [Google Scholar]
  • Nakajima K, Nobusawa E, Nakajima S. Genetic relatedness between A/Swine/Iowa/15/30(H1N1) and human influenza viruses. Virology. 1984 Nov;139(1):194–198. [PubMed] [Google Scholar]
  • Nakajima S, Sugiura A. Neurovirulence of influenza virus in mice. II. Mechanism of virulence as studied in a neuroblastoma cell line. Virology. 1980 Mar;101(2):450–457. [PubMed] [Google Scholar]
  • Nardelli L, Pascucci S, Gualandi GL, Loda P. Outbreaks of classical swine influenza in Italy in 1976. Zentralbl Veterinarmed B. 1978 Dec;25(10):853–857. [PubMed] [Google Scholar]
  • Nerome K, Nakayama M, Ishida M, Fukumi H, Butterfield WK, Webster RG, Campbell CH. Isolation and serological characterization of influenza A viruses from birds that were dead on arrival at Tokyo airport. Arch Virol. 1978;57(3):261–270. [PubMed] [Google Scholar]
  • Nestorowicz A, Kawaoka Y, Bean WJ, Webster RG. Molecular analysis of the hemagglutinin genes of Australian H7N7 influenza viruses: role of passerine birds in maintenance or transmission? Virology. 1987 Oct;160(2):411–418. [PubMed] [Google Scholar]
  • Nishikawa F, Sugiyama T, Yamamoto K, Yonemura H. Isolation of influenza type A viruses from imported pet birds. Jpn J Med Sci Biol. 1977 Feb;30(1):31–36. [PubMed] [Google Scholar]
  • O'Callaghan RJ, Gohd RS, Labat DD. Human antibody to influenza C virus: its age-related distribution and distinction from receptor analogs. Infect Immun. 1980 Nov;30(2):500–505.[PMC free article] [PubMed] [Google Scholar]
  • Okazaki K, Kawaoka Y, Webster RG. Evolutionary pathways of the PA genes of influenza A viruses. Virology. 1989 Oct;172(2):601–608. [PubMed] [Google Scholar]
  • Okazaki K, Yanagawa R, Kida H. Contact infection of mink with 5 subtypes of avian influenza virus. Brief report. Arch Virol. 1983;77(2-4):265–269. [PubMed] [Google Scholar]
  • Otsuki K, Kariya H, Matsuo K, Sugiyama S, Hoshina K, Yoshikane T, Matsumoto A, Tsubokura M. Isolation of influenza A viruses from migratory waterfowls in San-In District Japan in the winter of 1984-1985. Nihon Juigaku Zasshi. 1987 Aug;49(4):721–723. [PubMed] [Google Scholar]
  • Otsuki K, Takemoto O, Fujimoto R, Kawaoka Y, Tsubokura M. Isolation of influenza A viruses from migratory waterfowls in San-in District, Western Japan in winters of 1980-1982. Zentralbl Bakteriol Mikrobiol Hyg A. 1987 Jun;265(1-2):235–242. [PubMed] [Google Scholar]
  • Otsuki K, Takemoto O, Fujimoto R, Yamazaki K, Kubota N, Hosaki H, Kawaoka Y, Tsubokura M. Isolation of influenza A viruses from migratory waterfowls in San-in District, Western Japan, in the winter of 1982-1983. Acta Virol. 1987 Sep;31(5):439–442. [PubMed] [Google Scholar]
  • Palese P, Young JF. Variation of influenza A, B, and C viruses. Science. 1982 Mar 19;215(4539):1468–1474. [PubMed] [Google Scholar]
  • Pease CM. An evolutionary epidemiological mechanism, with applications to type A influenza. Theor Popul Biol. 1987 Jun;31(3):422–452. [PubMed] [Google Scholar]
  • Pensaert M, Ottis K, Vandeputte J, Kaplan MM, Bachmann PA. Evidence for the natural transmission of influenza A virus from wild ducts to swine and its potential importance for man. Bull World Health Organ. 1981;59(1):75–78.[PMC free article] [PubMed] [Google Scholar]
  • Raymond FL, Caton AJ, Cox NJ, Kendal AP, Brownlee GG. The antigenicity and evolution of influenza H1 haemagglutinin, from 1950-1957 and 1977-1983: two pathways from one gene. Virology. 1986 Jan 30;148(2):275–287. [PubMed] [Google Scholar]
