Host shifts and molecular evolution of H7 avian influenza virus hemagglutinin

Virology Journal

Volumn 8, Issue , 2011, Pages

  Lebarbenchon, Camille ^a   Stallknecht, David E ^a  

^a UNIVERSITY OF GEORGIA   (United States)

Author keywords

adaptation; duck; Influenza A; parallel evolution; poultry; receptor binding domain; virulence

Indexed keywords

INFLUENZA VIRUS HEMAGGLUTININ; VIRUS RNA;

ADAPTATION; ARTICLE; AUSTRALIA; AVIAN INFLUENZA VIRUS; CONTROLLED STUDY; GENETIC VARIABILITY; GLYCOSYLATION; MICROBIAL POPULATION DYNAMICS; MOLECULAR EVOLUTION; NONHUMAN; NORTH AMERICA; NUCLEOTIDE SEQUENCE; PHYLOGEOGRAPHY; PROTEIN DOMAIN; RECEPTOR BINDING; SOUTH AMERICA; VIRUS VIRULENCE; AFRICA; AMINO ACID SUBSTITUTION; ANIMAL; ASIA; AVIAN INFLUENZA; BIRD; EUROPE; GENETIC SELECTION; GENETICS; HOST RANGE; INFLUENZA VIRUS A; ISOLATION AND PURIFICATION; MISSENSE MUTATION; PATHOGENICITY; POULTRY; VIROLOGY; VIRULENCE;

AVES; AVIAN INFLUENZA VIRUS; INFLUENZA A VIRUS;

ADAPTATION, BIOLOGICAL; AFRICA; AMINO ACID SUBSTITUTION; ANIMALS; ASIA; AUSTRALIA; BIRDS; EUROPE; EVOLUTION, MOLECULAR; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; HOST SPECIFICITY; INFLUENZA A VIRUS; INFLUENZA IN BIRDS; MUTATION, MISSENSE; NORTH AMERICA; PHYLOGEOGRAPHY; POULTRY; RNA, VIRAL; SELECTION, GENETIC; SOUTH AMERICA; VIRULENCE;

EID: 79959580466     PISSN: None     EISSN: 1743422X     Source Type: Journal    
DOI: 10.1186/1743-422X-8-328     Document Type: Article

References (92)

