Avian influenza virus and DIVA strategies

Viral Immunology

Volumn 29, Issue 4, 2016, Pages 198-211

  Hasan, Noor Haliza ^a,b   Ignjatovic, Jagoda ^c   Peaston, Anne ^a   Hemmatzadeh, Farhid ^a  

^a UNIVERSITY OF ADELAIDE   (Australia)

^b UNIVERSITI MALAYSIA SABAH   (Malaysia)

^c UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

INFLUENZA VIRUS HEMAGGLUTININ; MATRIX 2 ECTODOMAIN PROTEIN; NONSTRUCTURAL PROTEIN 1; SIALIDASE; SUBUNIT VACCINE; UNCLASSIFIED DRUG; INFLUENZA VACCINE; VIRAL PROTEIN; VIRUS ANTIBODY;

AVIAN INFLUENZA VIRUS; BIRD; EVOLUTION; HIGHLY PATHOGENIC AVIAN INFLUENZA VIRUS; IMMUNE RESPONSE; INFLUENZA A VIRUS (H5N1); LOW PATHOGENIC AVIAN INFLUENZA VIRUS; NONHUMAN; REVIEW; VACCINATION; VIRUS DETECTION; VIRUS TRANSMISSION; VIRUS VIRULENCE; ANIMAL; AVIAN INFLUENZA; BLOOD; CHICKEN; ENDEMIC DISEASE; EPIDEMIOLOGICAL MONITORING; IMMUNOLOGY; INFLUENZA A VIRUS; ISOLATION AND PURIFICATION; PATHOGENICITY; PROCEDURES; SENTINEL SPECIES; SEROLOGY; VETERINARY; VIROLOGY;

ANIMALS; ANTIBODIES, VIRAL; CHICKENS; ENDEMIC DISEASES; EPIDEMIOLOGICAL MONITORING; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; INFLUENZA A VIRUS; INFLUENZA IN BIRDS; INFLUENZA VACCINES; NEURAMINIDASE; SENTINEL SPECIES; SEROLOGIC TESTS; VACCINATION; VIRAL NONSTRUCTURAL PROTEINS;

EID: 84969286284     PISSN: 08828245     EISSN: 15578976     Source Type: Journal    
DOI: 10.1089/vim.2015.0127     Document Type: Review

References (178)

1. Alexander DJ. A review of avian influenza in different bird species. Vet Microbiol 2000;74:3-13.
2. Alexander DJ. Summary of avian influenza activity in Europe, Asia, Africa, and Australasia, 2002-2006. Avian Dis 2007;51:161-166.
3. Alexander DJ, and Brown IH. History of highly pathogenic avian influenza. Rev Sci Tech Off Int Epiz 2009; 28:19-38.
4. Alexander DJ, Parsons G, and Manvell RJ. Experimental assessment of the pathogenicity of eight avian influenza A viruses of H5 subtype for chickens, turkeys, ducks and quail. Avian Pathol 1986;15:647-662.
5. Artois M, Bicout D, Doctrinal D, et al. Outbreaks of highly pathogenic avian influenza in Europe: the risks associated with wild birds. Rev Sci Tech Off Int Epiz 2009;28:69-92.
6. Assaad FA, Bres P, Chu CM, et al. A revision of the system of nomenclature for influenza viruses: a WHO memorandum. Bull World Health Organ 1980;58:585-591.
7. Avellaneda G, Mundt E, Lee CW, et al. Differentiation of infected and vaccinated animals (DIVA) using the NS1 protein of avian influenza virus.AvianDis 2010;54:278-286.
8. Avellaneda G, Sylte MJ, Lee CW, et al. A heterologous neuraminidase subtype strategy for the differentiation of infected and vaccinated animals (DIVA) for avian influenza virus using an alternative neuraminidase inhibition test. Avian Dis 2010;54:272-277.
9. Aymard-Henry M, Coleman MT, Dowdle WR, et al. Influenza virus neuraminidase and neuraminidase-inhibition test procedures. Bull World Health Organ 1973;48:199-202.
10. Beato MS, Rigoni M, Milani A, et al. Generation of avian influenza reassortant viruses of the H7N5 subtype as potential vaccine candidates to be used in the framework of a ''DIVA'' vaccination strategy. Avian Dis 2007;50:479-480.
11. Becker WB. The isolation and classification of Tern virus: influenza virus A/Tern/South Africa/1961. J Hyg (Cambridge) 1966;64:309-320.
12. Birch-Machin I, Rowan A, Pick J, et al. Expression of the nonstructural protein NS1 of equine influenza A virus: detection of anti-NS1 antibody in post infection equine sera. J Virol Methods 1997;65:255-263.