  • Robertson JS, Bootman JS, Newman R, Oxford JS, Daniels RS, Webster RG, Schild GC. Structural changes in the haemagglutinin which accompany egg adaptation of an influenza A(H1N1) virus. Virology. 1987 Sep;160(1):31–37. [PubMed] [Google Scholar]
  • Rogers GN, D'Souza BL. Receptor binding properties of human and animal H1 influenza virus isolates. Virology. 1989 Nov;173(1):317–322. [PubMed] [Google Scholar]
  • Rogers GN, Paulson JC. Receptor determinants of human and animal influenza virus isolates: differences in receptor specificity of the H3 hemagglutinin based on species of origin. Virology. 1983 Jun;127(2):361–373. [PubMed] [Google Scholar]
  • 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;304(5921):76–78. [PubMed] [Google Scholar]
  • Rogers GN, Pritchett TJ, Lane JL, Paulson JC. Differential sensitivity of human, avian, and equine influenza A viruses to a glycoprotein inhibitor of infection: selection of receptor specific variants. Virology. 1983 Dec;131(2):394–408. [PubMed] [Google Scholar]
  • Rota PA, Rocha EP, Harmon MW, Hinshaw VS, Sheerar MG, Kawaoka Y, Cox NJ, Smith TF. Laboratory characterization of a swine influenza virus isolated from a fatal case of human influenza. J Clin Microbiol. 1989 Jun;27(6):1413–1416.[PMC free article] [PubMed] [Google Scholar]
  • Rott R, Orlich M, Scholtissek C. Correlation of pathogenicity and gene constellation of influenza A viruses. III. Non-pathogenic recombinants derived from highly pathogenic parent strains. J Gen Virol. 1979 Aug;44(2):471–477. [PubMed] [Google Scholar]
  • Ryan-Poirier KA, Kawaoka Y. Distinct glycoprotein inhibitors of influenza A virus in different animal sera. J Virol. 1991 Jan;65(1):389–395.[PMC free article] [PubMed] [Google Scholar]
  • Schnurrenberger PR, Woods GT, Martin RJ. Serologic evidence of human infection with swine influenza virus. Am Rev Respir Dis. 1970 Sep;102(3):356–361. [PubMed] [Google Scholar]
  • Scholtissek C. Stability of infectious influenza A viruses at low pH and at elevated temperature. Vaccine. 1985 Sep;3(3 Suppl):215–218. [PubMed] [Google Scholar]
  • Scholtissek C, Bürger H, Bachmann PA, Hannoun C. Genetic relatedness of hemagglutinins of the H1 subtype of influenza A viruses isolated from swine and birds. Virology. 1983 Sep;129(2):521–523. [PubMed] [Google Scholar]
  • 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] [Google Scholar]
  • Schulman JL, Palese P. Virulence factors of influenza A viruses: WSN virus neuraminidase required for plaque production in MDBK cells. J Virol. 1977 Oct;24(1):170–176.[PMC free article] [PubMed] [Google Scholar]
  • Shaw MW, Lamb RA, Erickson BW, Briedis DJ, Choppin PW. Complete nucleotide sequence of the neuraminidase gene of influenza B virus. Proc Natl Acad Sci U S A. 1982 Nov;79(22):6817–6821.[PMC free article] [PubMed] [Google Scholar]
  • Shortridge KF. Avian influenza A viruses of southern China and Hong Kong: ecological aspects and implications for man. Bull World Health Organ. 1982;60(1):129–135.[PMC free article] [PubMed] [Google Scholar]
  • Shortridge KF, Stuart-Harris CH. An influenza epicentre? Lancet. 1982 Oct 9;2(8302):812–813. [PubMed] [Google Scholar]
  • Shortridge KF, Webster RG. Geographical distribution of swine (Hsw1N1) and Hong Kong (H3N2) influenza virus variants in pigs in Southeast Asia. Intervirology. 1979;11(1):9–15. [PubMed] [Google Scholar]
