期刊论文详细信息
Virology Journal
Host shifts and molecular evolution of H7 avian influenza virus hemagglutinin
David E Stallknecht1  Camille Lebarbenchon1 
[1] Southeastern Cooperative Wildlife Disease Study, Department of Population Health, College of Veterinary Medicine, The University of Georgia, Athens, Georgia 30602, USA
关键词: parallel evolution;    receptor binding domain;    virulence;    adaptation;    poultry;    duck;    Influenza A;   
Others  :  1156487
DOI  :  10.1186/1743-422X-8-328
 received in 2011-04-26, accepted in 2011-06-28,  发布年份 2011
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【 摘 要 】

Evolutionary consequences of host shifts represent a challenge to identify the mechanisms involved in the emergence of influenza A (IA) viruses. In this study we focused on the evolutionary history of H7 IA virus in wild and domestic birds, with a particular emphasis on host shifts consequences on the molecular evolution of the hemagglutinin (HA) gene. Based on a dataset of 414 HA nucleotide sequences, we performed an extensive phylogeographic analysis in order to identify the overall genetic structure of H7 IA viruses. We then identified host shift events and investigated viral population dynamics in wild and domestic birds, independently. Finally, we estimated changes in nucleotide substitution rates and tested for positive selection in the HA gene. A strong association between the geographic origin and the genetic structure was observed, with four main clades including viruses isolated in North America, South America, Australia and Eurasia-Africa. We identified ten potential events of virus introduction from wild to domestic birds, but little evidence for spillover of viruses from poultry to wild waterbirds. Several sites involved in host specificity (addition of a glycosylation site in the receptor binding domain) and virulence (insertion of amino acids in the cleavage site) were found to be positively selected in HA nucleotide sequences, in genetically unrelated lineages, suggesting parallel evolution for the HA gene of IA viruses in domestic birds. These results highlight that evolutionary consequences of bird host shifts would need to be further studied to understand the ecological and molecular mechanisms involved in the emergence of domestic bird-adapted viruses.

【 授权许可】

   
2011 Lebarbenchon and Stallknecht; licensee BioMed Central Ltd.

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【 参考文献 】
  • [1]Palumbi SR: Humans as the world's greatest evolutionary force. Science 2001, 293:1786-1790.
  • [2]Lebarbenchon C, Brown SP, Poulin R, Gauthier-Clerc M, Thomas F: Evolution of pathogens in a man-made world. Mol Ecol 2008, 17:475-484.
  • [3]Barrett R, Kuzawa C, McDade T, Armelagos G: Emerging and re-emerging infectious diseases: the third epidemiological transition. Annu Rev Anthropol 1998, 27:247-271.
  • [4]Mennerat A, Nilsen F, Ebert D, Skorping A: Intensive farming: evolutionary implications for parasites and pathogens. Evol Biol 2010, 37:59-67.
  • [5]Gilbert M, Xiao X, Pfeiffer DU, Epprecht M, Boles S, Czarnecki C, Chaitaweesub P, Kalpravidh W, Minh PQ, Otte MJ, Martin V, Slingenbergh J: Mapping H5N1 highly pathogenic avian influenza risk in Southeast Asia. Proc Natl Acad Sci USA 2008, 105:4769-4774.
  • [6]Woo PC, Lau SK, Yuen K: Infectious diseases emerging from Chinese wet-markets: zoonotic origins of severe respiratory viral infections. Curr Opin Infect Dis 2006, 19:401-407.
  • [7]Leibler JH, Otte J, Roland-Holst D, Pfeiffer DU, Soares Magalhaes R, Rushton J, Graham JP, Silbergeld EK: Industrial food animal production and global health risks: exploring the ecosystems and economics of avian influenza. Ecohealth 2009, 6:58-70.
  • [8]Harder TC, Teuffert J, Starick E, Gethmann J, Grund C, Fereidouni S, Durban M, Bogner KH, Neubauer-Juric A, Repper R, Hlinak A, Engelhardt A, Nöckler A, Smietanka K, Minta Z, Kramer M, Globig A, Mettenleiter TC, Conraths FJ, Beer M: Highly pathogenic avian influenza virus (H5N1) in frozen duck carcasses, Germany, 2007. Emerg Infect Dis 2009, 15:272-279.
  • [9]Hogerwerf L, Wallace RG, Ottaviani D, Slingenbergh J, Prosser D, Bergmann L, Gilbert M: Persistence of Highly Pathogenic Avian Influenza H5N1 Virus Defined by Agro-Ecological Niche. Ecohealth 2010, 7:213-225.
