Perpetuation and reassortment of gull influenza A viruses in Atlantic North America

Virology

Volumn 456-457, Issue 1, 2014, Pages 353-363

  Huang, Yanyan ^a   Wille, Michelle ^a,e   Benkaroun, Jessica ^a   Munro, Hannah ^a   Bond, Alexander L ^a,c   Fifield, David A ^b   Robertson, Gregory J ^c   Ojkic, Davor ^d   Whitney, Hugh ^b   Lang, Andrew S ^a  

^a MEMORIAL UNIVERSITY OF NEWFOUNDLAND   (Canada)

^b Newfoundland Department of Natural Resources   (Canada)

^c ENVIRONMENT CANADA   (Canada)

^d UNIVERSITY OF GUELPH   (Canada)

^e LINNAEUS UNIVERSITY   (Sweden)

Author keywords

Gulls; Laridae; Phylogenetics; Prevalence; Seroprevalence; Virus sequencing

Indexed keywords

VIRUS RNA;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ATLANTIC OCEAN; AVIAN INFLUENZA; AVIAN INFLUENZA VIRUS; BIRD; CLADISTICS; CONTROLLED STUDY; GENETIC REASSORTMENT; GENETIC VARIABILITY; GEOGRAPHIC DISTRIBUTION; MOLECULAR PHYLOGENY; NONHUMAN; NORTH AMERICA; NUCLEOTIDE SEQUENCE; POPULATION DYNAMICS; PRIORITY JOURNAL; RNA SEQUENCE; SEA GULL; SEASONAL VARIATION; SEQUENCE ANALYSIS; SEROPREVALENCE; UNINDEXED SEQUENCE; VIRUS CELL INTERACTION; VIRUS IDENTIFICATION; VIRUS TRANSMISSION;

GULLS; LARIDAE; PHYLOGENETICS; PREVALENCE; SEROPREVALENCE; VIRUS SEQUENCING;

ANIMALS; CHARADRIIFORMES; GENETIC VARIATION; INFLUENZA A VIRUS; INFLUENZA IN BIRDS; MOLECULAR SEQUENCE DATA; NORTH AMERICA; PREVALENCE; REASSORTANT VIRUSES; RNA, VIRAL; SEQUENCE ANALYSIS, DNA;

EID: 84900433146     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2014.04.009     Document Type: Article

References (69)

