Genetic Analysis of Avian Influenza Viruses: Cocirculation of Avian Influenza Viruses with Allele A and B Nonstructural Gene in Northern Pintail (Anas acuta) Ducks Wintering in Japan
The pandemic influenza virus strains of 1918 (H1N1), 1957 (H2N2), 1968 (H3N2), and 2009 (H1N1) have genes related to avian influenza viruses (AIVs). The nonstructural (NS) gene of AIVs plays a significant role in host-viral interaction. However, little is known about the degree of diversity of this gene in Northern pintail (Anas acuta) ducks wintering in Japan. This study describes characteristics of pintail-originated H1N1, H1N2, H1N3, H5N2, H5N3, H5N9, and H7N7 viruses. Most of the viruses were revealed to be avian strains and not related to pandemic and seasonal flu strains. Nevertheless, the NP genes of 62.5% (5/8) viruses were found closely related to a A/swine/Korea/C12/08, indicating exchange of genetic material and ongoing mammalian-linked evolution of AIVs. Besides, all the viruses, except Aomori/422/07 H1N1, contain PSIQSR*GLF motif usually found in avian, porcine, and human H1 strains. The Aomori/422/07 H1N1 has a PSVQSR*GLF motif identical to a North American strain. This findings linked to an important intercontinental, Asian-American biogeographical interface. Phylogenetically all the viruses were clustered in Eurasian lineage. Cocirculation of allele A and B (NS gene) viruses was evident in the study implying the existence of a wide reservoir of influenza A viruses in pintail wintering in Japan. 1. Introduction Influenza A virus infections in birds account for important inputs into the evolutionary porcine-human complex of this prominent anthropozoonotic pathogen. Among influenza A viruses, which broadly exhibit 17 HA and 9 NA antigenic subtypes, only three haemagglutinin (HA) subtypes (H1, H2, and H3) and two neuraminidase (NA) subtypes (N1 and N2) have circulated widely in swine and human populations since the 20th century [1]. Viruses from waterfowl reassorted with existing human and/or porcine influenza viruses to generate the 1957, 1968 [2], and 2009 (Novel swine-origin influenza A (H1N1) virus investigation team, 2009) pandemic influenza viruses and may expectably play a similar role in the creation of future pandemic viruses. In addition, on multiple occasions, it has been evident that avian influenza viruses (AIVs), chiefly the subtypes H5N1, H7N7, and H9N2, directly transmitted from birds to humans [3, 4]. Avian-originated H1N1, H3N2, H5N1, and H9N2 viruses have been recovered from pigs in Asia, Europe, and Canada [5–7]. Furthermore, H2N3 avian virus reassortants were isolated from pigs in the United States [8]. Pigs have been postulated, hence, to be the ultimate “mixing vessels” for mammalian influenza viruses and AIVs and can
References
[1]
L. Campitelli, C. Fabiani, S. Puzelli et al., “H3N2 influenza viruses from domestic chickens in Italy: an increasing role for chickens in the ecology of influenza?” Journal of General Virology, vol. 83, no. 2, pp. 413–420, 2002.
[2]
Y. Kawaoka, S. Krauss, and R. G. Webster, “Avian-to-human transmission of the PB1 gene of influenza A viruses in the 1957 and 1968 pandemics,” Journal of Virology, vol. 63, no. 11, pp. 4603–4608, 1989.
[3]
E. C. J. Claas, A. D. M. E. Osterhaus, R. Van Beek et al., “Human influenza A H5N1 virus related to a highly pathogenic avian influenza virus,” Lancet, vol. 351, no. 9101, pp. 472–477, 1998.
[4]
Y. P. Lin, M. Shaw, V. Gregory et al., “Avian-to-human transmission of H9N2 subtype influenza A viruses: relationship between H9N2 and H5N1 human isolates,” Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 17, pp. 9654–9658, 2000.
[5]
Y. Guan, K. F. Shortridge, S. Krauss, P. H. Li, Y. Kawaoka, and R. G. Webster, “Emergence of avian H1N1 influenza viruses in pigs in China,” Journal of Virology, vol. 70, no. 11, pp. 8041–8046, 1996.
[6]
A. I. Karasin, K. West, S. Carman, and C. W. Olsen, “Characterization of avian H3N3 and H1N1 influenza A viruses isolated from pigs in Canada,” Journal of Clinical Microbiology, vol. 42, no. 9, pp. 4349–4354, 2004.
[7]
J. S. M. Peiris, Y. Guan, D. Markwell, P. Ghose, R. G. Webster, and K. F. Shortridge, “Cocirculation of avian H9N2 and contemporary “human” H3N2 influenza A viruses in pigs in southeastern China: potential for genetic reassortment?” Journal of Virology, vol. 75, no. 20, pp. 9679–9686, 2001.
