A mutation in the receptor binding site enhances infectivity of 2009 H1N1 influenza hemagglutinin pseudotypes without changing antigenicity

Virology

Volumn 407, Issue 2, 2010, Pages 374-380

  Wang, Wei ^a   Castelán Vega, Juan A ^a   Jiménez Alberto, Alicia ^a   Vassell, Russell ^a   Ye, Zhiping ^b   Weiss, Carol D ^a  

^a CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

^b CENTER FOR BIOLOGICS EVALUATION AND RESEARCH   (United States)

Author keywords

Hemagglutinin; Hemagglutinin pseudotypes; Influenza A 2009 H1N1 virus; Influenza A antigenicity; Influenza infectivity; Pseudotype neutralization

Indexed keywords

ARGININE; GLUTAMINE; INFLUENZA VIRUS HEMAGGLUTININ; PROTEIN M2; VIRUS SIALIDASE; VIRUS ANTIGEN; VIRUS RECEPTOR;

AMINO ACID SUBSTITUTION; ANTIGENICITY; ARTICLE; BINDING SITE; CHORIOALLANTOIS; CONTROLLED STUDY; EGG; GLYCOSYLATION; INFLUENZA VIRUS A H1N1; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PSEUDOTYPING; RECEPTOR BINDING; VIRUS CELL INTERACTION; VIRUS INFECTIVITY; VIRUS MUTATION; VIRUS NEUTRALIZATION; VIRUS STRAIN; VIRUS VIRULENCE; ANIMAL; BIOLOGY; CHICK EMBRYO; CLASSIFICATION; GENETICS; HUMAN; IMMUNOLOGY; METABOLISM; MUTATION; PATHOGENICITY; PROCEDURES; SERODIAGNOSIS;

ANIMALS; ANTIGENS, VIRAL; BINDING SITES; CHICK EMBRYO; COMPUTATIONAL BIOLOGY; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; HUMANS; INFLUENZA A VIRUS, H1N1 SUBTYPE; MUTATION; NEUTRALIZATION TESTS; RECEPTORS, VIRUS;

EID: 77957688042     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2010.08.027     Document Type: Article

References (42)