1. Humans as the world's greatest evolutionary force. SR Palumbi, Science 2001 293 1786 1790 10.1126/science.293.5536.1786 11546863 (Pubitemid 32845769)
2. Evolution of pathogens in a man-made world. C Lebarbenchon SP Brown R Poulin M Gauthier-Clerc F Thomas, Mol Ecol 2008 17 475 484 10.1111/j.1365-294X. 2007.03375.x 18173509 (Pubitemid 350292452)
3. Emerging and re-emerging infectious diseases: the third epidemiological transition. R Barrett C Kuzawa T McDade G Armelagos, Annu Rev Anthropol 1998 27 247 271 10.1146/annurev.anthro.27.1.247
4. Intensive farming: evolutionary implications for parasites and pathogens. A Mennerat F Nilsen D Ebert A Skorping, Evol Biol 2010 37 59 67 10.1007/s11692-010-9089-0 21151485
5. Mapping H5N1 highly pathogenic avian influenza risk in Southeast Asia. M Gilbert X Xiao DU Pfeiffer M Epprecht S Boles C Czarnecki P Chaitaweesub W Kalpravidh PQ Minh MJ Otte V Martin J Slingenbergh, Proc Natl Acad Sci USA 2008 105 4769 4774 10.1073/pnas.0710581105 18362346 (Pubitemid 351753821)
6. Infectious diseases emerging from Chinese wet-markets: zoonotic origins of severe respiratory viral infections. PC Woo SK Lau K Yuen, Curr Opin Infect Dis 2006 19 401 407 10.1097/01.qco.0000244043.08264.fc 16940861 (Pubitemid 44338097)
7. Industrial food animal production and global health risks: exploring the ecosystems and economics of avian influenza. JH Leibler J Otte D Roland-Holst DU Pfeiffer R Soares Magalhaes J Rushton JP Graham EK Silbergeld, Ecohealth 2009 6 58 70 10.1007/s10393-009-0226-0 19437076
8. Highly pathogenic avian influenza virus (H5N1) in frozen duck carcasses, Germany, 2007. TC Harder J Teuffert E Starick J Gethmann C Grund S Fereidouni M Durban KH Bogner A Neubauer-Juric R Repper A Hlinak A Engelhardt A Nöckler K Smietanka Z Minta M Kramer A Globig TC Mettenleiter FJ Conraths M Beer, Emerg Infect Dis 2009 15 272 279 10.3201/eid1502.080949 19193272
9. Persistence of Highly Pathogenic Avian Influenza H5N1 Virus Defined by Agro-Ecological Niche. L Hogerwerf RG Wallace D Ottaviani J Slingenbergh D Prosser L Bergmann M Gilbert, Ecohealth 2010 7 213 225 10.1007/s10393-010-0324-z 20585972
10. Avian influenza virus (H5N1): a threat to human health. JSM Peiris MD de Jong Y Guan, Clin Microbiol Rev 2007 20 243 267 10.1128/CMR.00037-06 17428885 (Pubitemid 46709304)
11. Antigenic and genetic characteristics of swine-origin 2009 A(H1N1) influenza viruses circulating in humans. RJ Garten CT Davis CA Russell B Shu S Lindstrom A Balish WM Sessions X Xu E Skepner V Deyde M Okomo-Adhiambo L Gubareva J Barnes CB Smith SL Emery MJ Hillman P Rivailler J Smagala M de Graaf DF Burke RAM Fouchier C Pappas CM Alpuche-Aranda H Lápez-Gatell H Olivera I Lápez CA Myers D Faix PJ Blair C Yu,, et al. Science 2009 325 197 201 10.1126/science.1176225 19465683
12. Origins and evolutionary genomics of the 2009 swine-origin H1N1 influenza A epidemic. GJD Smith D Vijaykrishna J Bahl SJ Lycett M Worobey OG Pybus SK Ma CL Cheung J Raghwani S Bhatt JSM Peiris Y Guan A Rambaut, Nature 2009 459 1122 1125 10.1038/nature08182 19516283
13. Evolution in health and medicine Sackler colloquium: The comparative genomics of viral emergence. EC Holmes, Proc Natl Acad Sci USA 2010 107 S1 1742 1746 19858482
14. Global patterns of influenza a virus in wild birds. B Olsen VJ Munster A Wallensten J Waldenström ADME Osterhaus RAM Fouchier, Science 2006 312 384 388 10.1126/science.1122438 16627734
15. Hampered foraging and migratory performance in swans infected with low-pathogenic avian influenza A virus. JA van Gils VJ Munster R Radersma D Liefhebber RAM Fouchier M Klaassen, PLoS ONE 2007 2 184 10.1371/journal.pone. 0000184 17264886
