Co-infection of influenza A viruses of swine contributes to effective shuffling of gene segments in a naturally reared pig

Virology

Volumn 484, Issue , 2015, Pages 203-212

  Abe, Haruka ^a   Mine, Junki ^a,b   Parchariyanon, Sujira ^c   Takemae, Nobuhiro ^a,b   Boonpornprasert, Prakit ^c   Ubonyaem, Namfon ^c   Patcharasinghawut, Phornnachat ^c   Nuansrichay, Bandit ^c   Tanikawa, Taichiro ^a,b   Tsunekuni, Ryota ^a,b   Saito, Takehiko ^a,b  

^a NATIONAL INSTITUTE OF ANIMAL HEALTH   (Japan)

^b Thailand Japan Zoonotic Diseases Collaborating Center (ZDCC)   (Thailand)

^c NATIONAL INSTITUTE OF ANIMAL HEALTH   (Thailand)

Author keywords

Bayesian MCMC; Co infection; IAV S; Surveillance; Swine influenza virus; Thailand

Indexed keywords

VIRUS HEMAGGLUTININ; VIRUS SIALIDASE;

ARTICLE; CONTROLLED STUDY; GENETIC REASSORTMENT; GENETIC VARIABILITY; GENOTYPE; HA GENE; INFLUENZA A; INFLUENZA A VIRUS (H1N1); INFLUENZA A VIRUS (H1N1-D); INFLUENZA A VIRUS (H1N2); INFLUENZA A VIRUS (H3N1); INFLUENZA A VIRUS (H3N2); INFLUENZA A VIRUS (H3N2-B); MIXED INFECTION; NA GENE; NONHUMAN; NOSE SMEAR; PHYLOGENY; PIG; PRIORITY JOURNAL; SWINE DISEASE; SWINE INFLUENZA VIRUS; THAILAND; VIRUS GENE; VIRUS GENOME; VIRUS IDENTIFICATION; VIRUS ISOLATION; VIRUS REPLICATION; VIRUS STRAIN; ANIMAL; GENETIC RECOMBINATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; INFLUENZA A VIRUS; ISOLATION AND PURIFICATION; NOSE MUCOSA; ORTHOMYXOVIRUS INFECTION; VETERINARY; VIROLOGY;

ANIMALS; COINFECTION; INFLUENZA A VIRUS; NASAL MUCOSA; ORTHOMYXOVIRIDAE INFECTIONS; REASSORTANT VIRUSES; RECOMBINATION, GENETIC; SWINE; THAILAND;

EID: 84955504344     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2015.06.002     Document Type: Article

References (46)

