Evaluation of the antigenic relatedness and cross-protective immunity of the neuraminidase between human influenza A (H1N1) virus and highly pathogenic avian influenza A (H5N1) virus

Virology

Volumn 454-455, Issue 1, 2014, Pages 169-175

  Lu, Xiuhua ^a   Liu, Feng ^a   Zeng, Hui ^a   Sheu, Tiffany ^a   Achenbach, Jenna E ^a   Veguilla, Vic ^a   Gubareva, Larisa V ^a   Garten, Rebecca ^a   Smith, Catherine ^a   Yang, Hua ^a   Stevens, James ^a   Xu, Xiyan ^a   Katz, Jacqueline M ^a   Tumpey, Terrence M ^a  

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

Author keywords

Anti neuraminidase antibodies; Antigenic and genetic analyses; BALB c mice; Cross protective immunity; Influenza virus; Passive immunization

Indexed keywords

AMINO ACID; NEURAMINIDASE ANTIBODY; RECOMBINANT ANTIBODY; UNCLASSIFIED DRUG; VIRUS SIALIDASE;

AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY RESPONSE; ANTIBODY SPECIFICITY; ANTIGENICITY; ARTICLE; BACULOVIRUS EXPRESSION SYSTEM; CROSS PROTECTION; ENZYME INHIBITION; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; HEMOLYSIS; INFLUENZA VIRUS A H1N1; INFLUENZA VIRUS A H5N1; MOUSE; NONHUMAN; PASSIVE IMMUNIZATION; PRIORITY JOURNAL; RABBIT; SEROLOGY; VIRUS IMMUNITY; VIRUS INHIBITION; VIRUS RECOMBINANT; VIRUS REPLICATION; WEIGHT REDUCTION;

ANTI-NEURAMINIDASE ANTIBODIES; ANTIGENIC AND GENETIC ANALYSES; BALB/C MICE; CROSS-PROTECTIVE IMMUNITY; INFLUENZA VIRUS; PASSIVE IMMUNIZATION;

ANIMALS; ANTIGENS, VIRAL; CROSS PROTECTION; CROSS REACTIONS; DISEASE MODELS, ANIMAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; IMMUNIZATION, PASSIVE; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA A VIRUS, H5N1 SUBTYPE; MICE; MICE, INBRED BALB C; NEURAMINIDASE; NEUTRALIZATION TESTS; ORTHOMYXOVIRIDAE INFECTIONS; RABBITS; VIRAL PLAQUE ASSAY; VIRAL PROTEINS;

EID: 84895448120     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2014.02.011     Document Type: Article

References (70)

