Competitive detection of influenza neutralizing antibodies using a novel bivalent fluorescence-based microneutralization assay (BiFMA)

Vaccine

Volumn 33, Issue 30, 2015, Pages 3562-3570

  Baker, Steven F ^a   Nogales, Aitor ^a   Santiago, Felix W ^a   Topham, David J ^a   Martínez Sobrido, Luis ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

Bivalent fluorescence based microneutralization assay (BiFMA); Green fluorescent protein (GFP); Hemagglutination inhibition (HAI); Hemagglutinin (HA); Monomeric red fluorescent protein (mRFP); Neutralizing antibody (NAb); Single cycle infectious influenza A virus (sciIAV); Virus neutralization (VN)

Indexed keywords

GREEN FLUORESCENT PROTEIN; HEMAGGLUTINATION INHIBITING ANTIBODY; INFLUENZA VIRUS HEMAGGLUTININ; NEUTRALIZING ANTIBODY; RED FLUORESCENT PROTEIN; PHOTOPROTEIN;

ANIMAL CELL; ANTIBODY DETECTION; ANTIBODY SCREENING; ANTIGENICITY; ARTICLE; BIVALENT FLUORESCENCE BASED MICRONEUTRALIZATION ASSAY; CONTROLLED STUDY; FLUORESCENCE ANALYSIS; FLUORESCENCE MICROSCOPY; FLUORESCENCE SPECTROSCOPY; HEMAGGLUTINATION INHIBITION TEST; INFLUENZA VIRUS A; LUCIFERASE ASSAY; MDCK CELL LINE; NONHUMAN; PRIORITY JOURNAL; PSEUDOTYPING; REPORTER GENE; REVERSE GENETICS; SERUM; SINGLE CYCLE INFECTIOUS INFLUENZA A VIRUS; STABLE EXPRESSION; VIROGENESIS; VIRUS IMMUNITY; VIRUS NEUTRALIZATION; BLOOD; FLUOROMETRY; GENETICS; HUMAN; IMMUNOLOGY; INFLUENZA A VIRUS; PROCEDURES; SERODIAGNOSIS;

ANTIBODIES, NEUTRALIZING; FLUOROMETRY; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; HUMANS; INFLUENZA A VIRUS; LUMINESCENT PROTEINS; NEUTRALIZATION TESTS;

EID: 84931568252     PISSN: 0264410X     EISSN: 18732518     Source Type: Journal    
DOI: 10.1016/j.vaccine.2015.05.049     Document Type: Article

References (58)