1. Brown, I.H., 2013. History and epidemiology of Swine influenza in Europe. Curr. Top. Microbiol. Immunol. 370, 133-146.
2. Charoenvisal, N., Keawcharoen, J., Sreta, D., Chaiyawong, S., Nonthabenjawan, N., Tantawet, S., Jittimanee, S., Arunorat, J., Amonsin, A., Thanawongnuwech, R., 2013. Genetic characterization of Thai swine influenza viruses after the introduction of pandemic H1N1 2009. Virus Genes 47, 75-85.
3. Choi, Y.K., Nguyen, T.D., Ozaki, H., Webby, R.J., Puthavathana, P., Buranathal, C., Chaisingh, A., Auewarakul, P., Hanh, N.T., Ma, S.K., Hui, P.Y., Guan, Y., Peiris, J.S., Webster, R.G., 2005. Studies of H5N1 influenza virus infection of pigs by using viruses isolated in Vietnam and Thailand in 2004. J. Virol. 79, 10821-10825.
4. Chou, Y., Albrecht, R.A., Pica, N., Lowen, A.C., Richt, J.A., García-Sastre, A., Palese, P., Hai, R., 2011. The M segment of the 2009 new pandemic H1N1 influenza virus is critical for its high transmission efficiency in the guinea pig model. J. Virol. 85, 11235-11241.
5. Cong, Y., Wang, G., Guan, Z., Chang, S., Zhang, Q., Yang, G., Wang, W., Meng, Q., Ren, W., Wang, C., Ding, Z., 2010. Reassortant between human-like H3N2 and avian H5 subtype influenza A viruses in pigs: a potential public health risk. PLoS One 5, e12591.
6. Drummond, A.J., Suchard, M.A., Xie, D., Rambaut, A., 2012. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol. Biol. Evol. 29, 1969-1973.
7. Fan, X., Zhu, H., Zhou, B., Smith, D.K., Chen, X., Lam, T.T.-Y., Poon, L.L.M., Peiris, M., Guan, Y., 2012. Emergence and dissemination of a swine H3N2 reassortant influenza virus with 2009 pandemic H1N1 genes in pigs in China. J. Virol. 86, 2375-2378.
8. Freidl, G.S., Meijer, A., de Bruin, E., de Nardi, M., Munoz, O., Capua, I., Breed, A.C., Harris, K., Hill, A., Kosmider, R., Banks, J., von Dobschuetz, S., Stark, K., Wieland, B., Stevens, K., van der Werf, S., Enouf, V., van der Meulen, K., Van Reeth, K., Dauphin, G., Koopmans, M., 2014. Influenza at the animal-human interface: a review of the literature for virological evidence of human infection with swine or avian influenza viruses other than A(H5N1). FLURISK Consortium. Euro Surveill. (19), 20793.
9. Garten, R.J., Davis, C.T., Russell, C.A., Shu, B., Lindstrom, S., Balish, A., Sessions, W.M., Xu, X., Skepner, E., Deyde, V., Okomo-Adhiambo, M., Gubareva, L., Barnes, J., Smith, C.B., Emery, S.L., Hillman, M.J., Rivailler, P., Smagala, J., de Graaf, M., Burke, D.F., Fouchier, R.A., Pappas, C., Alpuche-Aranda, C.M., López-Gatell, H., Olivera, H., López, I., Myers, C.A., Faix, D., Blair, P.J., Yu, C., Keene, K.M., Dotson Jr., P.D., Boxrud, D., Sambol, A.R., Abid, S.H., George, K. St., Bannerman, T., Moore, A. L., Stringer, D.J., Blevins, P., Demmler-Harrison, G.J., Ginsberg, M., Kriner, P., Waterman, S., Smole, S., Guevara, H.F., Belongia, E.A., Clark, P.A., Beatrice, S.T., Donis, R., Katz, J., Finelli, L., Bridges, C.B., Shaw, M., Jernigan, D.B., Uyeki, T.M., Smith, D.J., Klimov, A.I., Cox, N.J., 2009. Antigenic and genetic characteristics of swine-origin 2009A(H1N1) influenza viruses circulating in humans. Science, 325;, pp. 197-201.
10. Ghedin, E., Fitch, A., Boyne, A., Griesemer, S., DePasse, J., Bera, J., Zhang, X., Halpin, R.A., Smit, M., Jennings, L., St. George, K., Holmes, E.C., Spiro, D.J., 2009. Mixedinfection and the genesis of influenza virus diversity. J. Virol. 83, 8832-8841.
11. Hall, T.A., 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl. Acids Symp. Ser. 41, 95-98.
12. Hiromoto, Y., Parchariyanon, S., Ketusing, N., Netrabukkana, P., Hayashi, T., Kobayashi, T., Takemae, N., Saito, T., 2012. Isolation of the pandemic (H1N1) 2009 virus and its reassortant with an H3N2 swine influenza virus from healthy weaning pigs in Thailand in 2011. Virus Res. 169, 175-181.
13. Howard, W.A., Essen, S.C., Strugnell, B.W., Russell, C., Barass, L., Reid, S.M., Brown, I.H., 2011. Reassortant Pandemic (H1N1) 2009 virus in pigs, United Kingdom. Emerg. Infect.Dis. 17, 1049-1052.
