Diverse antigenic site targeting of influenza hemagglutinin in the murine antibody recall response to A(H1N1)pdm09 virus

Virology

Volumn 485, Issue , 2015, Pages 252-262

  Wilson, Jason R ^a   Guo, Zhu ^a   Tzeng, Wen Pin ^a   Garten, Rebecca J ^a   Xiyan, Xu ^a   Blanchard, Elisabeth G ^a   Blanchfield, Kristy ^a   Stevens, James ^a   Katz, Jacqueline M ^a   York, Ian A ^a  

^a NATIONAL CENTER FOR IMMUNIZATION AND RESPIRATORY DISEASES   (United States)

Author keywords

A H1N1 pdm09; Antigenic drift; Antigenic site; Epitope mapping; Influenza; Monoclonal antibody; Virus neutralization

Indexed keywords

INFLUENZA VACCINE; INFLUENZA VIRUS HEMAGGLUTININ; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY 065 C05; MONOCLONAL ANTIBODY 065 D01; MONOCLONAL ANTIBODY 069 A09; MONOCLONAL ANTIBODY 139 22A; MONOCLONAL ANTIBODY 145 C09; MONOCLONAL ANTIBODY 145 D11; MONOCLONAL ANTIBODY 146 B09; MONOCLONAL ANTIBODY 146 C07; MONOCLONAL ANTIBODY 146 D11; UNCLASSIFIED DRUG; EPITOPE; PROTEIN BINDING; RECOMBINANT PROTEIN; VIRUS ANTIBODY; VIRUS ANTIGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY AND IMMUNOGLOBULIN STRUCTURE, FUNCTION AND PRODUCTION; ANTIBODY COMBINING SITE; ANTIBODY RESPONSE; ANTIBODY TITER; ANTIGEN RECOGNITION; ANTIGENIC DRIFT; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; CROSS REACTION; DRUG BINDING; DRUG BINDING SITE; DRUG DETERMINATION; DRUG SCREENING; DRUG TARGETING; EMBRYO; EPITOPE MAPPING; HUMAN; INFLUENZA A (H1N1); INFLUENZA A VIRUS (H1N1); INFLUENZA VACCINATION; LIGHT CHAIN; MEMORY CELL; MOUSE; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; RMAB GENE; VIRUS GENE; VIRUS ISOLATION; VIRUS NEUTRALIZATION; ANIMAL; ANTIGENIC VARIATION; BINDING SITE; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; INFLUENZA; ORTHOMYXOVIRUS INFECTION; PROTEIN CONFORMATION; VIROLOGY;

MURINAE; MUS; TIPULA IRIDESCENT VIRUS;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIBODIES, VIRAL; ANTIGENIC VARIATION; ANTIGENS, VIRAL; BINDING SITES; CROSS REACTIONS; EPITOPE MAPPING; EPITOPES; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; HUMANS; IMMUNOLOGIC MEMORY; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA, HUMAN; MICE; MODELS, MOLECULAR; ORTHOMYXOVIRIDAE INFECTIONS; PROTEIN BINDING; PROTEIN CONFORMATION; RECOMBINANT PROTEINS;

EID: 84940045229     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2015.08.004     Document Type: Article

References (40)