16. Effects of influenza A virus infection on migrating mallard ducks. N Latorre-Margalef G Gunnarsson VJ Munster RAM Fouchier ADME Osterhaus J Elmberg B Olsen A Wallensten PD Haemig T Fransson L Brudin J Waldenström, P Roy Soc B-Biol Sci 2009 276 1029 1036 10.1098/rspb.2008.1501
17. Highly pathogenic avian influenza. DE Swayne DL Suarez, Rev Sci Tech 2000 19 463 482 10935274
18. An overview of the epidemiology of avian influenza. DJ Alexander, Vaccine 2007 25 5637 5644 10.1016/j.vaccine.2006.10.051 17126960 (Pubitemid 47031360)
19. The isolation and classification of Tern virus: influenza A-Tern South Africa - 1961. WB Becker, J Hyg 1966 64 309 320 10.1017/S0022172400040596
20. Evidence of infection by H5N2 highly pathogenic avian influenza viruses in healthy wild waterfowl. N Gaidet G Cattoli S Hammoumi SH Newman W Hagemeijer JY Takekawa J Cappelle T Dodman T Joannis P Gil I Monne A Fusaro I Capua S Manu P Micheloni U Ottosson JH Mshelbwala J Lubroth J Domenech F Monicat, PLoS Pathog 2008 4 1000127 10.1371/journal.ppat.1000127 18704172
21. Interspecies transmission of an H7N3 influenza virus from wild birds to intensively reared domestic poultry in Italy. L Campitelli E Mogavero MA De Marco M Delogu S Puzelli F Frezza M Facchini C Chiapponi E Foni P Cordioli R Webby G Barigazzi RG Webster I Donatelli, Virology 2004 323 24 36 10.1016/j.virol.2004.02.015 15165816 (Pubitemid 38681017)
22. Mallards and highly pathogenic avian influenza ancestral viruses, northern Europe. VJ Munster A Wallensten C Baas GF Rimmelzwaan M Schutten B Olsen ADME Osterhaus RAM Fouchier, Emerg Infect Dis 2005 11 1545 1551 16318694 (Pubitemid 41384340)
23. Characterization of low-pathogenic H5 subtype influenza viruses from Eurasia: implications for the origin of highly pathogenic H5N1 viruses. L Duan L Campitelli XH Fan YHC Leung D Vijaykrishna JX Zhang I Donatelli M Delogu KS Li E Foni C Chiapponi WL Wu H Kai RG Webster KF Shortridge JSM Peiris GJD Smith H Chen Y Guan, J Virol 2007 81 7529 7539 10.1128/JVI.00327-07 17507485 (Pubitemid 47047839)
24. Avian flu: H5N1 virus outbreak in migratory waterfowl. H Chen GJD Smith SY Zhang K Qin J Wang KS Li RG Webster JSM Peiris Y Guan, Nature 2005 436 191 192 10.1038/nature03974 16007072 (Pubitemid 41021261)
25. Analysis of H5N1 avian influenza infections from wild bird surveillance in Hong Kong from January 2006 to October 2007. TM Ellis KC Dyrting CW Wong B Chadwick C Chan M Chiang C Li P Li GJD Smith Y Guan JS Malik Peiris, Avian Pathol 2009 38 107 119 10.1080/03079450902751855 19322709
26. Role of wild birds in the spread of highly pathogenic avian influenza virus H5N1 and implications for global surveillance. CJ Feare, Avian Dis 2010 54 201 212 10.1637/8766-033109-ResNote.1 20521633
27. Changes in the haemagglutinin and the neuraminidase genes prior to the emergence of highly pathogenic H7N1 avian influenza viruses in Italy. J Banks ES Speidel E Moore L Plowright A Piccirillo I Capua P Cordioli A Fioretti DJ Alexander, Arch Virol 2001 146 963 973 10.1007/s007050170128 11448033 (Pubitemid 32477408)
28. Molecular characterization of low pathogenicity H7N3 avian influenza viruses isolated in Italy. L Di Trani B Bedini P Cordioli M Muscillo E Vignolo A Moreno M Tollis, Avian Dis 2004 48 376 383 10.1637/7088 15283425 (Pubitemid 39508874)
29. Molecular analysis of avian H7 influenza viruses circulating in Eurasia in 1999-2005: detection of multiple reassortant virus genotypes. L Campitelli A Di Martino D Spagnolo GJD Smith L Di Trani M Facchini MA De Marco E Foni C Chiapponi AM Martin H Chen Y Guan M Delogu I Donatelli, J Gen Virol 2008 89 48 59 10.1099/vir.0.83111-0 18089728