  • [10]Peiris JSM, de Jong MD, Guan Y: Avian influenza virus (H5N1): a threat to human health. Clin Microbiol Rev 2007, 20:243-267.
  • [11]Garten RJ, Davis CT, Russell CA, Shu B, Lindstrom S, Balish A, Sessions WM, Xu X, Skepner E, Deyde V, Okomo-Adhiambo M, Gubareva L, Barnes J, Smith CB, Emery SL, Hillman MJ, Rivailler P, Smagala J, de Graaf M, Burke DF, Fouchier RAM, Pappas C, Alpuche-Aranda CM, López-Gatell H, Olivera H, López I, Myers CA, Faix D, Blair PJ, Yu C, et al.: Antigenic and genetic characteristics of swine-origin 2009 A(H1N1) influenza viruses circulating in humans. Science 2009, 325:197-201.
  • [12]Smith GJD, Vijaykrishna D, Bahl J, Lycett SJ, Worobey M, Pybus OG, Ma SK, Cheung CL, Raghwani J, Bhatt S, Peiris JSM, Guan Y, Rambaut A: Origins and evolutionary genomics of the 2009 swine-origin H1N1 influenza A epidemic. Nature 2009, 459:1122-1125.
  • [13]Holmes EC: Evolution in health and medicine Sackler colloquium: The comparative genomics of viral emergence. Proc Natl Acad Sci USA 2010, 107(S1):1742-1746.
  • [14]Olsen B, Munster VJ, Wallensten A, Waldenström J, Osterhaus ADME, Fouchier RAM: Global patterns of influenza a virus in wild birds. Science 2006, 312:384-388.
  • [15]van Gils JA, Munster VJ, Radersma R, Liefhebber D, Fouchier RAM, Klaassen M: Hampered foraging and migratory performance in swans infected with low-pathogenic avian influenza A virus. PLoS ONE 2007, 2:e184.
  • [16]Latorre-Margalef N, Gunnarsson G, Munster VJ, Fouchier RAM, Osterhaus ADME, Elmberg J, Olsen B, Wallensten A, Haemig PD, Fransson T, Brudin L, Waldenström J: Effects of influenza A virus infection on migrating mallard ducks. P Roy Soc B-Biol Sci 2009, 276:1029-1036.
  • [17]Swayne DE, Suarez DL: Highly pathogenic avian influenza. Rev Sci Tech 2000, 19:463-482.
  • [18]Alexander DJ: An overview of the epidemiology of avian influenza. Vaccine 2007, 25:5637-5644.
  • [19]Becker WB: The isolation and classification of Tern virus: influenza A-Tern South Africa--1961. J Hyg 1966, 64:309-320.
  • [20]Gaidet N, Cattoli G, Hammoumi S, Newman SH, Hagemeijer W, Takekawa JY, Cappelle J, Dodman T, Joannis T, Gil P, Monne I, Fusaro A, Capua I, Manu S, Micheloni P, Ottosson U, Mshelbwala JH, Lubroth J, Domenech J, Monicat F: Evidence of infection by H5N2 highly pathogenic avian influenza viruses in healthy wild waterfowl. PLoS Pathog 2008, 4:e1000127.
  • [21]Campitelli L, Mogavero E, De Marco MA, Delogu M, Puzelli S, Frezza F, Facchini M, Chiapponi C, Foni E, Cordioli P, Webby R, Barigazzi G, Webster RG, Donatelli I: Interspecies transmission of an H7N3 influenza virus from wild birds to intensively reared domestic poultry in Italy. Virology 2004, 323:24-36.
  • [22]Munster VJ, Wallensten A, Baas C, Rimmelzwaan GF, Schutten M, Olsen B, Osterhaus ADME, Fouchier RAM: Mallards and highly pathogenic avian influenza ancestral viruses, northern Europe. Emerg Infect Dis 2005, 11:1545-1551.
  • [23]Duan L, Campitelli L, Fan XH, Leung YHC, Vijaykrishna D, Zhang JX, Donatelli I, Delogu M, Li KS, Foni E, Chiapponi C, Wu WL, Kai H, Webster RG, Shortridge KF, Peiris JSM, Smith GJD, Chen H, Guan Y: Characterization of low-pathogenic H5 subtype influenza viruses from Eurasia: implications for the origin of highly pathogenic H5N1 viruses. J Virol 2007, 81:7529-7539.