13. Black RA, Rota PA, Gorodkova N, et al. Antibody response to the M2 protein of influenza A virus expressed in insect cells. J Gen Virol 1993;74:143-146.
14. Bogs J, Veits J, Gohrbandt S, et al. Highly pathogenic H5N1 influenza viruses carry virulence determinants beyond the polybasic hemagglutinin cleavage site. PLoS One 2010;5:e11826.
15. Bosch FX, Garten W, Klenk HD, et al. Proteolytic cleavage of influenza virus hemagglutinins: primary structure of the connecting peptide between HA1 and HA2 determines proteolytic cleavability and pathogenicity of avian influenza viruses. Virology 1981;113:725-735.
16. Boyle DB, and Heine HG. Recombinant fowlpox virus vaccines for poultry. Immunol Cell Biol 1993;71:391-397.
17. Brahmakshatriya VR, Lupiani B, and Reddy SM. Characterization and evaluation of avian influenza NS1 mutant virus as a potential live and killed DIVA (differentiating between infected and vaccinated animals) vaccine for chickens. Vaccine 2010;28:2388-2396.
18. Bublot M, Pritchard N, Swayne DE, et al. Development and use of fowlpox vectored vaccines for avian influenza. Ann N Y Acad Sci 2006;1081:193-201.
19. Bullough PA, Hughson FM, Skehel JJ, et al. Structure of influenza haemagglutinin at the pH of membrane fusion. Nature 1994;371:37-43.
20. Capua I, and Alexander J. Avian influenza: recent developments. Avian Pathol 2004;33:393-404.
21. Capua I, Mutinelli F, Pozza MD, et al. The 1999-2000 avian influenza (H7N1) epidemic in Italy: veterinary and human health implications. Acta Tropica 2002;83:7-11.
22. Capua I, Schmitz A, Jestin V, et al. Vaccination as a tool to combat introductions of notifiable avian influenza viruses in Europe, 2000 to 2006. Rev Sci Tech Off Int Epiz 2009;28:245-259.
23. Capua I, Terregino C, Cattoli G, et al. Development of a DIVA strategy using a vaccine containing a heterologous neuraminidase for the control of avian influenza. Avian Pathol 2002;32:47-55.
24. Cattoli G, Milani A, Bettini F, et al. Development and validation of an anti-N3 indirect immunofluorescent antibody test to be used as a companion diagnostic test in the framework of a ''DIVA'' vaccination strategy for avian influenza infections in poultry. Avian Pathol 2006;35:154-159.
25. Cattoli G, Terregino C, Brasola V, et al. Development and preliminary validation of an ad hoc N1-N3 discriminatory test for the control of avian influenza in Italy. Avian Dis 2003;47:1060-1062.
26. Cauthen AN, Swayne DE, Schultz-Cherry S, et al. Continued circulation in China of highly pathogenic avian influenza viruses encoding the hemagglutinin gene associated with the 1997 H5N1 outbreak in poultry and humans. J Virol 2000;74:6592-6599.
27. Chen H. Avian influenza vaccination: the experience in China. Rev Sci Tech Off Int Epiz 2009;28:267-274.
28. Chen H, Deng G, Li Z, et al. The evolution of H5N1 influenza viruses in ducks in southern China. PNAS 2004;101:10452-10457.
29. Chen H, Smith GJD, Zhang SY, et al. H5N1 virus outbreak in migratory waterfowl. Nature 2005;436:191-192.
30. Chen J, Lee KH, Steinhauer DA, et al. Structure of the hemagglutinin precursor cleavage site, a determinant of influenza pathogenicity and the origin of the labile conformation. Cell 1998;95:409-417.
31. Chen W, Calvo PA, Malide D, et al. A novel influenza A virus mitochondrial protein that induces cell death. Nat Med 2001;7:1306-1312.
32. Crawford J, WilkinsonB,Vosnesensky A, et al. Baculovirusderived hemagglutinin vaccines protect against lethal influenza infections by avian H5 and H7 subtypes. Vaccine 1999;17:2265-2274.
33. Daniels RS, Downie JC, Hay AJ, et al. Fusion mutants of the Influenza virus hemagglutinin glycoprotein. Cell 1985; 40:431-439.
34. Davis AR, Bos T, Ueda M, et al. Immune response to human influenza virus hemagglutinin expressed in Escherichia coli. Gene 1983;21:273-284.
35. de Wit E, Munster VJ, van Riel D, et al. Molecular determinants of adaptation of highly pathogenic avian influenza H7N7 viruses to efficient replication in the human host. J Virol 2010;84:1597-1606.
36. Deshpande KL, Naeve CW, and Webster RG. The neuraminidase of the virulent and avirulent A/chicken/Pennsylvania/ 83 (H5N2) influenza A viruses: sequence and antigenic analyses. Virology 1985;147:49-60.