30. Different hemagglutinin cleavage site variants of H7N7 in an influenza outbreak in chickens in Leipzig, Germany. C Röhm J Süss V Pohle RG Webster, Virology 1996 218 253 257 10.1006/viro.1996.0187 8615031 (Pubitemid 26133105)
31. Avian influenza A virus (H7N7) epidemic in The Netherlands in 2003: course of the epidemic and effectiveness of control measures. A Stegeman A Bouma ARW Elbers MCM de Jong G Nodelijk F de Klerk G Koch M van Boven, J Infect Dis 2004 190 2088 2095 10.1086/425583 15551206 (Pubitemid 39636355)
32. An outbreak of highly pathogenic avian influenza in Australia in 1997 caused by an H7N4 virus. PW Selleck G Arzey PD Kirkland RL Reece AR Gould PW Daniels HA Westbury, Avian Dis 2003 47 806 811 10.1637/0005-2086-47.s3.806 14575068 (Pubitemid 37143840)
33. Molecular analysis of H7 avian influenza viruses from Australia and New Zealand: genetic diversity and relationships from 1976 to 2007. D Bulach R Halpin D Spiro L Pomeroy D Janies DB Boyle, J Virol 2010 84 9957 9966 10.1128/JVI.00930-10 20668069
34. Characterization of an avian influenza virus of subtype H7N2 isolated from chickens in northern China. Y Li C Li L Liu H Wang C Wang G Tian RG Webster K Yu H Chen, Virus Genes 2006 33 117 122 10.1007/s11262-005-0042-8 16791426 (Pubitemid 43961589)
35. Sequence and phylogenetic analysis of H7N3 avian influenza viruses isolated from poultry in Pakistan 1995-2004. MA Abbas E Spackman DE Swayne Z Ahmed L Sarmento N Siddique K Naeem A Hameed S Rehmani, Virol J 2010 7 137 10.1186/1743-422X-7-137 20576101
36. 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 Pasick K Handel J Robinson J Copps D Ridd K Hills H Kehler C Cottam-Birt J Neufeld Y Berhane S Czub, J Gen Virol 2005 86 727 731 10.1099/vir.0.80478-0 15722533 (Pubitemid 40331252)
37. Highly pathogenic avian influenza virus A (H7N3) in domestic poultry, Saskatchewan, Canada, 2007. Y Berhane T Hisanaga H Kehler J Neufeld L Manning C Argue K Handel K Hooper-McGrevy M Jonas J Robinson RG Webster J Pasick, Emerg Infect Dis 2009 15 1492 1495 19788823
38. Phylogenetic analysis of H7 avian influenza viruses isolated from the live bird markets of the Northeast United States. DL Suarez M Garcia J Latimer D Senne M Perdue, J Virol 1999 73 3567 3573 10196246 (Pubitemid 29189795)
39. Sequence analysis of recent H7 avian influenza viruses associated with three different outbreaks in commercial poultry in the United States. E Spackman DA Senne S Davison DL Suarez, J Virol 2003 77 13399 13402 10.1128/JVI.77.24. 13399-13402.2003 14645595 (Pubitemid 37494334)
40. 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. E Spackman KG McCracken K Winker DE Swayne, J Virol 2006 80 7760 7764 10.1128/JVI.00445-06 16840356 (Pubitemid 44092596)
41. The influenza virus resource at the National Center for Biotechnology Information. Y Bao P Bolotov D Dernovoy B Kiryutin L Zaslavsky T Tatusova J Ostell D Lipman, J Virol 2008 82 596 601 10.1128/JVI.02005-07 17942553
42. Anomalies in the influenza virus genome database: new biology or laboratory errors? M Krasnitz AJ Levine R Rabadan, J Virol 2008 82 8947 8950 10.1128/JVI.00101-08 18579605
43. R Development Core Team, R: A language and environment for statistical computing Vienna, Austria 2009
44. Clustal W and Clustal X version 2.0. MA Larkin G Blackshields NP Brown R Chenna PA McGettigan H McWilliam F Valentin IM Wallace A Wilm R Lopez JD Thompson TJ Gibson DG Higgins, Bioinformatics 2007 23 2947 2948 10.1093/bioinformatics/btm404 17846036 (Pubitemid 350162903)
45. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. S Guindon O Gascuel, Syst Biol 2003 52 696 704 10.1080/10635150390235520 14530136 (Pubitemid 37365050)