  • [24]Chen H, Smith GJD, Zhang SY, Qin K, Wang J, Li KS, Webster RG, Peiris JSM, Guan Y: Avian flu: H5N1 virus outbreak in migratory waterfowl. Nature 2005, 436:191-192.
  • [25]Ellis TM, Dyrting KC, Wong CW, Chadwick B, Chan C, Chiang M, Li C, Li P, Smith GJD, Guan Y, Malik Peiris JS: Analysis of H5N1 avian influenza infections from wild bird surveillance in Hong Kong from January 2006 to October 2007. Avian Pathol 2009, 38:107-119.
  • [26]Feare CJ: Role of wild birds in the spread of highly pathogenic avian influenza virus H5N1 and implications for global surveillance. Avian Dis 2010, 54:201-212.
  • [27]Banks J, Speidel ES, Moore E, Plowright L, Piccirillo A, Capua I, Cordioli P, Fioretti A, Alexander DJ: Changes in the haemagglutinin and the neuraminidase genes prior to the emergence of highly pathogenic H7N1 avian influenza viruses in Italy. Arch Virol 2001, 146:963-973.
  • [28]Di Trani L, Bedini B, Cordioli P, Muscillo M, Vignolo E, Moreno A, Tollis M: Molecular characterization of low pathogenicity H7N3 avian influenza viruses isolated in Italy. Avian Dis 2004, 48:376-383.
  • [29]Campitelli L, Di Martino A, Spagnolo D, Smith GJD, Di Trani L, Facchini M, De Marco MA, Foni E, Chiapponi C, Martin AM, Chen H, Guan Y, Delogu M, Donatelli I: Molecular analysis of avian H7 influenza viruses circulating in Eurasia in 1999-2005: detection of multiple reassortant virus genotypes. J Gen Virol 2008, 89:48-59.
  • [30]Röhm C, Süss J, Pohle V, Webster RG: Different hemagglutinin cleavage site variants of H7N7 in an influenza outbreak in chickens in Leipzig, Germany. Virology 1996, 218:253-257.
  • [31]Stegeman A, Bouma A, Elbers ARW, de Jong MCM, Nodelijk G, de Klerk F, Koch G, van Boven M: Avian influenza A virus (H7N7) epidemic in The Netherlands in 2003: course of the epidemic and effectiveness of control measures. J Infect Dis 2004, 190:2088-2095.
  • [32]Selleck PW, Arzey G, Kirkland PD, Reece RL, Gould AR, Daniels PW, Westbury HA: An outbreak of highly pathogenic avian influenza in Australia in 1997 caused by an H7N4 virus. Avian Dis 2003, 47:806-811.
  • [33]Bulach D, Halpin R, Spiro D, Pomeroy L, Janies D, Boyle DB: Molecular analysis of H7 avian influenza viruses from Australia and New Zealand: genetic diversity and relationships from 1976 to 2007. J Virol 2010, 84:9957-9966.
  • [34]Li Y, Li C, Liu L, Wang H, Wang C, Tian G, Webster RG, Yu K, Chen H: Characterization of an avian influenza virus of subtype H7N2 isolated from chickens in northern China. Virus Genes 2006, 33:117-122.
  • [35]Abbas MA, Spackman E, Swayne DE, Ahmed Z, Sarmento L, Siddique N, Naeem K, Hameed A, Rehmani S: Sequence and phylogenetic analysis of H7N3 avian influenza viruses isolated from poultry in Pakistan 1995-2004. Virol J 2010, 7:137. BioMed Central Full Text
  • [36]Pasick J, Handel K, Robinson J, Copps J, Ridd D, Hills K, Kehler H, Cottam-Birt C, Neufeld J, Berhane Y, Czub S: Intersegmental recombination between the haemagglutinin and matrix genes was responsible for the emergence of a highly pathogenic H7N3 avian influenza virus in British Columbia. J Gen Virol 2005, 86:727-731.
  • [37]Berhane Y, Hisanaga T, Kehler H, Neufeld J, Manning L, Argue C, Handel K, Hooper-McGrevy K, Jonas M, Robinson J, Webster RG, Pasick J: Highly pathogenic avian influenza virus A (H7N3) in domestic poultry, Saskatchewan, Canada, 2007. Emerg Infect Dis 2009, 15:1492-1495.
  • [38]Suarez DL, Garcia M, Latimer J, Senne D, Perdue M: Phylogenetic analysis of H7 avian influenza viruses isolated from the live bird markets of the Northeast United States. J Virol 1999, 73:3567-3573.