1. Alberini I., Del Tordello E., Fasolo A., Temperton N.J., Galli G., Gentile C., Montomoli E., Hilbert A.K., Banzhoff A., Del Giudice G., Donnelly J.J., Rappuoli R., Capecchi B. Pseudoparticle neutralization is a reliable assay to measure immunity and cross-reactivity to H5N1 influenza viruses. Vaccine 2009, 27(43):5998-6003.
2. Bottcher E., Matrosovich T., Beyerle M., Klenk H.D., Garten W., Matrosovich M. Proteolytic activation of influenza viruses by serine proteases TMPRSS2 and HAT from human airway epithelium. J. Virol. 2006, 80(19):9896-9898.
3. Bottcher-Friebertshauser E., Freuer C., Sielaff F., Schmidt S., Eickmann M., Uhlendorff J., Steinmetzer T., Klenk H.D., Garten W. Cleavage of influenza virus hemagglutinin by airway proteases TMPRSS2 and HAT differs in subcellular localization and susceptibility to protease inhibitors. J. Virol. 2010, 84(11):5605-5614.
4. Chen Z., Wang W., Zhou H., Suguitan A.L., Shambaugh C., Kim L., Zhao J., Kemble G., Jin H. Generation of live attenuated novel influenza virus A/California/7/09 (H1N1) vaccines with high yield in embryonated chicken eggs. J. Virol. 2010, 84(1):44-51.
5. Childs R.A., Palma A.S., Wharton S., Matrosovich T., Liu Y., Chai W., Campanero-Rhodes M.A., Zhang Y., Eickmann M., Kiso M., Hay A., Matrosovich M., Feizi T. Receptor-binding specificity of pandemic influenza A (H1N1) 2009 virus determined by carbohydrate microarray. Nat. Biotechnol. 2009, 27(9):797-799.
6. Gamblin S.J., Haire L.F., Russell R.J., Stevens D.J., Xiao B., Ha Y., Vasisht N., Steinhauer D.A., Daniels R.S., Elliot A., Wiley D.C., Skehel J.J. The structure and receptor binding properties of the 1918 influenza hemagglutinin. Science 2004, 303(5665):1838-1842.
7. Garten R.J., Davis C.T., Russell C.A., Shu B., Lindstrom S., Balish A., Sessions W.M., Xu X., Skepner E., Deyde V., Okomo-Adhiambo M., Gubareva L., Barnes J., Smith C.B., Emery S.L., Hillman M.J., Rivailler P., Smagala J., de Graaf M., Burke D.F., Fouchier R.A., Pappas C., Alpuche-Aranda C.M., Lopez-Gatell H., Olivera H., Lopez I., Myers C.A., Faix D., Blair P.J., Yu C., Keene K.M., Dotson P.D., Boxrud D., Sambol A.R., Abid S.H., St George K., Bannerman T., Moore A.L., Stringer D.J., Blevins P., Demmler-Harrison G.J., Ginsberg M., Kriner P., Waterman S., Smole S., Guevara H.F., Belongia E.A., Clark P.A., Beatrice S.T., Donis R., Katz J., Finelli L., Bridges C.B., Shaw M., Jernigan D.B., Uyeki T.M., Smith D.J., Klimov A.I., Cox N.J. Antigenic and genetic characteristics of swine-origin 2009 A(H1N1) influenza viruses circulating in humans. Science 2009, 325(5937):197-201.
8. Guo Y., Rumschlag-Booms E., Wang J., Xiao H., Yu J., Wang J., Guo L., Gao G.F., Cao Y., Caffrey M., Rong L. Analysis of hemagglutinin-mediated entry tropism of H5N1 avian influenza. Virol. J. 2009, 6:39.
9. Humphrey W., Dalke A., Schulten K. VMD: visual molecular dynamics. J. Mol. Graph 1996, 14(1):33-38.
10. Itoh Y., Shinya K., Kiso M., Watanabe T., Sakoda Y., Hatta M., Muramoto Y., Tamura D., Sakai-Tagawa Y., Noda T., Sakabe S., Imai M., Hatta Y., Watanabe S., Li C., Yamada S., Fujii K., Murakami S., Imai H., Kakugawa S., Ito M., Takano R., Iwatsuki-Horimoto K., Shimojima M., Horimoto T., Goto H., Takahashi K., Makino A., Ishigaki H., Nakayama M., Okamatsu M., Takahashi K., Warshauer D., Shult P.A., Saito R., Suzuki H., Furuta Y., Yamashita M., Mitamura K., Nakano K., Nakamura M., Brockman-Schneider R., Mitamura H., Yamazaki M., Sugaya N., Suresh M., Ozawa M., Neumann G., Gern J., Kida H., Ogasawara K., Kawaoka Y. In vitro and in vivo characterization of new swine-origin H1N1 influenza viruses. Nature 2009, 460(7258):1021-1025.