[8]
W. Ma, A. L. Vincent, M. R. Gramer et al., “Identification of H2N3 influenza A viruses from swine in the United States,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 52, pp. 20949–20954, 2007.
[9]
D. Shoham, “The modes of evolutionary emergence of primal and late pandemic influenza virus strains from viral reservoir in animals: an interdisciplinary analysis,” Influenza Research and Treatment, vol. 2011, Article ID 861792, 27 pages, 2011.
[10]
S. Tong, Y. Li, P. Rivailler, et al., “A distinct lineage of influenza A virus from bats,” Proceedings of the National Academy of Sciences of the United States of America, vol. 109, pp. 4269–4274, 2012.
[11]
Y. Kawaoka and R. G. Webster, “Sequence requirements for cleavage activation of influenza virus hemagglutinin expressed in mammalian cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 85, no. 2, pp. 324–328, 1988.
[12]
H. Hatta, P. Gao, P. Halfmann, and Y. Kawaoka, “Molecular basis for high virulence of Hong Kong H5N1 influenza a viruses,” Science, vol. 293, no. 5536, pp. 1840–1842, 2001.
[13]
Z. Li, H. Chen, P. Jiao et al., “Molecular basis of replication of duck H5N1 influenza viruses in a mammalian mouse model,” Journal of Virology, vol. 79, no. 18, pp. 12058–12064, 2005.
[14]
Z. Li, Y. Jiang, P. Jiao et al., “The NS1 gene contributes to the virulence of H5N1 avian influenza viruses,” Journal of Virology, vol. 80, no. 22, pp. 11115–11123, 2006.
[15]
D. L. Noah, K. Y. Twu, and R. M. Krug, “Cellular antiviral responses against influenza A virus are countered at the posttranscriptional level by the viral NS1A protein via its binding to a cellular protein required for the end processing of cellular pre-mRNAS,” Virology, vol. 307, no. 2, pp. 386–395, 2003.
[16]
S. H. Seo, E. Hoffmann, and R. G. Webster, “Lethal H5N1 influenza viruses escape host anti-viral cytokine responses,” Nature Medicine, vol. 8, no. 9, pp. 950–954, 2002.
[17]
A. Jahangir, Y. Watanabe, O. Chinen et al., “Surveillance of avian influenza viruses in Northern pintails (Anas acuta) in Tohoku District, Japan,” Avian Diseases, vol. 52, no. 1, pp. 49–53, 2008.
[18]
A. Jahangir, S. Ruenphet, S. Ueda et al., “Avian influenza and Newcastle disease viruses from northern pintail in Japan: isolation, characterization and inter-annual comparisons during 2006–2008,” Virus Research, vol. 143, no. 1, pp. 44–52, 2009.
[19]
A. Jahangir, S. Ruenphet, D. Shoham, M. Okamura, M. Nakamaura, and K. Takehara, “Haemagglutinin and neuraminidase characterization of low pathogenic H5 and H7 avian influenza viruses isolated from Northern pintails (Anas acuta) in Japan, with special reference to genomic and biogeographical aspects,” Virus Genes, vol. 40, no. 1, pp. 94–105, 2010.
[20]
E. Hoffmann, J. Stech, Y. Guan, R. G. Webster, and D. R. Perez, “Universal primer set for the full-length amplification of all influenza A viruses,” Archives of Virology, vol. 146, no. 12, pp. 2275–2289, 2001.
[21]
K. Tamura, J. Dudley, M. Nei, and S. Kumar, “MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0,” Molecular Biology and Evolution, vol. 24, no. 8, pp. 1596–1599, 2007.
[22]
S. Liu, K. Ji, J. Chen et al., “Panorama phylogenetic diversity and distribution of type A influenza virus,” PLoS ONE, vol. 4, no. 3, Article ID e5022, 2009.
[23]
S. Ludwig, U. Schultz, J. Mandler, W. M. Fitch, and C. Scholtissek, “Phylogenetic relationship of the nonstructural (NS) genes of influenza A viruses,” Virology, vol. 183, no. 2, pp. 566–577, 1991.
[24]
S. Zohari, P. Gyarmati, P. Thorén et al., “Genetic characterization of the NS gene indicates co-circulation of two sub-lineages of highly pathogenic avian influenza virus of H5N1 subtype in Northern Europe in 2006,” Virus Genes, vol. 36, no. 1, pp. 117–125, 2008.
[25]
Y. Li, Z. Lin, J. Shi et al., “Detection of Hong Kong 97-like H5N1 influenza viruses from eggs of Vietnamese waterfowl,” Archives of Virology, vol. 151, no. 8, pp. 1615–1624, 2006.