1. 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.
2. WHO Influenza (seasonal) fact sheet No. 211 2014, WHO.
3. Shaw M.L., Palese P.S. Orthomyxoviridae: the viruses and their replication. Fields virology 2007, 1647-1689. Lippincott Williams and WIlkins, Philadelphia, PA. 5th ed. D.M. Knipe, P.M. Howley, D.E. Griffin, R.A. Lamb, M.A. Martin (Eds.).
4. Gamblin S.J., Skehel J.J. Influenza hemagglutinin and neuraminidase membrane glycoproteins. J Biol Chem 2010, 285:28403-28409.
5. Tong S., Li Y., Rivailler P., Conrardy C., Castillo D.A., Chen L.M., et al. A distinct lineage of influenza A virus from bats. Proc Natl Acad Sci USA 2012, 109:4269-4274.
6. Tong S., Zhu X., Li Y., Shi M., Zhang J., Bourgeois M., et al. New world bats harbor diverse influenza A viruses. PLoS Pathog 2013, 9:e1003657.
7. Fouchier R.A., Munster V., Wallensten A., Bestebroer T.M., Herfst S., Smith D., et al. Characterization of a novel influenza A virus hemagglutinin subtype (H16) obtained from black-headed gulls. J Virol 2005, 79:2814-2822.
8. Hancock K., Veguilla V., Lu X., Zhong W., Butler E.N., Sun H., et al. Cross-reactive antibody responses to the 2009 pandemic H1N1 influenza virus. N Engl J Med 2009, 361:1945-1952.
9. Cox N.J., Subbarao K. Influenza. Lancet 1999, 354:1277-1282.
10. Grohskopf L.A., Olsen S.J., Sokolow L.Z., Bresee J.S., Cox N.J., Broder K.R., et al. Prevention and control of seasonal influenza with vaccines: recommendations of the Advisory Committee on Immunization Practices (ACIP)-United States, 2014-15 influenza season. MMWR Morb Mortal Wkly Rep 2014, 63:691-697.
11. Dowdle W.N., Kendal A.P., Noble G.R. Diagnostic Procedures for Viral, Rickettsial, and Chlamydial Infections 1979, 585-609. American Public Health Association, Washington, DC. 5th ed. E.H. Jennette, N.J. Schmitt (Eds.).
12. Potter C.W., Oxford J.S. Determinants of immunity to influenza infection in man. Br Med Bull 1979, 35:69-75.
13. de Jong J.C., Palache A.M., Beyer W.E., Rimmelzwaan G.F., Boon A.C., Osterhaus A.D. Haemagglutination-inhibiting antibody to influenza virus. Dev Biol 2003, 115:63-73.
14. Hirst G.K. Adsorption of influenza hemagglutinins and virus by red blood cells. J Exp Med 1942, 76:195-209.
15. Webster R.G.C.N., Stoehr K. WHO manual on animal influenza diagnosis and surveillance 2002, WHO.
16. Jonges M., Liu W.M., van der Vries E., Jacobi R., Pronk I., Boog C., et al. Influenza virus inactivation for studies of antigenicity and phenotypic neuraminidase inhibitor resistance profiling. J Clin Microbiol 2010, 48:928-940.
17. Killian M.L. Hemagglutination assay for the avian influenza virus. Methods Mol Biol 2008, 436:47-52.
18. Rimmelzwaan G.F., Baars M., Claas E.C., Osterhaus A.D. Comparison of RNA hybridization, hemagglutination assay, titration of infectious virus and immunofluorescence as methods for monitoring influenza virus replication in vitro. J Virol Methods 1998, 74:57-66.
19. Stephenson I., Heath A., Major D., Newman R.W., Hoschler K., Junzi W., et al. Reproducibility of serologic assays for influenza virus A (H5N1). Emerg Infect Dis 2009, 15:1252-1259.
20. Rowe T., Abernathy R.A., Hu-Primmer J., Thompson W.W., Lu X., Lim W., et al. Detection of antibody to avian influenza A (H5N1) virus in human serum by using a combination of serologic assays. J Clin Microbiol 1999, 37:937-943.
21. World Health Organization/World Organisation for Animal HF, Agriculture Organization HNEWG Revised and updated nomenclature for highly pathogenic avian influenza A (H5N1) viruses. Influenza and other respiratory viruses 2014, 8:384-388.
22. Martinez-Sobrido L., Cadagan R., Steel J., Basler C.F., Palese P., Moran T.M., et al. Hemagglutinin-pseudotyped green fluorescent protein-expressing influenza viruses for the detection of influenza virus neutralizing antibodies. J Virol 2010, 84:2157-2163.
23. Ozawa M., Victor S.T., Taft A.S., Yamada S., Li C., Hatta M., et al. Replication-incompetent influenza A viruses that stably express a foreign gene. J Gen Virol 2011, 92:2879-2888.
24. Hooper K.A., Bloom J.D. A mutant influenza virus that uses an N1 neuraminidase as the receptor-binding protein. J Virol 2013, 87:12531-12540.
25. Rimmelzwaan G.F., Verburgh R.J., Nieuwkoop N.J., Bestebroer T.M., Fouchier R.A., Osterhaus A.D. Use of GFP-expressing influenza viruses for the detection of influenza virus A/H5N1 neutralizing antibodies. Vaccine 2011, 29:3424-3430.
26. Baker S.F., Nogales A., Finch C., Tuffy K.M., Domm W., Perez D.R., et al. Influenza A and B virus intertypic reassortment through compatible viral packaging signals. J Virol 2014, 88:10778-10791.
27. Marsh G.A., Hatami R., Palese P. Specific residues of the influenza A virus hemagglutinin viral RNA are important for efficient packaging into budding virions. J Virol 2007, 81:9727-9736.
28. Guo H., Baker S.F., Martinez-Sobrido L., Topham D.J. Induction of CD8 T cell heterologous protection by a single dose of single-cycle infectious influenza virus. J Virol 2014, 88:12006-12016.
29. Rodrigo W.W., de la Torre J.C., Martinez-Sobrido L. Use of single-cycle infectious lymphocytic choriomeningitis virus to study hemorrhagic fever arenaviruses. J Virol 2011, 85:1684-1695.
30. Baker S.F., Guo H., Albrecht R.A., Garcia-Sastre A., Topham D.J., Martinez-Sobrido L. Protection against lethal influenza with a viral mimic. J Virol 2013, 87:8591-8605.
