Molecular adaptation of an H7N3 wild duck influenza virus following experimental multiple passages in quail and turkey

Virology

Volumn 408, Issue 2, 2010, Pages 167-173

  Giannecchini, Simone ^a   Clausi, Valeria ^a   Di Trani, Livia ^b   Falcone, Emiliana ^b   Terregino, Calogero ^c   Toffan, Anna ^c   Cilloni, Filippo ^c   Matrosovich, Mikhail ^d   Gambaryan, Alexandra S ^e   Bovin, Nicolai V ^f   Delogu, Mauro ^g   Capua, Ilaria ^c   Donatelli, Isabella ^b   Azzi, Alberta ^a  

^a UNIVERSITY OF FLORENCE   (Italy)

^b ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^c OIE/FAO National Reference Laboratory for Newcastle Disease   (Italy)

^d PHILIPPS UNIVERSITY MARBURG   (Germany)

^e CHUMAKOV INSTITUTE OF POLIOMYELITIS AND VIRAL ENCEPHALITIDES   (Russian Federation)

^f SHEMYAKIN OVCHINNIKOV INSTITUTE OF BIOORGANIC CHEMISTRY   (Russian Federation)

^g UNIVERSITY OF BOLOGNA   (Italy)

Author keywords

Avian influenza virus; H7N3; HA glycosylation site; HA receptor binding activity; Interspecies transmission; NA stalk deletion; Quail; Turkey; Virus adaptation; Wild birds

Indexed keywords

HEMAGGLUTININ; SIALIDASE; VIRUS PROTEIN;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DUCK; ENZYME ACTIVITY; EVOLUTIONARY ADAPTATION; GENE DELETION; GENE SEQUENCE; GENOTYPE PHENOTYPE CORRELATION; GLYCOSYLATION; INFLUENZA VIRUS A; INFLUENZA VIRUS A H7N3; MOLECULAR MECHANICS; NONHUMAN; PRIORITY JOURNAL; QUAIL; RECEPTOR BINDING; SEQUENCE ANALYSIS; TURKEY (BIRD); VIRUS TRANSMISSION; WILD ANIMAL;

ADAPTATION, BIOLOGICAL; AMINO ACID SEQUENCE; ANIMALS; CARBOHYDRATE SEQUENCE; COTURNIX; DUCKS; GENES, VIRAL; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; INFLUENZA A VIRUS, H7N3 SUBTYPE; INFLUENZA IN BIRDS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; NEURAMINIDASE; OLIGOSACCHARIDES; RECEPTORS, VIRUS; SEQUENCE HOMOLOGY, AMINO ACID; SPECIES SPECIFICITY; TURKEYS; VIRULENCE;

AVES; AVIAN INFLUENZA VIRUS; ORTHOMYXOVIRIDAE; PHASIANIDAE;

EID: 78149406883     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2010.09.011     Document Type: Article

References (51)