46. 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. TM Keane CJ Creevey MM Pentony TJ Naughton JO Mclnerney, BMC Evol Biol 2006 6 29 10.1186/1471-2148-6-29 16563161
47. BEAST: Bayesian evolutionary analysis by sampling trees. AJ Drummond A Rambaut, BMC Evol Biol 2007 7 214 10.1186/1471-2148-7-214 17996036
48. Choosing appropriate substitution models for the phylogenetic analysis of protein-coding sequences. B Shapiro A Rambaut AJ Drummond, Mol Biol Evol 2006 23 7 9 16177232 (Pubitemid 41785947)
49. Evolutionary dynamics and emergence of panzootic H5N1 influenza viruses. D Vijaykrishna J Bahl S Riley L Duan JX Zhang H Chen JSM Peiris GJD Smith Y Guan, PLoS Pathog 2008 4 1000161 10.1371/journal.ppat.1000161 18818732
50. Gene flow and competitive exclusion of avian influenza A virus in natural reservoir hosts. J Bahl D Vijaykrishna EC Holmes GJD Smith Y Guan, Virology 2009 390 289 297 10.1016/j.virol.2009.05.002 19501380
51. Relaxed phylogenetics and dating with confidence. AJ Drummond SYW Ho MJ Phillips A Rambaut, PLoS Biol 2006 4 88 10.1371/journal.pbio.0040088 16683862
52. Bayes Factors. RE Kass AE Raftery, J Am Stat Assoc 1995 90 773 795 10.2307/2291091
53. Bayesian selection of continuous-time Markov chain evolutionary models. MA Suchard RE Weiss JS Sinsheimer, Mol Biol Evol 2001 18 1001 1013 11371589 (Pubitemid 32520473)
54. Tracer v1.5. A Rambaut AJ Drummond, http://tree.bio.ed.ac.uk/software/ tracer
55. Partitioned Bayesian analyses, partition choice, and the phylogenetic relationships of scincid lizards. MC Brandley A Schmitz TW Reeder, Syst Biol 2005 54 373 390 10.1080/10635150590946808 16012105 (Pubitemid 41040438)
56. Bayesian coalescent inference of past population dynamics from molecular sequences. AJ Drummond A Rambaut B Shapiro OG Pybus, Mol Biol Evol 2005 22 1185 1192 10.1093/molbev/msi103 15703244 (Pubitemid 40577756)
57. The genomic and epidemiological dynamics of human influenza A virus. A Rambaut OG Pybus MI Nelson C Viboud JK Taubenberger EC Holmes, Nature 2008 453 615 619 10.1038/nature06945 18418375 (Pubitemid 351769300)
58. HyPhy: hypothesis testing using phylogenies. SL Kosakovsky Pond SDW Frost SV Muse, Bioinformatics 2005 21 676 679 10.1093/bioinformatics/bti079 15509596 (Pubitemid 40424796)
59. Datamonkey: rapid detection of selective pressure on individual sites of codon alignments. SL Kosakovsky Pond SDW Frost, Bioinformatics 2005 21 2531 2533 10.1093/bioinformatics/bti320 15713735 (Pubitemid 40731616)
60. Datamonkey 2010: a suite of phylogenetic analysis tools for evolutionary biology. W Delport AFY Poon SDW Frost SL Kosakovsky Pond, Bioinformatics 2010 26 2455 2457 10.1093/bioinformatics/btq429 20671151
61. Not So Different After All: A Comparison of Methods for Detecting Amino Acid Sites Under Selection. SL Kosakovsky Pond SDW Frost, Mol Biol Evol 2005 22 1208 1222 10.1093/molbev/msi105 15703242 (Pubitemid 40577758)
62. Phylogenetic analysis of H7 haemagglutinin subtype influenza A viruses. J Banks EC Speidel JW McCauley DJ Alexander, Arch Virol 2000 145 1047 1058 10.1007/s007050050695 10881690 (Pubitemid 30333947)
63. Diagnostic test results and pathology associated with the 2007 Canadian H7N3 highly pathogenic avian influenza outbreak. J Pasick Y Berhane T Hisanaga H Kehler K Hooper-McGrevy K Handel J Neufeld C Argue F Leighton, Avian Dis 2010 54 213 219 10.1637/8822-040209-Reg.1 20521634
64. Influenza in migratory birds and evidence of limited intercontinental virus exchange. S Krauss CA Obert J Franks D Walker K Jones P Seiler L Niles SP Pryor JC Obenauer CW Naeve L Widjaja RJ Webby RG Webster, PLoS Pathog 2007 3 167 10.1371/journal.ppat.0030167 17997603