  • [39]Spackman E, Senne DA, Davison S, Suarez DL: Sequence analysis of recent H7 avian influenza viruses associated with three different outbreaks in commercial poultry in the United States. J Virol 2003, 77:13399-13402.
  • [40]Spackman E, McCracken KG, Winker K, Swayne DE: H7N3 avian influenza virus found in a South American wild duck is related to the Chilean 2002 poultry outbreak, contains genes from equine and North American wild bird lineages, and is adapted to domestic turkeys. J Virol 2006, 80:7760-7764.
  • [41]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.
  • [42]Krasnitz M, Levine AJ, Rabadan R: Anomalies in the influenza virus genome database: new biology or laboratory errors? J Virol 2008, 82:8947-8950.
  • [43]R Development Core Team: R: A language and environment for statistical computing. Vienna, Austria; 2009.
  • [44]Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG: Clustal W and Clustal X version 2.0. Bioinformatics 2007, 23:2947-2948.
  • [45]Guindon S, Gascuel O: A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 2003, 52:696-704.
  • [46]Keane TM, Creevey CJ, Pentony MM, Naughton TJ, Mclnerney JO: Assessment of methods for amino acid matrix selection and their use on empirical data shows that ad hoc assumptions for choice of matrix are not justified. BMC Evol Biol 2006, 6:29. BioMed Central Full Text
  • [47]Drummond AJ, Rambaut A: BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 2007, 7:214. BioMed Central Full Text
  • [48]Shapiro B, Rambaut A, Drummond AJ: Choosing appropriate substitution models for the phylogenetic analysis of protein-coding sequences. Mol Biol Evol 2006, 23:7-9.
  • [49]Vijaykrishna D, Bahl J, Riley S, Duan L, Zhang JX, Chen H, Peiris JSM, Smith GJD, Guan Y: Evolutionary dynamics and emergence of panzootic H5N1 influenza viruses. PLoS Pathog 2008, 4:e1000161.
  • [50]Bahl J, Vijaykrishna D, Holmes EC, Smith GJD, Guan Y: Gene flow and competitive exclusion of avian influenza A virus in natural reservoir hosts. Virology 2009, 390:289-297.
  • [51]Drummond AJ, Ho SYW, Phillips MJ, Rambaut A: Relaxed phylogenetics and dating with confidence. PLoS Biol 2006, 4:e88.
  • [52]Kass RE, Raftery AE: Bayes Factors. J Am Stat Assoc 1995, 90:773-795.
  • [53]Suchard MA, Weiss RE, Sinsheimer JS: Bayesian selection of continuous-time Markov chain evolutionary models. Mol Biol Evol 2001, 18:1001-1013.
  • [54]Rambaut A, Drummond AJ: Tracer v1.5. [http://tree.bio.ed.ac.uk/software/tracer] webcite
  • [55]Brandley MC, Schmitz A, Reeder TW: Partitioned Bayesian analyses, partition choice, and the phylogenetic relationships of scincid lizards. Syst Biol 2005, 54:373-390.
  • [56]Drummond AJ, Rambaut A, Shapiro B, Pybus OG: Bayesian coalescent inference of past population dynamics from molecular sequences. Mol Biol Evol 2005, 22:1185-1192.
  • [57]Rambaut A, Pybus OG, Nelson MI, Viboud C, Taubenberger JK, Holmes EC: The genomic and epidemiological dynamics of human influenza A virus. Nature 2008, 453:615-619.
  • [58]Kosakovsky Pond SL, Frost SDW, Muse SV: HyPhy: hypothesis testing using phylogenies. Bioinformatics 2005, 21:676-679.
  • [59]Kosakovsky Pond SL, Frost SDW: Datamonkey: rapid detection of selective pressure on individual sites of codon alignments. Bioinformatics 2005, 21:2531-2533.
  • [60]Delport W, Poon AFY, Frost SDW, Kosakovsky Pond SL: Datamonkey 2010: a suite of phylogenetic analysis tools for evolutionary biology. Bioinformatics 2010, 26:2455-2457.
  • [61]Kosakovsky Pond SL, Frost SDW: Not So Different After All: A Comparison of Methods for Detecting Amino Acid Sites Under Selection. Mol Biol Evol 2005, 22:1208-1222.
  • [62]Banks J, Speidel EC, McCauley JW, Alexander DJ: Phylogenetic analysis of H7 haemagglutinin subtype influenza A viruses. Arch Virol 2000, 145:1047-1058.