1. Aamir U.B., Naeem K., Ahmed Z., Obert C.A., Franks J., Krauss S., Seiler P., Webster R.G. Zoonotic potential of highly pathogenic avian H7N3 influenza viruses from Pakistan. Virology 2009, 390:212-220.
2. Alexander D.J. A review of avian influenza in different bird species. Vet. Microbiol. 2000, 74:3-13.
3. Baigent S.J., McCauley J.W. Glycosylation of haemagglutinin and stalk-length of neuraminidase combine to regulate the growth of avian influenza viruses in tissue culture. Virus Res. 2001, 79:177-185.
4. Banks J., Speidel E.S., Moore E., Plowright L., Piccirillo A., Capua I., Cordioli P., Fioretti A., Alexander D.J. 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.
5. Belser J.A., Blixt O., Chen L.M., Pappas C., Maines T.R., Van Hoeven N., Donis R., Busch J., McBride R., Paulson J.C., Katz J.M., Tumpey T.M. Contemporary North American influenza H7 viruses possess human receptor specificity: implications for virus transmissibility. Proc. Natl Acad. Sci. USA 2008, 105:7558-7563.
6. Bovin N.V. Polyacrylamide-based glycoconjugates as tools in glycobiology. Glycoconj. J. 1998, 15:431-446.
7. Bovin N.V., Korchagina E.Y., Zemlyanukhina T.V., Byramova N.E., Galanina O.E., Zemlyakov A.E., Ivanov A.E., Zubov V.P., Mochalova L.V. Synthesis of polymeric neoglycoconjugates based on N-substituted polyacrylamides. Glycoconj. J. 1993, 10:142-151.
8. Cameron K.R., Gregory V., Banks J., Brown I.H., Alexander D.J., Hay A.J., Lin Y.P. H9N2 subtype influenza A viruses in poultry in Pakistan are closely related to the H9N2 viruses responsible for human infection in Hong Kong. Virology 2000, 278:36-41.
9. Campitelli L., Mogavero E., De Marco M.A., Delogu M., Puzelli S., Frezza F., Facchini M., Chiapponi C., Foni E., Cordioli P., Webby R., Barigazzi G., Webster R.G., Donatelli I. Interspecies transmission of an H7N3 influenza virus from wild birds to intensively reared domestic poultry in Italy. Virology 2004, 323:24-36.
10. Campitelli L., Di Martino A., Spagnolo D., Smith G.J., Di Trani L., Facchini M., De Marco M.A., Foni E., Chiapponi C., Martin A.M., 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.
11. Capua I., Alexander D.J. Avian influenza: recent developments. Avian Pathol. 2004, 33:393-404.
12. Capua I., Marangon S., Cordioli P., Bonfanti L., Santucci U. H7N3 avian influenza in Italy. Vet. Rec. 2002, 151:743-744.
13. Castrucci M.R., Kawaoka Y. Biologic importance of neuraminidase stalk length in influenza A virus. J. Virol. 1993, 67:759-764.
14. Chen G.-W., Chang S.-C., Mok C.-K., Lo Y.-L., Kung Y.-N., Huang J.H., Shih Y.-H., Wang J.-Y., Chiang C., Chen C.-J., Shih S.-R. Genomic signatures of human versus avian influenza A viruses. Emerg. Infect. Dis. 2006, 12:1353-1360.
15. Cilloni F., Toffan A., Giannecchini S., Clausi V., Azzi A., Capua I., Terregino C. Increased pathogenicity and shedding in chickens of a wild bird origin LPAI virus of the H7N3 subtype following multiple in vivo passages in quail and turkey. Avian Dis. 2010, 54:555-557.
16. de Wit E., Munster V.J., van Riel D., Beyer W.E., Rimmelzwaan G.F., Kuiken T., Osterhaus A.D., Fouchier R.A. Molecular determinants of adaptation of highly pathogenic avian influenza H7N7 viruses to efficient replication in the human host. J. Virol. 2010, 84:1597-1606.
17. Gambaryan A.S., Matrosovich M.N. A solid-phase enzyme-linked assay for influenza virus receptor-binding activity. J. Virol. Methods 1992, 39:111-123.
18. Gambaryan A., Webster R., Matrosovich M. Differences between influenza virus receptors on target cells of duck and chicken. Arch. Virol. 2002, 147:1197-1208.