37. Domenech J, Dauphin G, Rushton J, et al. Experiences with vaccination in countries endemically infected with highly pathogenic avian influenza: the Food and Agriculture Organization perspective. Rev Sci Tech Off Int Epiz 2009; 28:293-305.
38. Dundon WG, Maniero S, Toffan A, et al. Appearance of serum antibodies against the avian influenza nonstructural 1 protein in experimentally infected chickens and turkeys. Avian Dis 2007;51:209-212.
39. Dundon WG, Milani A, Cattoli G, et al. Progressive truncation of the non-structural 1 gene of H7N1 avian influenza viruses following extensive circulation in poultry. Virus Res 2006;119:171-176.
40. Enami K, Sato TA, Nakada S, et al. Influenza virus NS1 protein stimulates translation of the M1 protein. J Virol 1994;68:1432-1437.
41. FAO. Approaches to controlling, preventing and eliminating H5N1 highly pathogenic avian influenza in endemic countries Animal Production and Health Paper. Food and Agriculture Organization of the United Nation, Rome, 2011, Vol 171.
42. Feng JQ, Zhang M, Mozdzanowska K, et al. Influenza A virus infection engenders a poor antibody response against the ectodomain of matrix protein 2. Virol J 2006;3:102.
43. Fiers W, De Filette M, Bakkouri KE, et al. M2e-based universal influenza A vaccine. Vaccine 2009;27:6280-6283.
44. Forman AJ, Parsonson IM, and Doughty WJ. The pathogenicity of an avian influenza virus isolated in Victoria. Aust Vet J 1986;63:294-296.
45. Fouchier RAM, and Guan Y. Ecology and evolution of influenza viruses in wild and domestic birds. In: Webster RG, Monto AS, Braciale TJ, et al., eds. Textbook of Influenza. 2nd ed. West Sussex, UK: Wiley Blackwell, 2013: 175-189.
46. Fouchier RAM, Munster VJ, Wallensten A, et al. Characterization of a novel Influenza A virus hemagglutinin subtype (H16) obtained from black-headed gulls. J Virol 2005;79:2814-2822.
47. Garcia M, Crawford JM, Latimer JW, et al. Heterogeneity in the haemagglutinin gene and emergence of the highly pathogenic phenotype among recent H5N2 avian influenza viruses from Mexico. J Gen Virol 1996;77:1493-1504.
48. Ge J, Deng G, Wen Z, et al. Newcastle disease virus-based live attenuated vaccine completely protects chickens and mice from lethal challenge of homologous and heterologous H5N1 avian influenza viruses. J Virol 2007;81:150-158.
49. Gilbert M, Xiao X, Domenech J, et al. Anatidae migration in the western palearctic and spread of highly pathogenic avian influenza H5N1 virus. Emerg Infect Dis 2006;12: 1650-1656.
50. Grund C, Adbelwhab ESM, Arafa AS, et al. Highly pathogenic avian influenza virus H5N1 from Egypt escapes vaccine-induced immunity but confers clinical protection against a heterologous clade 2.2.1 Egyptian isolate. Vaccine 2011;29:5567-5573.
51. Guan Y, Peiris JSM, Lipatov AS, et al. Emergence of multiple genotypes of H5N1 avian influenza viruses in Hong Kong SAR. PNAS 2002;99:8950-8955.
52. Gutierrez RA, Naughtin MJ, HormSV, et al.A(H5N1) virus evolution in South East Asia. Viruses 2009;1:335-361.
53. Hadifar F, Ignjatovic J, Tarigan S, et al. Multimeric recombinant M2e protein-based ELISA: a significant improvement in differentiating avian influenza infected chickens from vaccinated ones. PLoS One 2014;9:e108420.
54. Hatta M, Gao P, Halfmann P, et al. Molecular basis for high virulence of Hong Kong H5N1 influenza A viruses. Science 2001;293:1840-1842.
55. Heinen PP, de Boer-Luijtze EA, and Bianchi ATJ. Respiratory and systemic humoral and cellular immune responses of pigs to a heterosubtypic influenza A virus infection. J Gen Virol 2001;82:2697-2707.
56. Hemmatzadeh F, Sumarningsih S, Tarigan S, et al. Recombinant M2e protein-based ELISA: a novel and inexpensive approach for differentiating avian Influenza infected chickens from vaccinated ones. PloS ONE 2013;8:e56801.
57. Hoffmann E, Krauss S, Perez DR, et al. Eight-plasmid system for rapid generation of influenza virus vaccines. Vaccine 2002;20:3165-3170.
58. Holmes EC, Ghedin E, Miller N, et al. Whole-genome analysis of human influenza A virus reveals multiple persistent lineages and reassortment among recent H3N2 viruses. PLoS Biol 2005;3:1579-1589.