  • [63]Pasick J, Berhane Y, Hisanaga T, Kehler H, Hooper-McGrevy K, Handel K, Neufeld J, Argue C, Leighton F: Diagnostic test results and pathology associated with the 2007 Canadian H7N3 highly pathogenic avian influenza outbreak. Avian Dis 2010, 54:213-219.
  • [64]Krauss S, Obert CA, Franks J, Walker D, Jones K, Seiler P, Niles L, Pryor SP, Obenauer JC, Naeve CW, Widjaja L, Webby RJ, Webster RG: Influenza in migratory birds and evidence of limited intercontinental virus exchange. PLoS Pathog 2007, 3:e167.
  • [65]Krauss S, Walker D, Pryor SP, Niles L, Chenghong L, Hinshaw VS, Webster RG: Influenza A viruses of migrating wild aquatic birds in North America. Vector Borne Zoonotic Dis 2004, 4:177-189.
  • [66]Wallensten A, Munster VJ, Latorre-Margalef N, Brytting M, Elmberg J, Fouchier RAM, Fransson T, Haemig PD, Karlsson M, Lundkvist A, Osterhaus ADME, Stervander M, Waldenström J, Björn O: Surveillance of influenza A virus in migratory waterfowl in northern Europe. Emerg Infect Dis 2007, 13:404-411.
  • [67]Sharp GB, Kawaoka Y, Wright SM, Turner B, Hinshaw V, Webster RG: Wild ducks are the reservoir for only a limited number of influenza A subtypes. Epidemiol Infect 1993, 110:161-176.
  • [68]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, 160:411-418.
  • [69]Smith GJD, Vijaykrishna D, Ellis TM, Dyrting KC, Leung YHC, Bahl J, Wong CW, Kai H, Chow MKW, Duan L, Chan ASL, Zhang LJ, Chen H, Luk GSM, Peiris JSM, Guan Y: Characterization of avian influenza viruses A (H5N1) from wild birds, Hong Kong, 2004-2008. Emerg Infect Dis 2009, 15:402-407.
  • [70]Hulse-Post DJ, Sturm-Ramirez KM, Humberd J, Seiler P, Govorkova EA, Krauss S, Scholtissek C, Puthavathana P, Buranathai C, Nguyen TD, Long HT, Naipospos TSP, Chen H, Ellis TM, Guan Y, Peiris JSM, Webster RG: Role of domestic ducks in the propagation and biological evolution of highly pathogenic H5N1 influenza viruses in Asia. Proc Natl Acad Sci USA 2005, 102:10682-10687.
  • [71]Sturm-Ramirez KM, Hulse-Post DJ, Govorkova EA, Humberd J, Seiler P, Puthavathana P, Buranathai C, Nguyen TD, Chaisingh A, Long HT, Naipospos TSP, Chen H, Ellis TM, Guan Y, Peiris JSM, Webster RG: Are ducks contributing to the endemicity of highly pathogenic H5N1 influenza virus in Asia? J Virol 2005, 79:11269-11279.
  • [72]Lebarbenchon C, Albespy F, Brochet A, Grandhomme V, Renaud F, Fritz H, Green AJ, Thomas F, van der Werf S, Aubry P, Guillemain M, Gauthier-Clerc M: Spread of avian influenza viruses by Common Teal (Anas crecca) in Europe. PLoS ONE 2009, 4:e7289.
  • [73]Brochet A, Guillemain M, Lebarbenchon C, Simon G, Fritz H, Green AJ, Renaud F, Thomas F, Gauthier-Clerc M: The potential distance of highly pathogenic avian influenza virus dispersal by mallard, common teal and Eurasian pochard. Ecohealth 2009, 6:449-457.
  • [74]Bourouiba L, Wu J, Newman S, Takekawa J, Natdorj T, Batbayar N, Bishop CM, Hawkes LA, Butler PJ, Wikelski M: Spatial dynamics of bar-headed geese migration in the context of H5N1. J R Soc Interface 2010, 7:1627-1639.
  • [75]Reperant LA, Fuckar NS, Osterhaus ADME, Dobson AP, Kuiken T: Spatial and temporal association of outbreaks of H5N1 influenza virus infection in wild birds with the 0 degrees C isotherm. PLoS Pathog 2010, 6:e1000854.
  • [76]Gaidet N, Capelle J, Takekawa J, Prosser D, Iverson S, Douglas D, Perry W, Mundkur T, Newman S: Potential spread of highly pathogenic avian influenza H5N1 by wildfowl: dispersal ranges and rates determined from large-scale satellite telemetry. J Appl Ecol 2010, 47:1147-1157.