65. Influenza A viruses of migrating wild aquatic birds in North America. S Krauss D Walker SP Pryor L Niles L Chenghong VS Hinshaw RG Webster, Vector Borne Zoonotic Dis 2004 4 177 189 10.1089/vbz.2004.4.177 15631061 (Pubitemid 39429943)
66. Surveillance of influenza A virus in migratory waterfowl in northern Europe. A Wallensten VJ Munster N Latorre-Margalef M Brytting J Elmberg RAM Fouchier T Fransson PD Haemig M Karlsson A Lundkvist ADME Osterhaus M Stervander J Waldenström O Björn, Emerg Infect Dis 2007 13 404 411 10.3201/eid1303.061130 17552093 (Pubitemid 46348127)
67. Wild ducks are the reservoir for only a limited number of influenza A subtypes. GB Sharp Y Kawaoka SM Wright B Turner V Hinshaw RG Webster, Epidemiol Infect 1993 110 161 176 10.1017/S0950268800050780 8381747 (Pubitemid 23217339)
68. Molecular analysis of the hemagglutinin genes of Australian H7N7 influenza viruses: role of passerine birds in maintenance or transmission? A Nestorowicz Y Kawaoka WJ Bean RG Webster, Virology 1987 160 411 418 10.1016/0042-6822(87)90012-2 3660587
69. Characterization of avian influenza viruses A (H5N1) from wild birds, Hong Kong, 2004-2008. GJD Smith D Vijaykrishna TM Ellis KC Dyrting YHC Leung J Bahl CW Wong H Kai MKW Chow L Duan ASL Chan LJ Zhang H Chen GSM Luk JSM Peiris Y Guan, Emerg Infect Dis 2009 15 402 407 10.3201/eid1503.081190 19239752
70. Role of domestic ducks in the propagation and biological evolution of highly pathogenic H5N1 influenza viruses in Asia. DJ Hulse-Post KM Sturm-Ramirez J Humberd P Seiler EA Govorkova S Krauss C Scholtissek P Puthavathana C Buranathai TD Nguyen HT Long TSP Naipospos H Chen TM Ellis Y Guan JSM Peiris RG Webster, Proc Natl Acad Sci USA 2005 102 10682 10687 10.1073/pnas.0504662102 16030144 (Pubitemid 41061614)
71. Are ducks contributing to the endemicity of highly pathogenic H5N1 influenza virus in Asia? KM Sturm-Ramirez DJ Hulse-Post EA Govorkova J Humberd P Seiler P Puthavathana C Buranathai TD Nguyen A Chaisingh HT Long TSP Naipospos H Chen TM Ellis Y Guan JSM Peiris RG Webster, J Virol 2005 79 11269 11279 10.1128/JVI.79.17.11269-11279.2005 16103179 (Pubitemid 41170669)
72. Spread of avian influenza viruses by Common Teal (Anas crecca) in Europe. C Lebarbenchon F Albespy A Brochet V Grandhomme F Renaud H Fritz AJ Green F Thomas S van der Werf P Aubry M Guillemain M Gauthier-Clerc, PLoS ONE 2009 4 7289 10.1371/journal.pone.0007289 19802387
73. The potential distance of highly pathogenic avian influenza virus dispersal by mallard, common teal and Eurasian pochard. A Brochet M Guillemain C Lebarbenchon G Simon H Fritz AJ Green F Renaud F Thomas M Gauthier-Clerc, Ecohealth 2009 6 449 457 10.1007/s10393-010-0275-4 20112048
74. Spatial dynamics of bar-headed geese migration in the context of H5N1. L Bourouiba J Wu S Newman J Takekawa T Natdorj N Batbayar CM Bishop LA Hawkes PJ Butler M Wikelski, J R Soc Interface 2010 7 1627 1639 10.1098/rsif.2010.0126 20472636
75. Spatial and temporal association of outbreaks of H5N1 influenza virus infection in wild birds with the 0 degrees C isotherm. LA Reperant NS Fuckar ADME Osterhaus AP Dobson T Kuiken, PLoS Pathog 2010 6 1000854 10.1371/journal.ppat.1000854 20386716
76. Potential spread of highly pathogenic avian influenza H5N1 by wildfowl: dispersal ranges and rates determined from large-scale satellite telemetry. N Gaidet J Capelle J Takekawa D Prosser S Iverson D Douglas W Perry T Mundkur S Newman, J Appl Ecol 2010 47 1147 1157 10.1111/j.1365-2664.2010.01845.x