59. Holsinger LJ, and Lamb RA. Influenza virus M2 integral membrane protein is a homotetramer stabilized by formation of disulfide bonds. Virology 1991;183:32-43.
60. Horimoto T, and Kawaoka Y. Reverse genetics provide direct evidence for a correlation of hemagglutinin cleavability and virulence of an avian Influenza A virus. J Virol 1994;68:3120-3128.
61. Horimoto T, Nakayama K, Smeekens SP, et al. Proprotein-processing endoproteases PC6 and furin both activate hemagglutinin of virulent avian influenza viruses. J Virol 1994;68:6074-6078.
62. Horimoto T, Rivera E, Pearson J, et al. Origin and molecular changes associated with emergence of a highly pathogenic H5N2 influenza virus in Mexico. Virology 1995;213:223-230.
63. Ito T, Gorman OT, Kawaoka Y, et al. Evolutionary analysis of the influenza A virus M gene with comparison of the M1 and M2 proteins. J Virol 1991;65:5491-5498.
64. Jagger BW, Wise HM, Kash JC, et al. An overlapping protein-coding region in influenza A virus segment 3 modulates the host response. Science 2012;337:199-204.
65. Jiao P, Tian G, Li Y, et al. A single amino acid substitution in the NS1 protein changes the pathogenicity of H5N1 avian influenza viruses in mice. J Virol 2008;82:1146-1154.
66. Kawaoka Y, Naeve CW, and Webster RG. Is virulence of H5N2 influenza viruses in chickens associated with loss of carbohydrate from the hemagglutinin? Virology 1984;139: 303-316.
67. Khatchikian D, Orlich M, and Rott R. Increased viral pathogenicity after insertion of a 28S ribosomal RNA sequence into the haemagglutinin gene of an influenza virus. Nature 1989;340:156-157.
68. Khurana S, Sasono P, Fox A, et al. H5N1-Serodetect EIA and Rapid test: a novel differential diagnostic assay for serodiagnosis of H5N1 infections and surveillance. J Virol 2011;85:12455-12463.
69. Khurana S, Suguitan AL, Rivera Y, et al. Antigenic fingerprinting of H5N1 avian influenza using convalescent sera and monoclonal antibodies reveals potential vaccine and diagnostic targets. PLoS Med 2009;6:e1000049.
70. Kim MC, Choi JG, Kwon JS, et al. Field application of the H9M2e ELISA for differentiation of H9N2 AIV-infected chickens from vaccinated chickens. Clin Vaccine Immunol 2010;17:1977-1984.
71. Kim SH, Paldurai A, Xiao S, et al. Modified Newcastle disease virus vectors expressing the H5 hemagglutinin induce enhanced protection against highly pathogenic H5N1 avian influenza virus in chickens. Vaccine 2014;32:4428-4435.
72. Klenk HD, and Garten W. Host cell proteases controlling virus pathogenicity. Trends Microbiol 1994;2:39-43.
73. Klenk HD, Rott R, Orlich M, et al. Activation of Influenza A viruses by trypsin treatment. Virology 1975;68:426-439.
74. Kwon JS, Kim MC, Jeong OM, et al. Novel use of a N2-specific enzyme-linked immunosorbent assay for differentiation of infected from vaccinated animals (DIVA)-based identification of avian influenza. Vaccine 2009;27:3189-3194.
75. Lamb RA, and Choppin PW. Identification of a second protein (M2) encoded by RNA segment 7 of influenza virus. Virology 1981;112:729-737.
76. Lamb RA, and Choppin PW. Segment 8 of the influenza virus genome is unique in coding for two polypeptides. Proc Natl Acad Sci USA 1979;76:4908-4912.
77. Lamb RA, and Krug RM. Orthomyxoviridae: the viruses and their replication. In: Knipe DMand Howley PM, eds. Fields Virology Vol I. 4th ed. Philadelphia: Lippincott Williams &Wilkins, 2001:1487-1531.
78. Lamb RA, and Lai CJ. Sequence of interrupted and uninterrupted mRNAs and clones DNA coding for the two overlapping nonstructural proteins of influenza virus. Cell 1980;21:475-485.
79. Lamb RA, Lai CJ, and Choppin PW. Sequences of mRNAs derived from genome RNA segment 7 of influenza virus: colinear and interrupted mRNAs code for overlapping proteins. Proc Natl Acad Sci USA 1981;78:4170-4174.
80. Lamb RA, Zabedee SL, and Richardson CD. Influenza virus M2 protein is an integral membrane protein expressed on the expressed-cell surface. Cell 1985;40:627-633.