  • Shortridge KF, Webster RG, Butterfield WK, Campbell CH. Persistence of Hong Kong influenza virus variants in pigs. Science. 1977 Jun 24;196(4297):1454–1455. [PubMed] [Google Scholar]
  • Sinnecker R, Sinnecker H, Zilske E, Köhler D. Surveillance of pelagic birds for influenza A viruses. Acta Virol. 1983 Jan;27(1):75–79. [PubMed] [Google Scholar]
  • Sivasubramanian N, Nayak DP. Sequence analysis of the polymerase 1 gene and the secondary structure prediction of polymerase 1 protein of human influenza virus A/WSN/33. J Virol. 1982 Oct;44(1):321–329.[PMC free article] [PubMed] [Google Scholar]
  • Slemons RD, Johnson DC, Osborn JS, Hayes F. Type-A influenza viruses isolated from wild free-flying ducks in California. Avian Dis. 1974 Jan-Mar;18(1):119–124. [PubMed] [Google Scholar]
  • Snyder MH, Buckler-White AJ, London WT, Tierney EL, Murphy BR. The avian influenza virus nucleoprotein gene and a specific constellation of avian and human virus polymerase genes each specify attenuation of avian-human influenza A/Pintail/79 reassortant viruses for monkeys. J Virol. 1987 Sep;61(9):2857–2863.[PMC free article] [PubMed] [Google Scholar]
  • Sonoguchi T, Naito H, Hara M, Takeuchi Y, Fukumi H. Cross-subtype protection in humans during sequential, overlapping, and/or concurrent epidemics caused by H3N2 and H1N1 influenza viruses. J Infect Dis. 1985 Jan;151(1):81–88. [PubMed] [Google Scholar]
  • 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] [Google Scholar]
  • Stallknecht DE, Kearney MT, Shane SM, Zwank PJ. Effects of pH, temperature, and salinity on persistence of avian influenza viruses in water. Avian Dis. 1990 Apr-Jun;34(2):412–418. [PubMed] [Google Scholar]
  • Stallknecht DE, Shane SM, Kearney MT, Zwank PJ. Persistence of avian influenza viruses in water. Avian Dis. 1990 Apr-Jun;34(2):406–411. [PubMed] [Google Scholar]
  • Stallknecht DE, Shane SM, Zwank PJ, Senne DA, Kearney MT. Avian influenza viruses from migratory and resident ducks of coastal Louisiana. Avian Dis. 1990 Apr-Jun;34(2):398–405. [PubMed] [Google Scholar]
  • Steinhauer DA, Holland JJ. Rapid evolution of RNA viruses. Annu Rev Microbiol. 1987;41:409–433. [PubMed] [Google Scholar]
  • Stünzner D, Thiel W, Pötsch F, Sixl W. Isolation of influenza viruses from exotic and Central European birds. Zentralbl Bakteriol A. 1980 Jun;247(1):8–17. [PubMed] [Google Scholar]
  • Sugimura T, Yonemochi H, Ogawa T, Tanaka Y, Kumagai T. Isolation of a recombinant influenza virus (Hsw 1 N2) from swine in Japan. Arch Virol. 1980;66(3):271–274. [PubMed] [Google Scholar]
  • Sugiura A, Ueda M. Neurovirulence of influenza virus in mice. I. Neurovirulence of recombinants between virulent and avirulent virus strains. Virology. 1980 Mar;101(2):440–449. [PubMed] [Google Scholar]
  • Suzuki Y, Kato H, Naeve CW, Webster RG. Single-amino-acid substitution in an antigenic site of influenza virus hemagglutinin can alter the specificity of binding to cell membrane-associated gangliosides. J Virol. 1989 Oct;63(10):4298–4302.[PMC free article] [PubMed] [Google Scholar]
  • Tian SF, Buckler-White AJ, London WT, Reck LJ, Chanock RM, Murphy BR. Nucleoprotein and membrane protein genes are associated with restriction of replication of influenza A/Mallard/NY/78 virus and its reassortants in squirrel monkey respiratory tract. J Virol. 1985 Mar;53(3):771–775.[PMC free article] [PubMed] [Google Scholar]