1. Barbey-Martin C., Gigant B., Bizebard T., Calder L.J., Wharton S.A., et al. An antibody that prevents the hemagglutinin low pH fusogenic transition. Virology 2002, 294:70-74.
2. Caton A.J., Brownlee G.G., Yewdell J.W., Gerhard W. The antigenic structure of the influenza virus A/PR/8/34 hemagglutinin (H1 subtype). Cell 1982, 31:417-427.
3. Chen J., Yan B., Chen Q., Yao Y., Wang H., et al. Evaluation of neutralizing efficacy of monoclonal antibodies specific for 2009 pandemic H1N1 influenza A virus in vitro and in vivo. Arch Virol. 2013.
4. Clarke S.H., Huppi K., Ruezinsky D., Staudt L., Gerhard W., et al. Interclonal and intraclonal diversity in the antibody-response to inflienza hemagglutinin. J. Exp. Med. 1985, 161:687-704.
5. Coudeville L., Bailleux F., Riche B., Megas F., Andre P., et al. Relationship between haemagglutination-inhibiting antibody titres and clinical protection against influenza: development and application of a bayesian random-effects model. BMC Med. Res. Methodol. 2010, 10:18.
6. Cox R.J. Correlates of protection to influenza virus, where do we go from here?. Hum. Vaccin. Immunother. 2013, 9:405-408.
7. Garten R.J., Davis C.T., Russell C.A., Shu B., Lindstrom S., et al. Antigenic and genetic characteristics of swine-origin 2009 A(H1N1) influenza viruses circulating in humans. Science 2009, 325:197-201.
8. Hobson D., Curry R.L., Beare A.S., Ward-Gardner A. The role of serum haemagglutination-inhibiting antibody in protection against challenge infection with influenza A2 and B viruses. J. Hyg. (London) 1972, 70:767-777.
9. Hong M., Lee P.S., Hoffman R.M., Zhu X., Krause J.C., et al. Antibody recognition of the pandemic H1N1 Influenza virus hemagglutinin receptor binding site. J. Virol. 2013, 87:12471-12480.
10. Hu W., Chen A., Miao Y., Xia S., Ling Z., et al. Fully human broadly neutralizing monoclonal antibodies against influenza A viruses generated from the memory B cells of a 2009 pandemic H1N1 influenza vaccine recipient. Virology 2013, 435:320-328.
11. Iba Y., Fujii Y., Ohshima N., Sumida T., Kubota-Koketsu R., et al. Conserved neutralizing epitope at globular head of hemagglutinin in H3N2 influenza viruses. J. Virol. 2014, 88:7130-7144.
12. Kaverin N.V., Rudneva I.A., Ilyushina N.A., Lipatov A.S., Krauss S., et al. Structural differences among hemagglutinins of influenza A virus subtypes are reflected in their antigenic architecture: analysis of H9 escape mutants. J. Virol. 2004, 78:240-249.
13. Koel B.F., Burke D.F., Bestebroer T.M., van der Vliet S., Zondag G.C., et al. Substitutions near the receptor binding site determine major antigenic change during influenza virus evolution. Science 2013, 342:976-979.
14. Koel B.F., Mogling R., Chutinimitkul S., Fraaij P.L., Burke D.F., et al. Identification of amino acid substitutions supporting antigenic change of A(H1N1)pdm09 viruses. J. Virol. 2015.
15. Krause J.C., Tsibane T., Tumpey T.M., Huffman C.J., Basler C.F., et al. A broadly neutralizing human monoclonal antibody that recognizes a conserved, novel epitope on the globular head of the influenza H1N1 virus hemagglutinin. J. Virol. 2011, 85:10905-10908.
16. Laeeq S., Smith C.A., Wagner S.D., Thomas D.B. Preferential selection of receptor-binding variants of influenza virus hemagglutinin by the neutralizing antibody repertoire of transgenic mice expressing a human immunoglobulin mu minigene. J. Virol. 1997, 71:2600-2605.
17. Lee P.S., Ohshima N., Stanfield R.L., Yu W., Iba Y., et al. Receptor mimicry by antibody F045-092 facilitates universal binding to the H3 subtype of influenza virus. Nat. Commun. 2014, 5:3614.
18. Matsuzaki Y., Sugawara K., Nakauchi M., Takahashi Y., Onodera T., et al. Epitope mapping of the hemagglutinin molecule of A/(H1N1)pdm09 virus by using monoclonal antibody escape mutants. J. Virol. 2014.
19. McCullers J.A., Huber V.C. Correlates of vaccine protection from influenza and its complications. Hum. Vaccin. Immunother. 2012, 8:34-44.
20. Molinari NA, Ortega-Sanchez IR, Messonnier ML, Thompson WW, Wortley PM, et al. The annual impact of seasonal influenza in the US: measuring disease burden and costs. Vaccine 2007, 25:5086-5096.