81. Lambrecht B, Steensels M, Van Borm S, et al. Development of an M2e-specific enzyme-linked immunosorbent assay for differentiating infected from vaccinated animals. Avian Dis 2007;51:221-226.
82. Lazarowitz SG, and Choppin PW. Enhancement of the infectivity of influenza A and B viruses by proteolytic cleavage of the hemagglutinin polypeptide. Virology 1975; 68:440-454.
83. Lazarowitz SG, Compans RW, and Choppin PW. Proteolytic cleavage of the hemagglutinin polypeptide of influenza virus. Function of the uncleaved polypeptide HA. Virology 1973;52:199-212.
84. This reference has been deleted.
85. Lee CW, Senne DA, and Suarez DL. Effect of vaccine use in the evolution of Mexican lineage H5N2 avian influenza virus. J Virol 2004;78:8372-8381.
86. Lee CW, Senne DA, and Suarez DL. Generation of reassortant influenza vaccines by reverse genetics that allows utilization of a DIVA (differentiating infected from vaccinated animals) strategy for the control of avian influenza. Vaccine 2004;22:3175-3181.
87. Lee CW, and Suarez DL. Avian influenza virus: prospects for prevention and control by vaccination. Anim Health Res Rev 2005;6:1-15.
88. Lee DH, Park JK, Lee YN, et al. H9N2 avian influenza virus-like particle vaccine provides protective immunity and a strategy for the differentiation of infected from vaccinated animals. Vaccine 2011;29:4003-4007.
89. Li C, Ping J, Jing B, et al. H5N1 influenza marker vaccine for serological differentiation between vaccinated and infected chickens. Biochem Biophys Res Commun 2008; 372:293-297.
90. Li KS, Guan Y, Wang J, et al. Genesis of a highly pathogenic and potentially pandemic H5N1 influenza virus in eastern Asia. Nature 2004;430:209-213.
91. Li Y, Reddy K, Reid SM, et al. Recombinant herpesvirus of turkeys as a vector-based vaccine against highly pathogenic H7N1 avian influenza and Marek's disease. Vaccine 2011;29:8257-8266.
92. Liu J, Xiao H, Lei F, et al. Highly pathogenic H5N1 influenza virus infection in migratory birds. Science 2005;309:1206.
93. Long JX, Peng DX, Liu YL, et al. Virulence of H5N1 avian influenza virus enhanced by a 15-nucleotide deletion in the viral nonstructural gene. Virus Genes 2008;36:471-478.
94. Lozano-Dubernard B, Soto-Priante E, Sarfati-Mizrahi D, et al. Protection and differentiation of infected from vaccinated animals by an inactivated recombinant Newcastle Disease virus/Avian Influenza H5 vaccine. Avian Dis 2010;54:242-245.
95. Maeda T, and Ohnishi S. Activation of Influenza virus by acidic media causes hemolysis and fusion of erythrocytes. FEBS Lett 1980;122:283-287.
96. Marangon S, Cecchinato M, and Capua I. Use of vaccination in avian influenza control and eradication. Zoonoses Public Health 2008;55:65-72.
97. Marinova-Petkova A, Feeroz MM, Alam SMR, et al. Multiple introductions of highly pathogenic avian influenza H5N1 viruses into Bangladesh. Emerg Microbes Infect 2014;3:e11.
98. McCown MF, and Pekosz A. The influenza A virus M2 cytoplasmic tail is required for infectious virus production and efficient genome packaging. J Virol 2005;79:3595-3605.
99. Munier S, Larcher T, Cormier-Aline F, et al. A genetically engineered waterfowl influenza virus with a deletion in the stalk of the neuraminidase has increased virulence for chickens. J Virol 2010;84:940-952.
100. Munster VJ, Bass C, Lexmond P, et al. Spatial, temporal, and species variation in prevalence of influenza A viruses in wild migratory birds. PLoS Pathogen 2007;3:e61.
101. Neirynck S, Deroo T, Saelens X, et al. A universal influenza A vaccine based on the extracellular domain of the M2 protein. Nat Med 1999;5:1157-1163.
102. Neitzert E, Beck E, de Mello PA, et al. Expression of the Aphthovirus RNA polymerase gene in Escherichia coli and its use together with other bioengineered nonstructural antigens in detection of late persistent infections. Virology 1991;184:799-804.
103. Nelson MI, and Holmes EC. The evolution of epidemic influenza. Nature 2007;8:196-205.
104. Neumann G, and Kawaoka Y. Reverse genetics of Influenza virus. Virology 2001;287:243-250.
105. Nobusawa E, Aoyama T, Kato H, et al. Comparison of complete amino acid sequences and receptor-binding properties among 13 serotypes of hemagglutinins of Influenza A viruses. Virology 1991;182:475-485.