[26]
A. Jahangir, S. Ruenphet, D. Shoham, M. Okamura, M. Nakamaura, and K. Takehara, “Phenotypic, genetic, and phylogeographical characterization of avian influenza virus subtype H5N2 isolated from northern pintail (Anas acuta) in Japan,” Virus Research, vol. 145, no. 2, pp. 329–333, 2009.
[27]
Y. Kawaoka, O. T. Gorman, T. Ito et al., “Influence of host species on the evolution of the nonstructural (NS) gene of influenza A viruses,” Virus Research, vol. 55, no. 2, pp. 143–156, 1998.
[28]
R. Chen and E. C. Holmes, “Avian influenza virus exhibits rapid evolutionary dynamics,” Molecular Biology and Evolution, vol. 23, pp. 2336–2341, 2006.
[29]
L. Duan, L. Campitelli, X. H. Fan et al., “Characterization of low-pathogenic H5 subtype influenza viruses from Eurasia: implications for the origin of highly pathogenic H5N1 viruses,” Journal of Virology, vol. 81, no. 14, pp. 7529–7539, 2007.
[30]
D. Shoham, “Biotic-abiotic mechanisms for long-term preservation and reemergence of influenza type A virus genes,” Progress in Medical Virology, vol. 40, pp. 178–192, 1993.
[31]
S. Zohari, P. Gyarmati, A. Ejdersund, et al., “Phylogenetic analysis of the non-structural (NS) gene of influenza A viruses isolated from mallards in Northern Europe in 2005,” Virology Journal, vol. 5, article 147, 2008.
[32]
E. Spackman, D. E. Stallknecht, R. D. Slemons et al., “Phylogenetic analyses of type A influenza genes in natural reservoir species in North America reveals genetic variation,” Virus Research, vol. 114, no. 1-2, pp. 89–100, 2005.
[33]
Yamashina Institute for Ornithology, Japanese Bird Banding in Recent Years (1961–1985), Bird Migration Research Center, Abiko, Chiba, Japan, 1985.
[34]
V. V. Bianki and I. N. Dobrynina, Migrations of Birds in Eastern Europe and Northern Asia, Nauka Press, Moscow, Russia, 1997.
[35]
Yamashina Institute for Ornithology, Japanese Bird Banding in Recent Years (1961–2004), Bird Migration Research Center, Abiko, Chiba, Japan, 2004.
[36]
C. A. Nicolai, P. L. Flint, and M. L. Wege, “Annual survival and site fidelity of northern pintails banded on the Yukon-Kuskokwim Delta, Alaska,” Journal of Wildlife Management, vol. 69, no. 3, pp. 1202–1210, 2005.
[37]
M. R. Miller, J. Y. Takekawa, J. P. Fleskes, D. L. Orthmeyer, M. L. Casazza, and W. M. Perry, “Spring migration of Northern Pintails from California's Central Valley wintering area tracked with satellite telemetry: routes, timing, and destinations,” Canadian Journal of Zoology, vol. 83, no. 10, pp. 1314–1332, 2005.
[38]
J. Wahlgren, J. Waldenstr?m, S. Sahlin et al., “Gene segment reassortment between American and asian lineages of avian influenza virus from waterfowl in the Beringia area,” Vector-Borne and Zoonotic Diseases, vol. 8, no. 6, pp. 783–790, 2008.
[39]
L. Campitelli, A. Di Martino, D. Spagnolo et al., “Molecular analysis of avian H7 influenza viruses circulating in Eurasia in 1999–2005: detection of multiple reassortant virus genotypes,” Journal of General Virology, vol. 89, no. 1, pp. 48–59, 2008.
[40]
M. D. De Jong, T. T. Thanh, T. H. Khanh et al., “Oseltamivir resistance during treatment of influenza A (H5N1) infection,” New England Journal of Medicine, vol. 353, no. 25, pp. 2667–2672, 2005.
[41]
P. M. Colman, P. A. Hoyne, and M. C. Lawrence, “Sequence and structure alignment of paramyxovirus hemagglutinin- neuraminidase with influenza virus neuraminidase,” Journal of Virology, vol. 67, no. 6, pp. 2972–2980, 1993.
[42]
P. Ward, I. Small, J. Smith, P. Suter, and R. Dutkowski, “Oseltamivir (Tamiflu) and its potential for use in the event of an influenza pandemic,” Journal of Antimicrobial Chemotherapy, vol. 55, no. 1, pp. i5–i21, 2005.
[43]
Q. Zhu, H. Yang, W. Chen et al., “A naturally occurring deletion in its NS gene contributes to the attenuation of an H5N1 swine influenza virus in chickens,” Journal of Virology, vol. 82, no. 1, pp. 220–228, 2008.
[44]
J. C. Obenauar, J. Denson, P. K. Mehta et al., “Large-scale sequence analysis of avian influenza isolates,” Science, vol. 311, no. 5767, pp. 1576–1580, 2006.