21. Patera A.C., Graham C.M., Thomas D.B., Smith C.A. Immunodominance with progenitor B cell diversity in the neutralizing antibody repertoire to influenza infection. Eur. J. Immunol. 1995, 25:1803-1809.
22. Reber A., Katz J. Immunological assessment of influenza vaccines and immune correlates of protection. Expert Rev. Vacc. 2013, 12:519-536.
23. Retamal M., Abed Y., Corbeil J., Boivin G. Epitope mapping of the 2009 pandemic and the A/Brisbane/59/2007 seasonal (H1N1) influenza virus hemagglutinins using monoclonal antibodies and escape mutants. J. Gen. Virol. 2014.
24. Rudneva I., Ignatieva A., Timofeeva T., Shilov A., Kushch A., et al. Escape mutants of pandemic influenza A/H1N1 2009 virus: variations in antigenic specificity and receptor affinity of the hemagglutinin. Virus Res 2012, 166:61-67.
25. Rudneva I.A., Kushch A.A., Masalova O.V., Timofeeva T.A., Klimova R.R., et al. Antigenic epitopes in the hemagglutinin of Qinghai-type influenza H5N1 virus. Viral Immunol. 2010, 23:181-187.
26. Russell C.A., Jones T.C., Barr I.G., Cox N.J., Garten R.J., et al. Influenza vaccine strain selection and recent studies on the global migration of seasonal influenza viruses. Vaccine 2008, 26(Suppl. 4):D31-D34.
27. Staudt L.M., Gerhard W. Generation of antibody diversity in the immune response of BALB/c mice to influenza virus hemagglutinin. I. Significant variation in repertoire expression between individual mice. J. Exp. Med. 1983, 157:687-704.
28. Temoltzin-Palacios F., Thomas D.B. Modulation of immunodominant sites in influenza hemagglutinin compromise antigenic variation and select receptor-binding variant viruses. J. Exp. Med. 1994, 179:1719-1724.
29. Throsby M., van den Brink E., Jongeneelen M., Poon L.L., Alard P., et al. Heterosubtypic neutralizing monoclonal antibodies cross-protective against H5N1 and H1N1 recovered from human IgM+ memory B cells. PLoS One 2008, 3:e3942.
30. Tsang T.K., Cauchemez S., Perera R.A., Freeman G., Fang V.J., et al. Association between antibody titers and protection against influenza virus infection within households. J. Infect. Dis 2014, 210:684-692.
31. Tsibane T., Ekiert D.C., Krause J.C., Martinez O., Crowe J.E., et al. Influenza human monoclonal antibody 1F1 interacts with three major antigenic sites and residues mediating human receptor specificity in H1N1 viruses. PLoS Pathog 2012, 8:e1003067.
32. Wan Z., Ye J., Xu L., Shao H., Jin W., et al. Antigenic mapping of the hemagglutinin of an H9N2 avian influenza virus reveals novel critical amino acid positions in antigenic sites. J. Virol. 2014, 88:3898-3901.
33. Whittle J.R., Zhang R., Khurana S., King L.R., Manischewitz J., et al. Broadly neutralizing human antibody that recognizes the receptor-binding pocket of influenza virus hemagglutinin. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:14216-14221.
34. Wilson J.R., Tzeng W.P., Spesock A., Music N., Guo Z., et al. Diversity of the murine antibody response targeting influenza A(H1N1pdm09) hemagglutinin. Virology 2014, 458-459:114-124.
35. World Health Organization. 2011. Manual for the Laboratory Diagnosis and Virological Surveillance of Influenza. http://www.who.int/csr/disease/influenza/manual_diagnosis_surveillance:influenza/en/index.html.
36. Wrammert J., Koutsonanos D., Li G.M., Edupuganti S., Sui J., et al. Broadly cross-reactive antibodies dominate the human B cell response against 2009 pandemic H1N1 influenza virus infection. J. Exp. Med. 2011, 208:181-193.
37. Yang H., Carney P., Stevens J. Structure and Receptor binding properties of a pandemic H1N1 virus hemagglutinin. PLoS Curr 2010, 2:RRN1152.
38. Yewdell J.W., Gerhard W. Antigenic characterization of viruses by monoclonal antibodies. Annu. Rev. Microbiol. 1981, 35:185-206.
39. Yewdell JW, Caton AJ, Gerhard W Selection of influenza A virus adsorptive mutants by growth in the presence of a mixture of monoclonal antihemagglutinin antibodies. J. Virol. 1986, 57:623-628.
40. Zhu X., Guo Y.H., Jiang T., Wang Y.D., Chan K.H., et al. A unique and conserved neutralization epitope in H5N1 influenza viruses identified by a murine antibody against the A/goose/Guangdong/1/96 hemagglutinin. J. Virol. 2013.