19. Gambaryan A.S., Tuzikov A.B., Pazynina G.V., Desheva J.A., Bovin N.V., Matrosovich M.N., Klimov A.I. 6-sulfo sialyl Lewis X is the common receptor determinant recognized by H5, H6, H7 and H9 influenza viruses of terrestrial poultry. Virol. J. 2008, 5:85.
20. Giannecchini S., Campitelli L., Calzoletti L., De Marco M.A., Azzi A., Donatelli I. Comparison of in vitro replication features of H7N3 influenza viruses from wild ducks and turkeys: potential implications for interspecies transmission. J. Gen. Virol. 2006, 87:171-175.
21. Guan Y., Shortridge K.F., Kraus S., Webster R.G. 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.
22. Guo C.T., Takahashi N., Yagi H., Kato K., Takahashi T., Yi S.Q., Chen Y., Ito T., Otsuki K., Kida H., Kawaoka Y., Hidari K.I., Miyamoto D., Suzuki T., Suzuki Y. The quail and chicken intestine have sialyl-galactose sugar chains responsible for the binding of influenza A viruses to human type receptors. Glycobiology 2007, 17:713-724.
23. Horimoto T., Kawaoka Y. Pandemic threat posed by avian influenza A viruses. Clin. Microbiol. Rev. 2001, 14:129-149.
24. Hossain M.J., Hickman D., Perez D.R. Evidence of expanded host range and mammalian-associated genetic changes in a duck H9N2 influenza virus following adaptation in quail and chickens. PLoS ONE 2008, 3:e3170.
25. Kurtz J., Manvell R.J., Banks J. Avian influenza virus isolated from a woman with conjunctivitis. Lancet 1996, 348:901-902.
26. Lin A.H., Cannon P.M. Use of pseudotyped retroviral vectors to analyze the receptor-binding pocket of hemagglutinin from a pathogenic avian influenza A virus (H7 subtype). Virus Res. 2002, 83:43-56.
27. Liu J., Stevens D.J., Haire L.F., Walker P.A., Coombs P.J., Russell R.J., Gamblin S.J., Skehel J.J. Structures of receptor complexes formed by hemagglutinins from the Asian Influenza pandemic of 1957. Proc. Natl Acad. Sci. USA 2009, 106:17175-17180.
28. Maines T.R., Szretter K.J., Perrone L., Belser J.A., Bright R.A., Zeng H., Tumpey T.M., Katz J.M. Pathogenesis of emerging avian influenza viruses in mammals and the host innate immune response. Immunol. Rev. 2008, 225:68-84.
29. Makarova N.V., Ozaki H., Kida H., Webster R.G., Perez D.R. Replication and transmission of influenza viruses in Japanese quail. Virology 2003, 310:8-15.
30. Matrosovich M.N., Gambaryan A.S., Tuzikov A.B., Byramova N.E., Mochalova L.V., Golbraikh A.A., Shenderovich M.D., Finne J., Bovin N.V. Probing of the receptor-binding sites of the H1 and H3 influenza A and influenza B virus hemagglutinins by synthetic and natural sialosides. Virology 1993, 196:111-121.
31. Matrosovich M.N., Gambaryan A.S., Teneberg S., Piskarev V.E., Yamnikova S.S., Lvov D.K., Robertson J.S., Karlsson K.A. Avian influenza A viruses differ from human viruses by recognition of sialyloligosaccharides and gangliosides and by a higher conservation of the HA receptor-binding site. Virology 1997, 233:224-234.
32. Matrosovich M., Zhou N., Kawaoka Y., Webster R. The surface glycoproteins of H5 influenza viruses isolated from humans, chickens, and wild aquatic birds have distinguishable properties. J. Virol. 1999, 73:1146-1155.
33. Matrosovich M., Tuzikov A., Bovin N., Gambaryan A., Klimov A., Castrucci M.R., Donatelli I., Kawaoka Y. Early alterations of the receptor-binding properties of H1, H2, and H3 avian influenza virus hemagglutinins after their introduction into mammals. J. Virol. 2000, 74:8502-8512.