106. OIE. Avian Influenza OIE Terrestrial Manual. Paris, France: TheWorld Organization for Animal Health (OIE) 2014:1-23. Available at www.oie.int/international-standard-setting/terres trialmanual/access-online
107. Okuno Y, Isegawa Y, Sasao, F, et al.Acommonneutralizing epitope conserved between the hemagglutinins of Influenza A virus H1 and H2 strains. J Virol 1993;67:2552-2558.
108. Olsen B,Munster VJ,Wallensten A, et al. Global patterns of influenza A virus in wild birds. Science 2006;312:384-388.
109. Ozaki H, Sugiura T, Sugita S, et al. Detection of antibodies to the nonstructural protein (NS1) of influenza A virus allows distinction between vaccinated and infected horses. Vet Microbiol 2001;82:111-119.
110. Pasick J, Handel K, Robinson J, et al. 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.
111. PerdueML, GarciaM, Senne DA, et al. Virulence-associated sequence duplication at the hemagglutinin cleavage site of avian influenza viruses. Virus Res 1997;49:173-186.
112. Quinlivan M, Zamarin D, Garcia-Sastre A, et al. Attenuation of equine influenza viruses through truncations of the NS1 protein. J Virol 2005;79:8431-8439.
113. Richt JA, Lekcharoensuk P, Lager KM, et al. Vaccination of pigs against swine influenza viruses by using an NS1-truncated modified live-virus vaccine. J Virol 2006;80: 11009-11018.
114. Robinson HL, Hunt LA, and Webster RG. Protection against a lethal influenza virus challenge by immunization with a haemagglutinin-expressing plasmid DNA. Vaccine 1993;11:957-960.
115. Rohm C, Horimoto T, Kawaoka Y, et al. Do hemagglutinin genes of highly pathogenic avian influenza viruses constitute unique phylogenetic lineages? Virology 1995;209: 664-670.
116. Rott R. The pathogenic determinant of influenza virus. Vet Microbiol 1992;33:303-310.
117. Rott R, Reinacher M, Orlich M, et al. Cleavability of hemagglutinin determines spread of avian influenza viruses in the chorioallantoic membrane of chicken embryo. Arch Virol 1980;65:123-133.
118. Saelens X, Vanlandschoot P, Martinet W, et al. Protection of mice against a lethal influenza virus challenge after immunization with yeast-derived secreted influenza virus hemagglutinin. Eur J Biochem 1999;260:166-175.
119. Senne DA, Panigrahy B, Kawaoka Y, et al. Survey of the hemagglutinin (HA) cleavage site sequence of H5 and H7 avian influenza viruses: amino acid sequence at the HA cleavage site as a marker of pathogenicity potential. Avian Dis 1996;40:425-437.
120. Shimizu K, Handa H, Nakada S, et al. Regulation of influenza virus RNA polymerase activity by cellular and viral factors. Nucleic Acids Res 1994;22:5047-5053.
121. Shortridge KF, Zhou NN, Guan Y, et al. Characterization of avian H5N1 influenza viruses from poultry in Hong Kong. Virology 1998;252:331-342.
122. Sims LD, Ellis TM, Liu KK, et al. Avian influenza in Hong Kong 1997-2002. Avian Dis 2003;47:832-838.
123. Skehel JJ. Polypeptide synthesis in influenza virusinfected cells. Virology 1972;49:23-36.
124. Skehel JJ, Bayley PM, Brown EB, et al. Changes in the conformation of influenza virus hemagglutinin at the pH optimum of virus-mediated membrane fusion. Proc Natl Acad Sci USA 1982;79:968-972.
125. Skehel JJ, and Waterfield MD. Studies on the primary structure of the Influenza virus hemagglutinin. Proc Natl Acad Sci USA 1975;72:93-97.
126. Skehel JJ, and Wiley DC. Receptor binding and membrane fusion in virus entry: the Influenza hemagglutinin. Annu Rev Biochem 2000;69:531-569.
127. Smith GJD, Fan XH, Wang J, et al. Emergence and predominance of an H5N1 influenza variant in China. PNAS 2006;103:16936-16941.
128. Soleimani E, Marandi MV, Hashemi-Soteh MB, et al. The cloning of non-structural-1 (NS1) gene of H9N2 subtype of avian influenza virus in pGEX-4T-1 and pMAL-c2X plasmids and expression in Escherichia coli DH5 alpha strain. Adv Biosci Biotechnol 2012;3:283-289.
129. Stanekova Z, Mucha V, Sladkova T, et al. Epitope specificity of anti-HA2 antibodies induced in humans during influenza infection. Influenza Other Respir Viruses 2012;6: 389-395.