31. Martinez-Sobrido L., Garcia-Sastre A. Generation of recombinant influenza virus from plasmid DNA. J Visualized Exp: JoVE 2010, (42). 10.3791/2057.
32. Fodor E., Devenish L., Engelhardt O.G., Palese P., Brownlee G.G., Garcia-Sastre A. Rescue of influenza A virus from recombinant DNA. J Virol 1999, 73:9679-9682.
33. Li S., Polonis V., Isobe H., Zaghouani H., Guinea R., Moran T., et al. Chimeric influenza virus induces neutralizing antibodies and cytotoxic T cells against human immunodeficiency virus type 1. J Virol 1993, 67:6659-6666.
34. Tan G.S., Krammer F., Eggink D., Kongchanagul A., Moran T.M., Palese P. A pan-H1 anti-hemagglutinin monoclonal antibody with potent broad-spectrum efficacy in vivo. J Virol 2012, 86:6179-6188.
35. Hai R., Krammer F., Tan G.S., Pica N., Eggink D., Maamary J., et al. Influenza viruses expressing chimeric hemagglutinins: globular head and stalk domains derived from different subtypes. J Virol 2012, 86:5774-5781.
36. Krammer F., Margine I., Tan G.S., Pica N., Krause J.C., Palese P. A carboxy-terminal trimerization domain stabilizes conformational epitopes on the stalk domain of soluble recombinant hemagglutinin substrates. PLoS ONE 2012, 7:e43603.
37. Santiago F.W., Fitzgerald T., Treanor J.J., Topham D.J. Vaccination with drifted variants of avian H5 hemagglutinin protein elicits a broadened antibody response that is protective against challenge with homologous or drifted live H5 influenza virus. Vaccine 2011, 29:8888-8897.
38. Nogales A., Baker S.F., Martinez-Sobrido L. Replication-competent influenza A viruses expressing a red fluorescent protein. Virology 2014, 476C:206-216.
39. Ramon S., Baker S.F., Sahler J.M., Kim N., Feldsott E.A., Serhan C.N., et al. The specialized proresolving mediator 17-HDHA enhances the antibody-mediated immune response against influenza virus: a new class of adjuvant. J Immunol 2014, 193:6031-6040.
40. Bodewes R., Nieuwkoop N.J., Verburgh R.J., Fouchier R.A., Osterhaus A.D., Rimmelzwaan G.F. Use of influenza A viruses expressing reporter genes to assess the frequency of double infections in vitro. J Gen Virol 2012, 93:1645-1648.
41. Inagaki A., Goto H., Kakugawa S., Ozawa M., Kawaoka Y. Competitive incorporation of homologous gene segments of influenza A virus into virions. J Virol 2012, 86:10200-10202.
42. Poole D.S., Yu S., Cai Y., Dinis J.M., Muller M.A., Jordan I., et al. Influenza A virus polymerase is a site for adaptive changes during experimental evolution in bat cells. J Virol 2014, 88:12572-12585.
43. Konig R., Stertz S., Zhou Y., Inoue A., Hoffmann H.H., Bhattacharyya S., et al. Human host factors required for influenza virus replication. Nature 2010, 463:813-817.
44. Rimmelzwaan G.F., Nieuwkoop N.J., de Mutsert G., Boon A.C., Kuiken T., Fouchier R.A., et al. Attachment of infectious influenza A viruses of various subtypes to live mammalian and avian cells as measured by flow cytometry. Virus Res 2007, 129:175-181.
45. Katsura H., Iwatsuki-Horimoto K., Fukuyama S., Watanabe S., Sakabe S., Hatta Y., et al. A replication-incompetent virus possessing an uncleavable hemagglutinin as an influenza vaccine. Vaccine 2012, 30:6027-6033.
46. Krammer F., Palese P. Influenza virus hemagglutinin stalk-based antibodies and vaccines. Curr Opin Virol 2013, 3:521-530.
47. Hirst G.K., Rickard E.R., Friedewald W.F. Studies in human immunization against influenza: duration of immunity induced by inactive virus. J Exp Med 1944, 80:265-273.
48. Salk J.E. A simplified procedure for titrating hemagglutinating capacity of influenza-virus and the corresponding antibody. J Immunol 1944, 49:87-98.
49. Corti D., Suguitan A.L., Pinna D., Silacci C., Fernandez-Rodriguez B.M., Vanzetta F., et al. Heterosubtypic neutralizing antibodies are produced by individuals immunized with a seasonal influenza vaccine. J Clin Invest 2010, 120:1663-1673.
50. Sui J., Hwang W.C., Perez S., Wei G., Aird D., Chen L.M., 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.
51. Corti D., Lanzavecchia A. Broadly neutralizing antiviral antibodies. Annu Rev Immunol 2013, 31:705-742.
52. Kohlmeier J.E., Woodland D.L. Immunity to respiratory viruses. Annu Rev Immunol 2009, 27:61-82.
53. Cox A., Baker S.F., Nogales A., Martinez-Sobrido L., Dewhurst S. Development of a mouse-adapted, live-attenuated influenza virus that permits in vivo analysis of enhancements to the safety of LAIV. J Virol 2015, 89(6):3421-3426.
54. Arzey G.G., Kirkland P.D., Arzey K.E., Frost M., Maywood P., Conaty S., et al. Influenza virus A (H10N7) in chickens and poultry abattoir workers, Australia. Emerg Infect Dis 2012, 18:814-816.
55. Jia N., de Vlas S.J., Liu Y.X., Zhang J.S., Zhan L., Dang R.L., et al. Serological reports of human infections of H7 and H9 avian influenza viruses in northern China. J Clin Virol 2009, 44:225-229.
56. Koopmans M., Wilbrink B., Conyn M., Natrop G., van der Nat H., Vennema H., et al. Transmission of H7N7 avian influenza A virus to human beings during a large outbreak in commercial poultry farms in the Netherlands. Lancet 2004, 363:587-593.
57. Wang M., Fu C.X., Zheng B.J. Antibodies against H5 and H9 avian influenza among poultry workers in China. N Engl J Med 2009, 360:2583-2584.
58. Molesti E., Wright E., Terregino C., Rahman R., Cattoli G., Temperton N.J. Multiplex evaluation of influenza neutralizing antibodies with potential applicability to in-field serological studies. J Immunol Res 2014, 2014:457932.