1. Alexander D.J. An overview of the epidemiology of avian influenza. Vaccine 2007, 25:5637-5644.
2. Altschul S.F., Madden T.L., Schaffer A.A., Zhang J., Zhang Z., Miller W., Lipman D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997, 25:3389-3402.
3. Arnal A., Vittecoq M., Pearce-Duvet J., Gauthier-Clerc M., Boulinier T., Jourdain E. Laridae: a neglected reservoir that could play a major role in avian influenza virus epidemiological dynamics. Crit. Rev. Microbiol. 2014, 10.3109/1040841x.2013.870967.
4. Bahl J., Vijaykrishna D., Holmes E.C., Smith G.J., Guan Y. Gene flow and competitive exclusion of avian influenza A virus in natural reservoir hosts. Virology 2009, 390:289-297.
5. Bao Y., Bolotov P., Dernovoy D., Kiryutin B., Zaslavsky L., Tatusova T., Ostell J., Lipman D. The Influenza Virus Resource at the National Center for Biotechnology Information. J. Virol. 2008, 82:596-601.
6. Becker W.B. The isolation and classification of tern virus: influenza Virus A/Tern/South Africa/1961. J. Hyg. 1966, 64:309-320.
7. Brown J., Poulson R., Carter D., Lebarbenchon C., Pantin-Jackwood M., Spackman E., Shepherd E., Killian M., Stallknecht D. Susceptibility of avian species to North American H13 low pathogenic avian influenza viruses. Avian Dis. 2012, 56:969-975.
8. Brown J.D., Luttrell M.P., Berghaus R.D., Kistler W., Keeler S.P., Howey A., Wilcox B., Hall J., Niles L., Dey A., Knutsen G., Fritz K., Stallknecht D.E. Prevalence of antibodies to type A influenza virus in wild avian species using two serologic assays. J. Wildl. Dis. 2010, 46:896-911.
9. Buscaglia C. A survey for avian influenza from gulls on the coasts of the District of Pinamar and the Lagoon Salada Grande, General Madariaga, Argentina. Avian Dis. 2012, 56:1017-1020.
10. Cardona C.J., Xing Z., Sandrock C.E., Davis C.E. Avian influenza in birds and mammals. Comp. Immunol. Microbiol. Infect. Dis. 2009, 32:255-273.
11. Chan C.-H., Lin K.-L., Chan Y., Wang Y.-L., Chi Y.-T., Tu H.-L., Shieh H.-K., Liu W.-T. Amplification of the entire genome of influenza A virus H1N1 and H3N2 subtypes by reverse-transcription polymerase chain reaction. J. Virol. Methods 2006, 136:38-43.
12. Chen H., Smith G.J.D., Zhang S.Y., Qin K., Wang J., Li K.S., Webster R.G., Peiris J.S.M., Guan Y. Avian flu H5N1 virus outbreak in migratory waterfowl. Nature 2005, 436:191-192.
13. Chen R., Holmes E.C. Frequent inter-species transmission and geographic subdivision in avian influenza viruses from wild birds. Virology 2009, 383:156-161.
14. Claas E.C., Osterhaus A.D., van Beek R., De Jong J.C., Rimmelzwaan G.F., Senne D.A., Krauss S., Shortridge K.F., Webster R.G. Human influenza A H5N1 virus related to a highly pathogenic avian influenza virus. Lancet 1998, 351:472-477.
15. Drummond A.J., Suchard M.A., Xie D., Rambaut A. Bayesian Phylogenetics with BEAUti and the BEAST 1.7. Mol. Biol. Evol. 2012, 29:1969-1973.
16. Dusek R.J., Hallgrimsson G.T., Ip H.S., Jónsson J.E., Sreevatsan S., Nashold S.W., TeSlaa J.L., Enomoto S., Halpin R.A., Lin X., Fedorova N., Stockwell T.B., Dugan V.G., Wentworth D.E., Hall J.S. North Atlantic migratory bird flyways provide routes for intercontinental movement of avian influenza viruses. PLoS One 2014, 9:e92075.
17. Fouchier R.A., Munster V., Wallensten A., Bestebroer T.M., Herfst S., Smith D., Rimmelzwaan G.F., Olsen B., Osterhaus A.D. Characterization of a novel influenza A virus hemagglutinin subtype (H16) obtained from black-headed gulls. J. Virol. 2005, 79:2814-2822.
18. Gao R., Cao B., Hu Y., Feng Z., Wang D., Hu W., Chen J., Jie Z., Qiu H., Xu K., Xu X., Lu H., Zhu W., Gao Z., Xiang N., Shen Y., He Z., Gu Y., Zhang Z., Yang Y., Zhao X., Zhou L., Li X., Zou S., Zhang Y., Li X., Yang L., Guo J., Dong J., Li Q., Dong L., Zhu Y., Bai T., Wang S., Hao P., Yang W., Zhang Y., Han J., Yu H., Li D., Gao G.F., Wu G., Wang Y., Yuan Z., Shu Y. Human infection with a novel avian-origin Influenza A (H7N9) virus. N. Engl. J. Med. 2013, 368:1888-1897.