  • Treanor JJ, Snyder MH, London WT, Murphy BR. The B allele of the NS gene of avian influenza viruses, but not the A allele, attenuates a human influenza A virus for squirrel monkeys. Virology. 1989 Jul;171(1):1–9. [PubMed] [Google Scholar]
  • Tsubokura M, Otsuki K, Kawaoka Y, Yanagawa R. Isolation of influenza A viruses from migratory waterfowls in San-in District, Western Japan in 1979-1980. Zentralbl Bakteriol Mikrobiol Hyg B. 1981 Sep;173(6):494–500. [PubMed] [Google Scholar]
  • Tumova B, Easterday BC, Stumpa A. Simultaneous occurrence of A-equi-1 and A-equi-2 infleunza viruses in a small group of horses. Am J Epidemiol. 1972 Jan;95(1):80–87. [PubMed] [Google Scholar]
  • Influenza according to Hoyle. Nature. 1990 Mar 29;344(6265):374–374. [PubMed] [Google Scholar]
  • WADDELL GH, TEIGLAND MB, SIGEL MM. A NEW INFLUENZA VIRUS ASSOCIATED WITH EQUINE RESPIRATORY DISEASE. J Am Vet Med Assoc. 1963 Sep 15;143:587–590. [PubMed] [Google Scholar]
  • Wang M, Webster RG. Lack of persistence of influenza virus genetic information in ducks. Arch Virol. 1990;111(3-4):263–267. [PubMed] [Google Scholar]
  • Webster RG, Campbell CH, Granoff A. The "in vivo" production of "new" influenza A viruses. I. Genetic recombination between avian and mammalian influenza viruses. Virology. 1971 May;44(2):317–328. [PubMed] [Google Scholar]
  • Webster RG, Geraci J, Petursson G, Skirnisson K. Conjunctivitis in human beings caused by influenza A virus of seals. N Engl J Med. 1981 Apr 9;304(15):911–911. [PubMed] [Google Scholar]
  • Webster RG, Hinshaw VS, Bean WJ, Van Wyke KL, Geraci JR, St Aubin DJ, Petursson G. Characterization of an influenza A virus from seals. Virology. 1981 Sep;113(2):712–724. [PubMed] [Google Scholar]
  • Webster RG, Kawaoka Y, Bean WJ. What is the potential of avirulent influenza viruses to complement a cleavable hemagglutinin and generate virulent strains? Virology. 1989 Aug;171(2):484–492. [PubMed] [Google Scholar]
  • Webster RG, Laver WG, Tumova B. Studies on the origin of pandemic influenza viruses V. Persistence of Asian influenza virus hemagglutinin (H2) antigen in nature? Virology. 1975 Oct;67(2):534–543. [PubMed] [Google Scholar]
  • Webster RG, Morita M, Pridgen C, Tumova B. Ortho- and paramyxoviruses from migrating feral ducks: characterization of a new group of influenza A viruses. J Gen Virol. 1976 Aug;32(2):217–225. [PubMed] [Google Scholar]
  • Webster RG, Rott R. Influenza virus A pathogenicity: the pivotal role of hemagglutinin. Cell. 1987 Aug 28;50(5):665–666. [PubMed] [Google Scholar]
  • Webster RG, Yakhno M, Hinshaw VS, Bean WJ, Murti KG. Intestinal influenza: replication and characterization of influenza viruses in ducks. Virology. 1978 Feb;84(2):268–278. [PubMed] [Google Scholar]
  • Weis W, Brown JH, Cusack S, Paulson JC, Skehel JJ, Wiley DC. Structure of the influenza virus haemagglutinin complexed with its receptor, sialic acid. Nature. 1988 Jun 2;333(6172):426–431. [PubMed] [Google Scholar]
  • Whittaker RG, Underwood PA. A mechanism for influenza subtype disappearance. Med Hypotheses. 1980 Oct;6(10):997–1008. [PubMed] [Google Scholar]
  • Wilson IA, Skehel JJ, Wiley DC. Structure of the haemagglutinin membrane glycoprotein of influenza virus at 3 A resolution. Nature. 1981 Jan 29;289(5796):366–373. [PubMed] [Google Scholar]
  • Winkler GC, Cheville NF. Ultrastructural morphometric investigation of early lesions in the pulmonary alveolar region of pigs during experimental swine influenza infection. Am J Pathol. 1986 Mar;122(3):541–552.[PMC free article] [PubMed] [Google Scholar]