11. Johansson B.E., Bucher D.J., Kilbourne E.D. Purified influenza virus hemagglutinin and neuraminidase are equivalent in stimulation of antibody response but induce contrasting types of immunity to infection. J. Virol. 1989, 63(3):1239-1246.
12. Johansson B.E., Grajower B., Kilbourne E.D. Infection-permissive immunization with influenza virus neuraminidase prevents weight loss in infected mice. Vaccine 1993, 11(10):1037-1039.
13. Kong W.P., Hood C., Yang Z.Y., Wei C.J., Xu L., Garcia-Sastre A., Tumpey T.M., Nabel G.J. Protective immunity to lethal challenge of the 1918 pandemic influenza virus by vaccination. Proc. Natl. Acad. Sci. USA 2006, 103(43):15987-15991.
14. Maines T.R., Jayaraman A., Belser J.A., Wadford D.A., Pappas C., Zeng H., Gustin K.M., Pearce M.B., Viswanathan K., Shriver Z.H., Raman R., Cox N.J., Sasisekharan R., Katz J.M., Tumpey T.M. Transmission and pathogenesis of swine-origin 2009 A(H1N1) influenza viruses in ferrets and mice. Science 2009, 325(5939):484-487.
15. 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(18):8502-8512.
16. McKay T., Patel M., Pickles R.J., Johnson L.G., Olsen J.C. Influenza M2 envelope protein augments avian influenza hemagglutinin pseudotyping of lentiviral vectors. Gene Ther. 2006, 13(8):715-724.
17. Munster V.J., de Wit E., van den Brand J.M., Herfst S., Schrauwen E.J., Bestebroer T.M., van de Vijver D., Boucher C.A., Koopmans M., Rimmelzwaan G.F., Kuiken T., Osterhaus A.D., Fouchier R.A. Pathogenesis and transmission of swine-origin 2009 A(H1N1) influenza virus in ferrets. Science 2009, 325(5939):481-483.
18. Naldini L., Blomer U., Gallay P., Ory D., Mulligan R., Gage F.H., Verma I.M., Trono D. In vivo gene delivery and stable transduction of nondividing cells by a lentiviral vector. Science 1996, 272(5259):263-267.
19. Nefkens I., Garcia J.M., Ling C.S., Lagarde N., Nicholls J., Tang D.J., Peiris M., Buchy P., Altmeyer R. Hemagglutinin pseudotyped lentiviral particles: characterization of a new method for avian H5N1 influenza sero-diagnosis. J. Clin. Virol. 2007, 39(1):27-33.
20. Phillips J.C., Braun R., Wang W., Gumbart J., Tajkhorshid E., Villa E., Chipot C., Skeel R.D., Kale L., Schulten K. Scalable molecular dynamics with NAMD. J. Comput. Chem. 2005, 26(16):1781-1802.
21. Potdar V.A., Chadha M.S., Jadhav S.M., Mullick J., Cherian S.S., Mishra A.C. Genetic characterization of the influenza A pandemic (H1N1) 2009 virus isolates from India. PLoS ONE 2010, 5(3):e9693.
22. Qiu M., Fang F., Chen Y., Wang H., Chen Q., Chang H., Wang F., Wang H., Zhang R., Chen Z. Protection against avian influenza H9N2 virus challenge by immunization with hemagglutinin- or neuraminidase-expressing DNA in BALB/c mice. Biochem. Biophys. Res. Commun. 2006, 343(4):1124-1131.
23. Quan F.S., Vunnava A., Compans R.W., Kang S.M. Virus-like particle vaccine protects against 2009 H1N1 pandemic influenza virus in mice. PLoS ONE 2010, 5(2):e9161.
24. Rogers G.N., Paulson J.C., Daniels R.S., Skehel J.J., Wilson I.A., Wiley D.C. Single amino acid substitutions in influenza haemagglutinin change receptor binding specificity. Nature 1983, 304(5921):76-78.
25. Rossman J.S., Jing X., Leser G.P., Balannik V., Pinto L.H., Lamb R.A. Influenza virus m2 ion channel protein is necessary for filamentous virion formation. J. Virol. 2010, 84(10):5078-5088.
26. Skehel J.J., Wiley D.C. Receptor binding and membrane fusion in virus entry: the influenza hemagglutinin. Annu. Rev. Biochem. 2000, 69:531-569.