14. Ito, T., Couceiro, J.N., Kelm, S., Baum, L.G., Krauss, S., Castrucci, M.R., Donatelli, I., Kida, H., Paulson, J.C., Webster, R.G., Kawaoka, Y., 1998. Molecular basis for the generation in pigs of influenza A viruses with pandemic potential. J. Virol. 72, 7367-7373.
15. Karasin, A.I., West, K., Carman, S., Olsen, C.W., 2004. Characterization of avian H3N3 and H1N1 influenza A viruses isolated from pigs in Canada. J. Clin. Microbiol. 42, 4349-4354.
16. Kida, H., Ito, T., Yasuda, J., Shimizu, Y., Itakura, C., Shortridge, K.F., Kawaoka, Y., Webster, R.G., 1994. Potential for transmission of avian influenza viruses to pigs. J. Gen. Virol. 75, 2183-2188.
17. Kitikoon, P., Sreta, D., Na Ayudhya, S.N., Wongphatcharachai, M., Lapkuntod, J., Prakairungnamthip, D., Bunpapong, N., Suradhat, S., Thanawongnuwech, R., Amonsin, A., 2011. Brief report: molecular characterization of a novel reassorted pandemic H1N1 2009 in Thai pigs. Virus Genes 43, 1-5.
18. Lakdawala, S.S., Lamirande, E.W., Suguitan Jr., A.L., Wang, W., Santos, C.P., Vogel, L., Matsuoka, Y., Lindsley, W.G., Jin, H., Subbarao, K., 2011. Eurasian-origin gene segments contribute to the transmissibility, aerosol release, and morphology of the 2009 pandemic H1N1 influenza virus. PLoS Pathog. 7, e1002443.
19. Lam, T.T., Zhu, H., Wang, J., Smith, D.K., Holmes, E.C., Webster, R.G., Webby, R., Peiris, J.M., Guan, Y., 2011. Reassortment events among swine influenza A viruses in China: implications for the origin of the 2009 influenza pandemic. J. Virol. 85, 10279-10285.
20. Lee, C.S., Kang, B.K., Kim, H.K., Park, S.J., Park, B.K., Jung, K., Song, D.S., 2008. Phylogenetic analysis of swine influenza viruses recently isolated in Korea. Virus Genes 37, 168-176.
21. Lindstrom, S., Garten, R., Balish, A., Shu, B., Emery, S., Berman, L., Barnes, N., Sleeman, K., Gubareva, L., Villanueva, J., Klimov, A., 2012. Human infections with novel reassortant influenza A(H3N2)v viruses, United States, 2011. Emerg. Infect. Dis. 18, 834-837.
22. Liu, W., Li, Z.D., Tang, F., Wei, M.T., Tong, Y.G., Zhang, L., Xin, Z.T., Ma, M.J., Zhang, X.A., Liu, L.J., Zhan, L., He, C., Yang, H., Boucher, C.A., Richardus, J.H., Cao, W.C., 2010. Mixed infections of pandemic H1N1 and seasonal H3N2 viruses in 1 outbreak. Clin. Infect. Dis. 50, 1359-1365.
23. Manzoor, R., Sakoda, Y., Nomura, N., Tsuda, Y., Ozaki, H., Okamatsu, M., Kida, H., 2009. PB2 protein of a highly pathogenic avian influenza virus strain A/chicken/Yamaguchi/7/2004 (H5N1) determines its replication potential in pigs. J. Virol. 83, 1572-1578.
24. Murcia, P.R., Hughes, J., Battista, P., Lloyd, L., Baillie, G.J., Ramirez-Gonzalez, R.H., Ormond, D., Oliver, K., Elton, D., Mumford, J.A., Caccamo, M., Kellam, P., Grenfell, B.T., Holmes, E.C., Wood, J.L.N., 2012. Evolution of an Eurasian avian-like influenza virus in naive and vaccinated pigs. PLoS Pathog. 8, e1002730.
25. Myers, K.P., Olsen, C.W., Gray, G.C., 2007. Cases of swine influenza in humans: a review of the literature. Clin. Infect. Dis. 44, 1084-1088.
26. Ngo, L.T., Hiromoto, Y., Pham, V.P., Le, H.T., Nguyen, H.T., Le, V.T., Takemae, N., Saito, T, 2012. Isolation of novel triple-reassortant swine H3N2 influenza viruses possessing the hemagglutinin and neuraminidase genes of a seasonal influenza virus in Vietnam in 2010. Influenza Other Respir. Viruses 6, 6-10.
27. Pappas, C., Aguilar, P.V., Basler, C.F., Solorzano, A., Zeng, H., Perrone, L.A., Palese, P., Garcia-Sastre, A., Katz, J.M., Tumpey, T.M., 2008. Single gene reassortants identify a critical role for PB1, HA, and NA in the high virulence of the 1918 pandemic influenza virus. Proc. Natl. Acad. Sci. U.S.A. 105, 3064-3069.
28. Peacey, M., Hall, R.J., Sonnberg, S., Ducatez, M., Paine, S., Nicol, M., Ralston, J.C., Bandaranayake, D., Hope, V., Webby, R.J., Huang, S., 2010. Pandemic (H1N1) 2009 and seasonal influenza A (H1N1) co-infection, New Zealand, 2009. Emerg. Infect. Dis. 16, 1618-1620.