19. Granter A., Wille M., Whitney H., Robertson G.J., Ojkic D., Lang A.S. The genome sequence of an H11N2 avian influenza virus from a Thick-billed Murre (Uria lomvia) shows marine-specific and regional patterns of relationships to other viruses. Virus Genes 2010, 41:224-230.
20. Hall J.S., TeSlaa J.L., Nashold S.W., Halpin R.A., Stockwell T., Wentworth D.E., Dugan V., Ip H.S. Evolution of a reassortant North American gull influenza virus lineage: drift, shift and stability. Virol. J. 2013, 10:179.
21. Hammouda A., Pearce-Duvet J., Chokri M.A., Arnal A., Gauthier-Clerc M., Boulinier T., Selmi S. Prevalence of influenza A antibodies in yellow-legged gull (Larus michahellis) eggs and adults in southern Tunisia. Vector-Borne Zoonotic Dis. 2011, 11:1583-1590.
22. Hanson B.A., Luttrell M.P., Goekjian V.H., Niles L., Swayne D.E., Senne D.A., Stallknecht D.E. Is the occurrence of avian influenza virus in Charadriiformes species and location dependent?. J. Wildl. Dis. 2008, 44:351-361.
23. Hinshaw V.S., Air G.M., Gibbs A.J., Graves L., Prescott B., Karunakaran D. Antigenic and genetic characterization of a novel hemagglutinin subtype of influenza A viruses from gulls. J. Virol. 1982, 42:865-872.
24. Hoffmann E., Stech J., Guan Y., Webster R.G., Perez D.R. Universal primer set for the full-length amplification of all influenza A viruses. Arch. Virol. 2001, 146:2275-2289.
25. Huang Y., Khan M., Mǎndoiu I.I. Neuraminidase subtyping of avian influenza viruses with PrimerHunter-designed primers and quadruplicate primer pools. PLoS One 2013, 8:e81842.
26. Huang Y., Wille M., Dobbin A., Robertson G.J., Ryan P., Ojkic D., Whitney H., Lang A.S. A four-year study of avian influenza virus prevalence and subtype diversity in ducks of Newfoundland, Canada. Can. J. Microbiol. 2013, 59:701-708.
27. Huang Y., Wille M., Dobbin A., Walzthöni N., Robertson G.J., Ojkic D., Whitney H., Lang A.S. Genetic structure of avian influenza viruses from ducks of the Atlantic flyway of North America. PLoS One 2014, 9:e86999.
28. Hulsager C.K., Breum S.O., Trebbien A.R., Handberg A.K., Therkildsen O.R., Madsen J.J., Thoru K., Baroch J.A., Deliberto T.J., Larsen L.E., Jorgensena P.H. Surveillance for avian influenza viruses in wild birds in Denmark and Greenland, 2007-10. Avian Dis. 2012, 56:992-998.
29. Ip H., Flint P., Franson J.C., Dusek R., Derksen D., Gill R., Ely C., Pearce J., Lanctot R., Matsuoka S., Irons D., Fischer J., Oates R., Petersen M., Fondell T., Rocque D., Pedersen J., Rothe T. Prevalence of influenza A viruses in wild migratory birds in Alaska: patterns of variation in detection at a crossroads of intercontinental flyways. Virol. J. 2008, 5:71.
30. Kawaoka Y., Chambers T.M., Sladen W.L., Webster R.G. Is the gene pool of influenza viruses in shorebirds and gulls different from that in wild ducks?. Virology 1988, 163:247-250.
31. Kawaoka Y., Cox N.J., Haller O., Hongo S., Kaverin N., Klenk H.-D., Lamb R.A., McCauley J., Palese P., Rimstad E., Webster R.G. Orthomyxoviridae. Virus Taxonomy: Eighth Report of the International Committee for the Taxonomy of Viruses 2005, 681-693. Elsevier Academic Press, San Diego, CA. C.M. Fauquet, M.A. Mayo, J. Maniloff, U. Desselberger, L.A. Ball (Eds.).
32. Kishida N., Sakoda Y., Shiromoto M., Bai G.-R., Isoda N., Takada A., Laver G., Kida H. H2N5 influenza virus isolates from terns in Australia: genetic reassortants between those of the Eurasian and American lineages. Virus Genes 2008, 37:16-21.
33. Koehler A.V., Pearce J.M., Flint P.L., Franson J.C., Ip H.C. Genetic evidence of intercontinental movement of avian influenza in a migratory bird: the northern pintail (Anas acuta). Mol. Ecol. 2008, 17:4754-4762.