  • [77]Dugan VG, Chen R, Spiro DJ, Sengamalay N, Zaborsky J, Ghedin E, Nolting J, Swayne DE, Runstadler JA, Happ GM, Senne DA, Wang R, Slemons RD, Holmes EC, Taubenberger JK: The evolutionary genetics and emergence of avian influenza viruses in wild birds. PLoS Pathog 2008, 4:e1000076.
  • [78]Lebarbenchon C, Feare CJ, Renaud F, Thomas F, Gauthier-Clerc M: Persistence of highly pathogenic avian influenza viruses in natural ecosystems. Emerg Infect Dis 2010, 16:1057-1062.
  • [79]Sakabe S, Sakoda Y, Haraguchi Y, Isoda N, Soda K, Takakuwa H, Saijo K, Sawata A, Kume K, Hagiwara J, Tuchiya K, Lin Z, Sakamoto R, Imamura T, Sasaki T, Kokumai N, Kawaoka Y, Kida H: A vaccine prepared from a non-pathogenic H7N7 virus isolated from natural reservoir conferred protective immunity against the challenge with lethal dose of highly pathogenic avian influenza virus in chickens. Vaccine 2008, 26:2127-2134.
  • [80]Guan Y, Shortridge KF, Krauss S, Webster RG: Molecular characterization of H9N2 influenza viruses: were they the donors of the "internal" genes of H5N1 viruses in Hong Kong? Proc Natl Acad Sci USA 1999, 96:9363-9367.
  • [81]Hoffmann E, Stech J, Leneva I, Krauss S, Scholtissek C, Chin PS, Peiris M, Shortridge KF, Webster RG: Characterization of the influenza A virus gene pool in avian species in southern China: was H6N1 a derivative or a precursor of H5N1? J Virol 2000, 74:6309-6315.
  • [82]Lee C, Senne DA, Suarez DL: Effect of vaccine use in the evolution of Mexican lineage H5N2 avian influenza virus. J Virol 2004, 78:8372-8381.
  • [83]Chen R, Holmes EC: Avian influenza virus exhibits rapid evolutionary dynamics. Mol Biol Evol 2006, 23:2336-2341.
  • [84]García M, Suarez DL, Crawford JM, Latimer JW, Slemons RD, Swayne DE, Perdue ML: Evolution of H5 subtype avian influenza A viruses in North America. Virus Res 1997, 51:115-124.
  • [85]Röhm C, Horimoto T, Kawaoka Y, Süss J, Webster RG: Do hemagglutinin genes of highly pathogenic avian influenza viruses constitute unique phylogenetic lineages? Virology 1995, 209:664-670.
  • [86]Suarez DL, Senne DA, Banks J, Brown IH, Essen SC, Lee C, Manvell RJ, Mathieu-Benson C, Moreno V, Pedersen JC, Panigrahy B, Rojas H, Spackman E, Alexander DJ: Recombination resulting in virulence shift in avian influenza outbreak, Chile. Emerg Infect Dis 2004, 10:693-699.
  • [87]Wood GW, Parsons G, Alexander DJ: Replication of influenza A viruses of high and low pathogenicity for chickens at different sites in chickens and ducks following intranasal inoculation. Avian Pathol 1995, 24:545-551.
  • [88]Swayne DE, Slemons RD: Using mean infectious dose of high- and low-pathogenicity avian influenza viruses originating from wild duck and poultry as one measure of infectivity and adaptation to poultry. Avian Dis 2008, 52:455-460.
  • [89]Wilson IA, Skehel JJ, Wiley DC: Structure of the haemagglutinin membrane glycoprotein of influenza virus at 3 A resolution. Nature 1981, 289:366-373.
  • [90]Vigerust DJ, Shepherd VL: Virus glycosylation: role in virulence and immune interactions. Trends Microbiol 2007, 15:211-218.
  • [91]Nobusawa E, Aoyama T, Kato H, Suzuki Y, Tateno Y, Nakajima K: Comparison of complete amino acid sequences and receptor-binding properties among 13 serotypes of hemagglutinins of influenza A viruses. Virology 1991, 182:475-485.
  • [92]Yang H, Chen L, Carney PJ, Donis RO, Stevens J: Structures of receptor complexes of a North American H7N2 influenza hemagglutinin with a loop deletion in the receptor binding site. PLoS Pathog 2010, 6:e1001081.
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