29. Peiris, J.S.M., Guan, Y., Markwell, D., Ghose, P., Webster, R.G., Shortridge, K.F., 2001. Cocirculation of avian H9N2 and contemporary"human" H3N2 influenza A viruses in pigs in southeastern China: potential for genetic reassortment? J. Virol. 75, 9679-9686.
30. Poonsuk, S., Sangthong, P., Petcharat, N., Lekcharoensuk, P., 2013. Genesis and genetic constellations of swine influenza viruses in Thailand. Vet. Microbiol. 167, 314-326.
31. Salomon, R., Webster, R.G., 2009. The influenza virus enigma. Cell 136, 402-410.
32. Scholtissek, C., Bürger, H., Bachmann, P.A., Hannoun, C., 1983. Genetic relatedness of hemagglutinins of the H1 subtype of influenza A viruses isolated from swine and birds. Virology 129, 521-523.
33. Scholtissek, C., 1990-1991. Pigs as 'mixing vessels' for the creation of new pandemic influenza. A viruses Med. Princ. Pract. 2, 65-71.
34. Smith, G.J., Vijaykrishna, D., Bahl, J., Lycett, S.J., Worobey, M., Pybus, O.G., Ma, S.K., Cheung, C.L., Raghwani, J., Bhatt, S., Peiris, J.S., Guan, Y., Rambaut, A., 2009. Origins and evolutionary genomics of the 2009 swine-origin H1N1 influenza A epidemic. Nature 459, 1122-1125.
35. Takemae, N., Parchariyanon, S., Damrongwatanapokin, S., Uchida, Y., Ruttanapumma, R., Watanabe, C., Yamaguchi, S., Saito, T., 2008. Genetic diversity of swine influenza viruses isolated from pigs during 2000-2005 in Thailand. Influenza Other Respir. Viruses 2, 181-189.
36. Takemae, N., Parchariyanon, S., Ruttanapumma, R., Hiromoto, Y., Hayashi, T., Uchida, Y., Saito, T., 2011. Swine influenza virus infection in different age groups of pigs in farrow-to-finish farms in Thailand. Virol. J. 8, 537.
37. Thrusfield, M., 1995. Veterinary Epidemiology. 2. Blackwell Science Ltd., Oxford.
38. Tian, S.F., Buckler-White, A.J., London, W.T., Reck, L.J., Chanock, R.M., Murphy, B.R., 1985. 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. 53, 771-775.
39. Tobita, K., Sugiura, A., Enomoto, C., Furuyama, M., 1975. Plaque assay and primary isolation of influenza A viruses in an established line of canine kidney cells (MDCK) in the presence of trypsin. Med. Microbiol. Immunol. 162, 9-14.
40. Vijaykrishna, D., Poon, L.L.M., Zhu, H.C., Ma, S.K., Li, O.T.W., Cheung, C.L., Smith, G.J. D., Peiris, J.S.M., Guan, Y., 2010. Reassortment of pandemic H1N1/2009 influenza A virus in swine. Science 328, 1529.
41. Vijaykrishna, D., Smith, G.J., Pybus, O.G., Zhu, H., Bhatt, S., Poon, L.L., Riley, S., Bahl, J., Ma, S.K., Cheung, C.L., Perera, R.A., Chen, H., Shortridge, K.F., Webby, R.J., Webster, R.G., Guan, Y., Peiris, J.S., 2011. Long-term evolution and transmission dynamics of swine influenza A virus. Nature 473, 519-522.
42. Vincent, A.L., Ma, W., Lager, K.M., Janke, B.H., Richt, J.A., 2008. Swine influenza viruses: a North American perspective. Adv. Virus Res. 72, 127-154.
43. Vincent, A., Awada, L., Brown, I., Chen, H., Claes, F., Dauphin, G., Donis, R., Culhane, M., Hamilton, K., Lewis, N., Mumford, E., Nguyen, T., Parchariyanon, S., Pasick, J., Pavade, G., Pereda, A., Peiris, M., Saito, T., Swenson, S., Van Reeth, K., Webby, R., Wong, F., Ciacci-Zanella, J., 2013. Review of influenza A virus in swine worldwide: a call for increased surveillance and research. Zoonoses Public Health, 61;, pp. 4-17.
44. Webster, R.G., Bean, W.J., Gorman, O.T., Chambers, T.M., Kawaoka, Y., 1992. Evolution and ecology of influenza A viruses. Microbiol. Rev. 56, 152-179.
45. Zhu, H., Zhou, B., Fan, X., Lam, T.T., Wang, J., Chen, A., Chen, X., Chen, H., Webster, R.G., Webby, R., Peiris, J.S., Smith, D.K., Guan, Y., 2011. NovelreassortmentofEurasian avian-like and pandemic/2009 influenza viruses in swine: infectious potential for humans. J. Virol. 85, 10432-10439.
46. Zhou, N.N., Senne, D.A., Landgraf, J.S., Swenson, S.L., Erickson, G., Rossow, K., Liu, L., Yoon, K-j., Krauss, S., Webster, R.G., 1999. Genetic reassortment of avian, swine, and human influenza A viruses in American pigs. J. Virol. 73, 8851-8856.