34. Krauss S., Obert C.A., Franks J., Walker D., Jones K., Seiler P., Niles L., Pryor S.P., Obenauer J.C., Naeve C.W., Widjaja L., Webby R.J., Webster R.G. Influenza in migratory birds and evidence of limited intercontinental virus exchange. PLoS Pathog. 2007, 3:e167.
35. Lewis N.S., Javakhishvili Z., Russell C.A., Machablishvili A., Lexmond P., Verhagen J.H., Vuong O., Onashvili T., Donduashvili M., Smith D.J., Fouchier R.A.M. Avian influenza virus surveillance in wild birds in Georgia: 2009-2011. PLoS One 2013, 8:e58534.
36. Lindskog C., Ellstrom P., Olsen B., Ponten F., van Riel D., Munster V.J., Gonzalez-Acuna D., Kuiken T., Jourdain E. European H16N3 gull influenza virus attaches to the human respiratory tract and eye. PLoS One 2013, 8:e60757.
37. Liu J., Xiao H., Lei F., Zhu Q., Qin K., Zhang X.-w., Zhang X.-l., Zhao D., Wang G., Feng Y., Ma J., Liu W., Wang J., Gao G.F. Highly pathogenic H5N1 influenza virus infection in migratory birds. Science 2005, 309:1206.
38. Lomakina N.F., Gambaryan A.C., Boravleva E.Y., Kropotkina E.A., Kirillov I.M., Lavrient'ev M.V., Yamnikova S.S. Character of apathogenic influenza A viruses found in Moscow, Russia. Mol. Gen. Microbiol. Virol. 2009, 24:37-45.
39. Lu G., Rowley T., Garten R., Donis R.O. FluGenome: a web tool for genotyping influenza A virus. Nucleic Acids Res. 2007, 35:W275-W279.
40. Marchenko V.Y., Alekseev A.Y., Sharshov K.A., Petrov V.N., Silko N.Y., Susloparov I.M., Tserennorov D., Otgonbaatar D., Savchenko I.A., Shestopalov A.M. Ecology of influenza virus in wild bird populations in Central Asia. Avian Dis. 2012, 56:234-237.
41. Munster V.J., Baas C., Lexmond P., Waldenström J., Wallensten A., Fransson T., Rimmelzwaan G.F., Beyer W.E.P., Schutten M., Olsen B., Osterhaus A.D.M.E., Fouchier R.A.M. Spatial, temporal, and species variation in prevalence of influenza A viruses in wild migratory birds. PLoS Pathog. 2007, 3:e61.
42. Obenauer J.C., Denson J., Mehta P.K., Su X., Mukatira S., Finkelstein D.B., Xu X., Wang J., Ma J., Fan Y., Rakestraw K.M., Webster R.G., Hoffmann E., Krauss S., Zheng J., Zhang Z., Naeve C.W. Large-scale sequence analysis of avian influenza isolates. Science 2006, 311:1576-1580.
43. Olsen B., Munster V.J., Wallensten A., Waldenstrom J., Osterhaus A.D.M.E., Fouchier R.A.M. Global patterns of influenza A virus in wild birds. Science 2006, 312:384-388.
44. Olsen K.M., Larsson H. Gulls of North America, Europe, and Asia 2003, Princeton University Press, Princeton, NJ.
45. Pearce-Duvet J., Gauthier-Clerc M., Jourdain E., Boulinier T. Maternal antibody transfer in yellow-legged gulls. Emerg. Infect. Dis. 2009, 15:1147-1149.
46. Peiris J.S.M., de Jong M.D., Guan Y. Avian influenza virus (H5N1): a threat to human health. Clin. Microbiol. Rev. 2007, 20:243-267.
47. Phipps L.P., Essen S.C., Brown I.H. Genetic subtyping of influenza A viruses using RT-PCR with a single set of primers based on conserved sequences within the HA2 coding region. J. Virol. Methods 2004, 122:119-122.
48. Pyle P. Identification Guide to North American Birds, Part 2 2008, Slate Creek Press, Bolinas, CA.
49. Ramey A.M., Pearce J.M., Ely C.R., Guy L.M., Irons D.B., Derksen D.V., Ip H.S. Transmission and reassortment of avian influenza viruses at the Asian-North American interface. Virology 2010, 406:352-359.
50. Ramey A.M., Pearce J.M., Flint P.L., Ip H.S., Derksen D.V., Franson J.C., Petrula M.J., Scotton B.D., Sowl K.M., Wege M.L., Trust K.A. Intercontinental reassortment and genomic variation of low pathogenic avian influenza viruses isolated from northern pintails (Anas acuta) in Alaska: examining the evidence through space and time. Virology 2010, 401:179-189.
51. Reeves A.B., Pearce J.M., Ramey A.M., Meixell B.W., Runstadler J.A. Interspecies transmission and limited persistence of low pathogenic avian influenza genomes among Alaska dabbling ducks. Infect. Genet. Evol. 2011, 11:2004-2010.