77. The evolutionary genetics and emergence of avian influenza viruses in wild birds. VG Dugan R Chen DJ Spiro N Sengamalay J Zaborsky E Ghedin J Nolting DE Swayne JA Runstadler GM Happ DA Senne R Wang RD Slemons EC Holmes JK Taubenberger, PLoS Pathog 2008 4 1000076 10.1371/journal.ppat.1000076 18516303
78. Persistence of highly pathogenic avian influenza viruses in natural ecosystems. C Lebarbenchon CJ Feare F Renaud F Thomas M Gauthier-Clerc, Emerg Infect Dis 2010 16 1057 1062 20587174
79. 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. S Sakabe Y Sakoda Y Haraguchi N Isoda K Soda H Takakuwa K Saijo A Sawata K Kume J Hagiwara K Tuchiya Z Lin R Sakamoto T Imamura T Sasaki N Kokumai Y Kawaoka H Kida, Vaccine 2008 26 2127 2134 18346824
80. Molecular characterization of H9N2 influenza viruses: were they the donors of the "internal" genes of H5N1 viruses in Hong Kong? Y Guan KF Shortridge S Krauss RG Webster, Proc Natl Acad Sci USA 1999 96 9363 9367 10.1073/pnas.96.16.9363 10430948 (Pubitemid 29374760)
81. Characterization of the influenza A virus gene pool in avian species in southern China: was H6N1 a derivative or a precursor of H5N1? E Hoffmann J Stech I Leneva S Krauss C Scholtissek PS Chin M Peiris KF Shortridge RG Webster, J Virol 2000 74 6309 6315 10.1128/JVI.74.14.6309-6315.2000 10864640 (Pubitemid 30429795)
82. Effect of vaccine use in the evolution of Mexican lineage H5N2 avian influenza virus. C Lee DA Senne DL Suarez, J Virol 2004 78 8372 8381 10.1128/JVI.78.15.8372-8381.2004 15254209 (Pubitemid 38944321)
83. Avian influenza virus exhibits rapid evolutionary dynamics. R Chen EC Holmes, Mol Biol Evol 2006 23 2336 2341 10.1093/molbev/msl102 16945980 (Pubitemid 44737127)
84. Evolution of H5 subtype avian influenza A viruses in North America. M García DL Suarez JM Crawford JW Latimer RD Slemons DE Swayne ML Perdue, Virus Res 1997 51 115 124 10.1016/S0168-1702(97)00087-7 9498610 (Pubitemid 27483586)
85. Do hemagglutinin genes of highly pathogenic avian influenza viruses constitute unique phylogenetic lineages? C Röhm T Horimoto Y Kawaoka J Süss RG Webster, Virology 1995 209 664 670 10.1006/viro.1995.1301 7778300
86. Recombination resulting in virulence shift in avian influenza outbreak, Chile. DL Suarez DA Senne J Banks IH Brown SC Essen C Lee RJ Manvell C Mathieu-Benson V Moreno JC Pedersen B Panigrahy H Rojas E Spackman DJ Alexander, Emerg Infect Dis 2004 10 693 699 15200862 (Pubitemid 38420303)
87. Replication of influenza A viruses of high and low pathogenicity for chickens at different sites in chickens and ducks following intranasal inoculation. GW Wood G Parsons DJ Alexander, Avian Pathol 1995 24 545 551 10.1080/03079459508419093 18645810
88. 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. DE Swayne RD Slemons, Avian Dis 2008 52 455 460 10.1637/8229-012508-Reg.1 18939635
89. Structure of the haemagglutinin membrane glycoprotein of influenza virus at 3 A resolution. IA Wilson JJ Skehel DC Wiley, Nature 1981 289 366 373 10.1038/289366a0 7464906
90. Virus glycosylation: role in virulence and immune interactions. DJ Vigerust VL Shepherd, Trends Microbiol 2007 15 211 218 10.1016/j.tim.2007.03.003 17398101 (Pubitemid 46660602)
91. Comparison of complete amino acid sequences and receptor-binding properties among 13 serotypes of hemagglutinins of influenza A viruses. E Nobusawa T Aoyama H Kato Y Suzuki Y Tateno K Nakajima, Virology 1991 182 475 485 10.1016/0042-6822(91)90588-3 2024485
92. Structures of receptor complexes of a North American H7N2 influenza hemagglutinin with a loop deletion in the receptor binding site. H Yang L Chen PJ Carney RO Donis J Stevens, PLoS Pathog 2010 6 1001081 10.1371/journal.ppat. 1001081 20824086