27. Soundararajan V., Tharakaraman K., Raman R., Raguram S., Shriver Z., Sasisekharan V., Sasisekharan R. Extrapolating from sequence-the 2009 H1N1 'swine' influenza virus. Nat. Biotechnol. 2009, 27(6):510-513.
28. Steinhauer D.A., Wharton S.A., Skehel J.J., Wiley D.C., Hay A.J. Amantadine selection of a mutant influenza virus containing an acid-stable hemagglutinin glycoprotein: evidence for virus-specific regulation of the pH of glycoprotein transport vesicles. Proc. Natl. Acad. Sci. USA 1991, 88(24):11525-11529.
29. Stevens J., Chen L.M., Carney P.J., Garten R., Foust A., Le J., Pokorny B.A., Manojkumar R., Silverman J., Devis R., Rhea K., Xu X., Bucher D.J., Paulson J., Cox N.J., Klimov A., Donis R.O. Receptor specificity of influenza A H3N2 viruses isolated in mammalian cells and embryonated chicken eggs. J. Virol. 2010, 84(16):8287-8299.
30. Su Y., Yang H.Y., Zhang B.J., Jia H.L., Tien P. Analysis of a point mutation in H5N1 avian influenza virus hemagglutinin in relation to virus entry into live mammalian cells. Arch. Virol. 2008, 153(12):2253-2261.
31. Su B., Wurtzer S., Rameix-Welti M.A., Dwyer D., van der Werf S., Naffakh N., Clavel F., Labrosse B. Enhancement of the influenza A hemagglutinin (HA)-mediated cell-cell fusion and virus entry by the viral neuraminidase (NA). PLoS ONE 2009, 4(12):e8495.
32. Subbarao K., Murphy B.R., Fauci A.S. Development of effective vaccines against pandemic influenza. Immunity 2006, 24(1):5-9.
33. Temperton N.J., Hoschler K., Major D., Nicolson C., Manvell R., Hien V.M., Ha D.Q., Jong M.D., Zambon M., Takeuchi Y., Weiss R.A. A sensitive retroviral pseodotype assay for influenza H5N1-neutralizing antibodies. Influenza Other Respir. Viruses 2007, 1(3):105-112.
34. Wang W., Butler E.N., Veguilla V., Vassell R., Thomas J.T., Moos M., Ye Z., Hancock K., Weiss C.D. Establishment of retroviral pseudotypes with influenza hemagglutinins from H1, H3, and H5 subtypes for sensitive and specific detection of neutralizing antibodies. J. Virol. Methods 2008, 153(2):111-119.
35. Wang W., Xie H., Ye Z., Vassell R., Weiss C.D. Characterization of lentiviral pseudotypes with influenza H5N1 hemagglutinin and their performance in neutralization assays. J. Virol. Methods 2010, 165(2):305-310.
36. WHO Characteristics of the emergent influenza A (H1N1) viruses and recommendations for vaccine development http://www.who.int/csr/resources/publications/swineflu/vaccine_recommendations/en/.
37. WHO Gene sequences of the reassortant candidate vaccine viruses for the novel influenza A (H1N1) http://www.who.int/csr/resources/publications/swineflu/gene_sequences_20090605_en.pdf.
38. WHO World now at the start of 2009 influenza pandemic http://www.who.int/mediacentre/news/statements/2009/h1n1_pandemic_phase6_20090611/en/index.html.
39. Xu Q., Wang W., Cheng X., Zengel J., Jin H. Influenza H1N1 A/Solomon Island/3/06 virus receptor binding specificity correlates with virus pathogenicity, antigenicity, and immunogenicity in ferrets. J. Virol. 2010, 84(10):4936-4945.
40. Xu R., Ekiert D.C., Krause J.C., Hai R., Crowe J.E., Wilson I.A. Structural basis of preexisting immunity to the 2009 H1N1 pandemic influenza virus. Science 2010, 328(5976):357-360.
41. Yang H., Carney P., Stevens J. Structure and Receptor binding properties of a pandemic H1N1 virus hemagglutinin. PLoS Curr Influenza 2010, RRN1152.
42. Zufferey R., Nagy D., Mandel R.J., Naldini L., Trono D. Multiply attenuated lentiviral vector achieves efficient gene delivery in vivo. Nat. Biotechnol. 1997, 15(9):871-875.