52. Sivanandan V., Halvorson D.A., Laudert E., Senne D.A., Kumar M.C. Isolation of H13N2 influenza A virus from turkeys and surface water. Avian Dis. 1991, 35:974-977.
53. Sivay M.V., Sayfutdinova S.G., Sharshov K.A., Alekseev A.Y., Yurlov A.K., Runstadler J., Shestopalov A.M. Surveillance of influenza A virus in wild birds in the Asian portion of Russia in 2008. Avian Dis. 2012, 56:456-463.
54. Slemons R.D., Johnson D.C., Osborn J.S., Hayes F. Type-A influenza viruses isolated from wild free-flying ducks in California. Avian Dis. 1974, 18:119-124.
55. Spackman E., Senne D.A., Myers T.J., Bulaga L.L., Garber L.P., Perdue M.L., Lohman K., Daum L.T., Suarez D.L. Development of a real-time reverse transcriptase PCR assay for type A influenza virus and the avian H5 and H7 hemagglutinin subtypes. J. Clin. Microbiol. 2002, 40:3256-3260.
56. Spackman E., Stallknecht D.E., Slemons R.D., Winker K., Suarez D.L., Scott M., Swayne D.E. Phylogenetic analyses of type A influenza genes in natural reservoir species in North America reveals genetic variation. Virus Res. 2005, 114:89-100.
57. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 2011, 28:2731-2739.
58. Toennessen R., Germundsson A., Jonassen C.M., Haugen I., Berg K., Barrett R.T., Rimstad E. Virological and serological surveillance for type A influenza in the black-legged kittiwake (Rissa tridactyla). Virol. J. 2011, 8:21.
59. Tønnessen R., Kristoffersen A.B., Jonassen C.M., Hjortaas M.J., Hansen E.F., Rimstad E., Hauge A.G. Molecular and epidemiological characterization of avian influenza viruses from gulls and dabbling ducks in Norway. Virol. J. 2013, 10:112.
60. Tonnessen R., Valheim M., Rimstad E., Jonassen C.M., Germundssond A. Experimental inoculation of chickens with gull-derived low pathogenic avian influenza virus subtype H16N3 causes limited infection. Avian Dis. 2011, 55:680-685.
61. Van Borm S., Rosseel T., Vangeluwe D., Vandenbussche F., van den Berg T., Lambrecht B. Phylogeographic analysis of avian influenza viruses isolated from Charadriiformes in Belgium confirms intercontinental reassortment in gulls. Arch. Virol. 2012, 157:1509-1522.
62. Velarde R., Calvin S.E., Ojkic D., Barker I.K., Nagy E. Avian influenza virus H13 circulating in ring-billed gulls (Larus delawarensis) in southern Ontario, Canada. Avian Dis. 2010, 54:411-419.
63. Verhagen J.H., Majoor F., Lexmond P., Vuong O., Kasemir G., Lutterop D., Osterhaus A.D.M.E., Fouchier R.A.M., Kuiken T. Epidemiology of influenza A virus among Black-headed Gulls, the Netherlands, 2006-2010. Emerg. Infect. Dis 2014, 20:138-141.
64. Webster R.G., Bean W.J., Gorman O.T., Chambers T.M., Kawaoka Y. Evolution and ecology of influenza A viruses. Microbiol. Rev. 1992, 56:152-179.
65. Webster R.G., Peiris M., Chen H., Guan Y. H5N1 outbreaks and enzootic influenza. Emerg. Infect. Dis. 2006, 12:3-8.
66. Widjaja L., Krauss S.L., Webby R.J., Xie T., Webster R.G. Matrix gene of influenza A viruses isolated from wild aquatic birds: ecology and emergence of influenza A viruses. J. Virol. 2004, 78:8771-8779.
67. Wille M., Robertson G., Whitney H., Ojkic D., Lang A.S. Reassortment of American and Eurasian genes in an influenza A virus isolated from a great black-backed gull (Larus marinus), a species demonstrated to move between these regions. Arch. Virol. 2011, 156:107-115.
68. Wille M., Robertson G.J., Whitney H., Bishop M.A., Runstadler J.A., Lang A.S. Extensive geographic mosaicism in avian influenza viruses from gulls in the northern hemisphere. PLoS One 2011, 6:e20664.
69. Yamnikova S.S., Gambaryan A.S., Asistova V.A., Lvov D.K., Lomakina N.F., Munster V., Lexmond P., Fouchier R.A. A/H13 and A/H16 influenza viruses: different lines of one presursor (in Russian). Vopr. Virusol. 2009, 54:10-18.