130. Stech O, Veits J, Weber S, et al. Acquisition of a polybasic hemagglutinin cleavage site by a low-pathogenic avian influenza virus is not sufficient for immediate transformation into a highly pathogenic strain. J Virol 2009;83:5864-5868.
131. Stieneke-Grober A, Vey M, Angliker H, et al. Influenza virus hemagglutinin with multibasic cleavage site is activated by furin, a substilisin-like endoprotease. EMBO J 1992;11:2407-2414.
132. Suarez DL. Avian influenza: our current understanding. Anim Health Res Rev 2010;11:19-33.
133. Suarez DL. DIVA vaccination strategies for avian influenza virus. Avian Dis 2012;56:836-844.
134. Suarez DL. Overview of avian influenza DIVA test strategies. Biologicals 2005;33:221-226.
135. Suarez DL, and Perdue ML. Multiple alignment comparison of the non-structural genes of influenza A viruses. Virus Res 1998;54:59-69.
136. Suarez DL, Senne DA, Banks J, et al. Recombination resulting in virulence shift in avian influenza outbreak, Chile. Emerg Infect Dis 2004;10:693-699.
137. Sugrue RJ, and Hay AJ. Structural characteristics of the M2 protein of Influenza A viruses: evidence that it forms a tetrameric channel. Virology 1991;180:617-624.
138. Sui J, Hwang WC, Perez S, et al. Structural and functional bases for broad-spectrum neutralization of avian and human influenza A viruses. Nat Struct Mol Biol 2009;16:265-273.
139. SwayneDE. Pathobiology ofH5N2Mexican avian influenza virus infections of chickens. Vet Pathol 1997;34:557-567.
140. Swayne DE. Understanding the complex pathobiology of high pathogenicity avian influenza viruses in birds. Avian Dis 2007;51:242-249.
141. Swayne DE, Beck JR, Perdue ML, et al. Efficacy of vaccines in chickens against highly pathogenic Hong Kong H5N1 avian influenza. Avian Dis 2001;45:355-365.
142. Swayne DE, Garcia M, Beck JR, et al. Protection against diverse highly pathogenic H5 avian influenza viruses in chickens immunized with a recombinant fowlpox vaccine containing an H5 avian influenza hemagglutinin gene insert. Vaccine 2000;18:1088-1095.
143. Swayne DE, and Kapczynski D. Strategies and challenges for eliciting immunity against avian influenza virus in birds. Immunol Rev 2008;225:314-331.
144. Swayne DE, Pavade G, Hamilton K, et al. Assessment of national strategies for control of high-pathogenicity avian influenza and low-pathogenicity notifiable avian influenza in poultry, with emphasis on vaccines and vaccination. Rev Sci Tech Off Int Epiz 2011;30:839-870.
145. Swayne DE, and 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.
146. Swayne DE, and Spackman E. Current status and future needs in diagnostics and vaccines for high pathogenicity avian influenza. Dev Biol 2013;135:79-94.
147. Swayne DE, and Suarez DL. Highly pathogenic avian influenza. Rev Sci Tech Off Int Epiz 2000;19:463-482.
148. Swayne DE, Suarez DL, Schultz-Cherry S, et al. Recombinant Paramyxovirus type 1-avian influenza-H7 virus as a vaccine for protection of chickens against influenza and Newcastle disease. Avian Dis 2003;47:1047-1050.
149. Takeyama N, Minari K, Kajihara M, et al. Detection of highly pathogenic avian influenza virus infection in vaccinated chicken flocks by monitoring antibodies against non-structural protein 1 (NS1). Vet Microbiol 2011;147: 283-291.
150. Talon J, Salvatore M, O'Neill RE, et al. Influenza A and B viruses expressing altered NS1 proteins: a vaccine approach. PNAS 2000;97:4309-4314.
151. Tarigan S, Indriani R, Durr PA, et al. Characterization of the M2e antibody response following highly pathogenic H5N1 avian influenza virus infection and reliability of M2e ELISA for identifying infected among vaccinated chickens. Avian Pathol 2015;27:1-40.
152. Taubenberger JK, and Kash JC. Influenza virus evolution, host adaptation, and pandemic formation. Cell Host Microbe 2010;7:440-451.
153. Tian H, Zhou S, Dong L, et al. Avian influenza H5N1 viral and bird migration networks in Asia. PNAS 2015;112:172-177.
154. Tong S, Li Y, Rivailler P, et al. A distinct lineage of influenza A virus from bats. PNAS 2012;109:4269-4274.
155. Tong S, Zhu X, Li Y, et al. Newworld bats harbor diverse influenza A viruses. PLoS Pathogen 2013;9:e1003657.
156. Tumpey TM, Alvarez R, Swayne DE, et al. Diagnostic approach for differentiating infected from vaccinated poultry on the basis of antibodies to NS1, the nonstructural protein of influenza A virus. J Clin Microbiol 2005; 43:676-683.