34. Matsuoka Y., Swayne D.E., Thomas C., Rameix-Welti M.A., Naffakh N., Warnes C., Altholtz M., Donis R., Subbarao K. Neuraminidase stalk length and additional glycosylation of the hemagglutinin influence the virulence of influenza H5N1 viruses for mice. J. Virol. 2009, 83:4704-4708.
35. Mitnaul L.J., Matrosovich M.N., Castrucci M.R., Tuzikov A.B., Bovin N.V., Kobasa D., Kawaoka Y. Balanced hemagglutinin and neuraminidase activities are critical for efficient replication of influenza A virus. J. Virol. 2000, 74:6015-6020.
36. Morgan O., Kuhne M., Nair P., Verlander N.Q., Preece R., McDouglas M., Zambon M., Reacher M. Personal protective equipment and risk for avian influenza (H7N3). Emerg. Infect. Dis. 2009, 15:59-62.
37. Palese P., Shaw M.L. Orthomyxoviridae: the viruses and their replication. Field Virology 2007, 1647-1690. Lippincott-Williams & Wilkins, Philadelphia, PA. 5th ed. D.M. Knipe, P.M. Howley (Eds.).
38. Perez D.R., Lim W., Seiler J.P., Yi G., Peiris M., Shortridge K.F., Webster R.G. Role of quail in the interspecies transmission of H9 influenza A viruses: molecular changes on HA that correspond to adaptation from ducks to chickens. J. Virol. 2003, 77:3148-3156.
39. Perez D.R., Webby R.J., Hoffmann E., Webster R.G. Land-based birds as potential disseminators of avian mammalian reassortant influenza A viruses. Avian Dis. 2003, 47:1114-1117.
40. Potier M., Mameli L., Belisle M., Dallaire L., Melancon S.B. Fluorometric assay of neuraminidase with a sodium (4-methylumbelliferyl-alpha-d-N-acetylneuraminate) substrate. Anal. Biochem. 1979, 94:287-296.
41. Puzelli S., Di Trani L., Fabiani C., Campitelli L., De Marco M.A., Capua I., Aguilera J.F., Zambon M., Donatelli I. Serological analysis of humans exposed to avian H7 influenza viruses in Italy between 1999 and 2003. J. Infect. Dis. 2005, 192:1318-1322.
42. Reed L.J., Müench H.A. A simple method for estimating fifty percent end points. Am. J. Hyg. 1938, 27:493-497.
43. Russell R.J., Gamblin S.J., Haire L.F., Stevens D.J., Xiao B., Ha Y., Skehel J.J. H1 and H7 influenza haemagglutinin structures extend a structural classification of haemagglutinin subtypes. Virology 2004, 325:287-296.
44. Russell R.J., Stevens D.J., Haire L.F., Gamblin S.J., Skehel J.J. Avian and human receptor binding by hemagglutinins of influenza A viruses. Glycoconj. J. 2006, 23:85-92.
45. 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. Origins and evolutionary genomics of the 2009 swine-origin H1N1 influenza A epidemic. Nature 2009, 459:1122-1125.
46. Sorrell E.M., Perez D.R. Adaptation of influenza A/Mallard/Potsdam/178-4/83 H2N2 virus in Japanese quail leads to infection and transmission in chickens. Avian Dis. 2007, 51:264-268.
47. Spackman E., Senne D.A., Myers T.J., Bulaga L.L., Garber L.P., Perdue M.L., Lohman K., Daum L.T., Suarez D.L. Development of a real-time reverse transcriptase PCR assay for type A influenza virus and the avian H5 and H7 hemagglutinin subtypes. J. Clin. Microbiol. 2002, 40:3256-3260.
48. Suarez D.L., 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.
49. Wan H., Perez D.R. Quail carry sialic acid receptors compatible with binding of avian and human influenza viruses. Virology 2006, 346:278-286.
50. Wasilenko J.L., Lee C.W., Sarmento L., Spackman E., Kapczynski D.R., Suarez D.L., Pantin-Jackwood M.J. NP, PB1, and PB2 viral genes contribute to altered replication of H5N1 avian influenza viruses in chickens. J. Virol. 2008, 82:4544-4553.
51. Webster R.G., Bean W.J., Gorman O.T., Chambers T.M., Kawaoka Y. Evolution and ecology of influenza A viruses. Microbiol. Rev. 1992, 56:152-179.