  • Wyde PR, Couch RB, Mackler BF, Cate TR, Levy BM. Effects of low- and high-passage influenza virus infection in normal and nude mice. Infect Immun. 1977 Jan;15(1):221–229.[PMC free article] [PubMed] [Google Scholar]
  • Yamada A, Brown LE, Webster RG. Characterization of H2 influenza virus hemagglutinin with monoclonal antibodies: influence of receptor specificity. Virology. 1984 Oct 30;138(2):276–286. [PubMed] [Google Scholar]
  • 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):112–122. [PubMed] [Google Scholar]
Department of Virology and Molecular Biology, St. Jude Children's Research Hospital, Memphis, Tennessee 38101.
Department of Virology and Molecular Biology, St. Jude Children's Research Hospital, Memphis, Tennessee 38101.
Abstract
In this review we examine the hypothesis that aquatic birds are the primordial source of all influenza viruses in other species and study the ecological features that permit the perpetuation of influenza viruses in aquatic avian species. Phylogenetic analysis of the nucleotide sequence of influenza A virus RNA segments coding for the spike proteins (HA, NA, and M2) and the internal proteins (PB2, PB1, PA, NP, M, and NS) from a wide range of hosts, geographical regions, and influenza A virus subtypes support the following conclusions. (i) Two partly overlapping reservoirs of influenza A viruses exist in migrating waterfowl and shorebirds throughout the world. These species harbor influenza viruses of all the known HA and NA subtypes. (ii) Influenza viruses have evolved into a number of host-specific lineages that are exemplified by the NP gene and include equine Prague/56, recent equine strains, classical swine and human strains, H13 gull strains, and all other avian strains. Other genes show similar patterns, but with extensive evidence of genetic reassortment. Geographical as well as host-specific lineages are evident. (iii) All of the influenza A viruses of mammalian sources originated from the avian gene pool, and it is possible that influenza B viruses also arose from the same source. (iv) The different virus lineages are predominantly host specific, but there are periodic exchanges of influenza virus genes or whole viruses between species, giving rise to pandemics of disease in humans, lower animals, and birds. (v) The influenza viruses currently circulating in humans and pigs in North America originated by transmission of all genes from the avian reservoir prior to the 1918 Spanish influenza pandemic; some of the genes have subsequently been replaced by others from the influenza gene pool in birds. (vi) The influenza virus gene pool in aquatic birds of the world is probably perpetuated by low-level transmission within that species throughout the year. (vii) There is evidence that most new human pandemic strains and variants have originated in southern China. (viii) There is speculation that pigs may serve as the intermediate host in genetic exchange between influenza viruses in avian and humans, but experimental evidence is lacking. (ix) Once the ecological properties of influenza viruses are understood, it may be possible to interdict the introduction of new influenza viruses into humans.
Collaboration tool especially designed for Life Science professionals.Drag-and-drop any entity to your messages.