157. Van Oirschot JT. DIVA vaccines that reduce virus transmission. J Biotechnol 1999;73:195-205.
158. Van Oirschot JT, Rziha HJ, Moonen PJLM, et al. Differentiation of serum antibodies from pigs vaccinated or infected with Aujeszky's disease virus by a competitive enzyme immunoassay. J Gen Virol 1986;67:1179-1182.
159. Vareckova E, Mucha V, and Kostolansky F. HA2 glycopolypeptide of influenza A virus and antiviral immunity. Acta Virol 2013;57:247-256.
160. Veits J, Luschow D, Kindermann K, et al. Deletion of the non-essentialUL0gene of infectious laryngotracheitis (ILT) virus leads to attenuation in chickens, and UL0 mutants expressing influenza virus haemagglutinin (H7) protect against ILT and fowl plague. J Gen Virol 2003;84:3343-3352.
161. Veits J, Wiesner D, Fuchs W, et al. Newcastle disease virus expressing H5 hemagglutinin gene protects chickens against Newcastle disease and avian influenza. PNAS 2006;103:8197-8202.
162. Verhagen JH, van Dijk JG, Vuong O, et al. Migratory birds reinforce local circulation of avian influenza viruses. PLoS One 2014;9:e112366.
163. Villareal C. Avian influenza in Mexico. Rev Sci Tech Off Int Epiz 2009;28:261-265.
164. Wang J, Vijaykrishna D, Duan L, et al. Identification of the progenitors of Indonesian and Vietnamese avian influenza A (H5N1) viruses from southern China. J Virol 2008;82.
165. Wang L, Qin Z, Pantin-Jackwood M, et al. Development of DIVA (differentiation of infected from vaccinated animals) vaccines utilizing heterologous NA and NS1 protein strategies for the control of triple reassortment H3N2 influenza in turkeys. Vaccine 2011;29:7966-7974.
166. Wang L, Suarez DL, Pantin-Jackwood M, et al. Characterization of influenza virus variants with different sizes of the non-structural (NS) genes and their potential as a live influenza vaccine in poultry. Vaccine 2008;26:3580-3586.
167. Watanabe Y, Ibrahim MS, Suzuki Y, et al. The changing nature of avian influenza A virus (H5N1). Trends Microbiol 2011;20:11-20.
168. Webster RG, Bean WJ, Gorman OT, et al. Evolution and ecology of influenza A viruses. Microbiol Rev 1992;56: 152-179.
169. Webster RG, Fynan EF, Santoro JC, et al. Protection of ferrets against influenza challenge with a DNA vaccine to the haemagglutinin. Vaccine 1994;12:1495-1498.
170. Webster RG, Guan Y, Peiris M, et al. Characterization of H5N1 influenza viruses that continue to circulate in geese in Southeastern China. J Virol 2002;76:118-126.
171. Wilson IA, Skehel JJ, and Wiley DC. Structure of the haemagglutinin membrane glycoprotein of influenza virus at 3A resolution. Nature 1981;289:366-373.
172. Wise HM, Foeglein A, Sun J, et al. A complicated message: Identification of a novel PB1-related protein translated from influenza A virus segment 2 mRNA. J Virol 2009;83:8021-8031.
173. Wise HM, Hutchinson EC, Jagger BW, et al. Identification of a novel splice variant form of the influenza A virus M2 ion channel with an antigenically distinct ectodomain. PLoS Pathogen 2012;8:e1002998.
174. Wu R, Chen Q, Zheng L, et al. Generation and evaluation of an H9N1 influenza vaccine derived by reverse genetics that allows utilization of a DIVA strategy for control of H9N2 avian influenza. Arch Virol 2009;154:1203-1210.
175. Xu X, Subbarao K, Cox NJ, et al. Genetic characterization of the pathogenic influenza A/Goose/Guangdong/1/96 (H5N1) virus: similarity of its hemagglutinin gene to those of H5N1 viruses from the 1997 outbreaks in Hong Kong. Virology 1999;261:15-19.
176. Zabedee SL, Richardson CD, and Lamb RA. Characterization of the influenza virus M2 integral membrane protein and expression at the infected-cell surface from cloned cDNA. J Virol 1985;56:502-511.
177. Zhao S, Jin M, Li H, et al. Detection of antibodies to the nonstructural protein (NS1) of avian influenza viruses allows distinction between vaccinated and infected chickens. Avian Dis 2005;49:488-493.
178. Zhirnov OP, and Klenk HD. Alterations in caspase cleavage motifs of NP and M2 proteins attenuate virulence of a highly pathogenic avian influenza virus. Virology 2009;394:57-63.