1. Air G.M., Els M.C., Brown L.E., Laver W.G., Webster R.G. Location of antigenic sites on the three-dimensional structure of the influenza N2 virus neuraminidase. Virology 1985, 145:237-248.
2. Air G.M., Laver W.G., Luo M., Stray S.J., Legrone G., Webster R.G. Antigenic, sequence, and crystal variation in influenza B neuraminidase. Virology 1990, 177:578-587.
3. Air G.M., Laver W.G., Webster R.G. Mechanism of antigenic variation in an individual epitope on influenza virus N9 neuraminidase. J. Virol. 1990, 64:5797-5803.
4. Aymard-Henry M., Coleman M.T., Dowdle W.R., Laver W.G., Schild G.C., Webster R.G. Influenzavirus neuraminidase and neuraminidase-inhibition test procedures. Bull. World Health Organ. 1973, 48:199-202.
5. Baker A.T., Varghese J.N., Laver W.G., Air G.M., Colman P.M. Three-dimensional structure of neuraminidase of subtype N9 from an avian influenza virus. Proteins 1987, 2:111-117.
6. Beutner K.R., Chow T., Rubi E., Strussenberg J., Clement J., Ogra P.L. Evaluation of a neuraminidase-specific influenza A virus vaccine in children: antibody responses and effects on two successive outbreaks of natural infection. J. Infect. Dis. 1979, 140:844-850.
7. Bramucci E., Paiardini A., Bossa F., Pascarella S. PyMod: sequence similarity searches, multiple sequence-structure alignments, and homology modeling within PyMOL. BMC Bioinforma. 2012, 13(Suppl 4):S2.
8. Brett I.C., Johansson B.E. Immunization against influenza A virus: comparison of conventional inactivated, live-attenuated and recombinant baculovirus produced purified hemagglutinin and neuraminidase vaccines in a murine model system. Virology 2005, 339:273-280.
9. Burmeister W.P., Ruigrok R.W., Cusack S. The 2.2 A resolution crystal structure of influenza B neuraminidase and its complex with sialic acid. EMBO J. 1992, 11:49-56.
10. Centers for Disease Control and Preventation Estimates of deaths associated with seasonal influenza-United States, 1976-2007. Morb. Mortal. Wkly Rep. 2010, 59:1057-1062.
11. Centers for Disease Control and Preventation Update: influenza activity-United States, 2009-10 season. Morb. Mortal. Wkly Rep. 2010, 59:901-908.
12. Chen Z., Kadowaki S., Hagiwara Y., Yoshikawa T., Matsuo K., Kurata T., Tamura S. Cross-protection against a lethal influenza virus infection by DNA vaccine to neuraminidase. Vaccine 2000, 18:3214-3222.
13. Collins P.J., Haire L.F., Lin Y.P., Liu J., Russell R.J., Walker P.A., Skehel J.J., Martin S.R., Hay A.J., Gamblin S.J. Crystal structures of oseltamivir-resistant influenza virus neuraminidase mutants. Nature 2008, 453:1258-1261.
14. Colman P.M., Laver W.G., Varghese J.N., Baker A.T., Tulloch P.A., Air G.M., Webster R.G. Three-dimensional structure of a complex of antibody with influenza virus neuraminidase. Nature 1987, 326:358-363.
15. Colman P.M., Varghese J.N., Laver W.G. Structure of the catalytic and antigenic sites in influenza virus neuraminidase. Nature 1983, 303:41-44.
16. Couch R.B., Atmar R.L., Franco L.M., Quarles J.M., Wells J., Arden N., Nino D., Belmont J.W. Antibody correlates and predictors of immunity to naturally occurring influenza in humans and the importance of antibody to the neuraminidase. J. Infect. Dis. 2013, 207:974-981.
17. Couch R.B., Kasel J.A., Gerin J.L., Schulman J.L., Kilbourne E.D. Induction of partial immunity to influenza by a neuraminidase-specific vaccine. J. Infect. Dis. 1974, 129:411-420.
18. Deroo T., Jou W.M., Fiers W. Recombinant neuraminidase vaccine protects against lethal influenza. Vaccine 1996, 14:561-569.
19. Farrohi K., Farrohi F.K., Noble G.R., Kaye H.S., Kendal A.P. Evaluation of the single radial hemolysis test for measuring hemagglutinin- and neuraminidase-specific antibodies to H3N2 influenza strains and antibodies to influenza B. J. Clin. Microbiol. 1977, 5:353-360.
20. Francis T. Influenza: the new acquayantance. Ann. Intern. Med. 1953, 39:203-221.
21. Frobert E., Bouscambert-Duchamp M., Escuret V., Mundweiler S., Barthelemy M., Morfin F., Valette M., Gerdil C., Lina B., Ferraris O. Anti N1 cross-protecting antibodies against H5N1 detected in H1N1 infected people. Curr. Microbiol. 2010, 61:25-28.
22. 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, 325:197-201.
23. Gulati U., Hwang C.C., Venkatramani L., Gulati S., Stray S.J., Lee J.T., Laver W.G., Bochkarev A., Zlotnick A., Air G.M. Antibody epitopes on the neuraminidase of a recent H3N2 influenza virus (A/Memphis/31/98). J. Virol. 2002, 76:12274-12280.
24. Jahiel R.I., Kilbourne E.D. Reduction in plaque size and reduction in plaque number as differing indices of influenza virus-antibody reactions. J. Bacteriol. 1966, 92:1521-1534.
25. Johansson B.E. Immunization with influenza A virus hemagglutinin and neuraminidase produced in recombinant baculovirus results in a balanced and broadened immune response superior to conventional vaccine. Vaccine 1999, 17:2073-2080.
26. 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, 63:1239-1246.
27. Johansson B.E., Matthews J.T., Kilbourne E.D. Supplementation of conventional influenza A vaccine with purified viral neuraminidase results in a balanced and broadened immune response. Vaccine 1998, 16:1009-1015.
28. Johansson B.E., Price P.M., Kilbourne E.D. Immunogenicity of influenza A virus N2 neuraminidase produced in insect larvae by baculovirus recombinants. Vaccine 1995, 13:841-845.
29. Katz J.M., Hancock K., Xu X. Serologic assays for influenza surveillance, diagnosis and vaccine evaluation. Expert Rev. Anti-infect. Ther. 2011, 9:669-683.
30. Katz J.M., Lu X., Young S.A., Galphin J.C. Adjuvant activity of the heat-labile enterotoxin from enterotoxigenic Escherichia coli for oral administration of inactivated influenza virus vaccine. J. Infect. Dis. 1997, 175:352-363.
31. Kendal A.P., Joseph J.M., Kobayashi G., Nelson D., Reyes C.R., Ross M.R., Sarandria J.L., White R., Woodall D.F., Noble G.R., Dowdle W.R. Laboratory-based surveillance of influenza virus in the United States during the winter of 1977-1978. I. Periods of prevalence of H1N1 and H3N2 influenza A strains, their relative rates of isolation in different age groups, and detection of antigenic variants. Am. J. Epidemiol. 1979, 110:449-461.
32. Kendal A.P., Skehel J.J., Pereura M.S. Concepts and Procedures for Laboratory-Based Influenza Surveillance 1982, U.S. Department of Health and Human Services, Public Health Service, Centers for Disease Control, Atlanta.
33. Kilbourne E.D., Couch R.B., Kasel J.A., Keitel W.A., Cate T.R., Quarles J.H., Grajower B., Pokorny B.A., Johansson B.E. Purified influenza A virus N2 neuraminidase vaccine is immunogenic and non-toxic in humans. Vaccine 1995, 13:1799-1803.
34. Kilbourne E.D., Laver W.G., Schulman J.L., Webster R.G. Antiviral activity of antiserum specific for an influenza virus neuraminidase. J. Virol. 1968, 2:281-288.
35. Kilbourne E.D., Pokorny B.A., Johansson B., Brett I., Milev Y., Matthews J.T. Protection of mice with recombinant influenza virus neuraminidase. J. Infect. Dis. 2004, 189:459-461.
36. Kilbourne E.D., Smith C., Brett I., Pokorny B.A., Johansson B., Cox N. The total influenza vaccine failure of 1947 revisited: major intrasubtypic antigenic change can explain failure of vaccine in a post-World War II epidemic. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:10748-10752.
37. Larkin M.A., Blackshields G., Brown N.P., Chenna R., McGettigan P.A., McWilliam H., Valentin F., Wallace I.M., Wilm A., Lopez R., Thompson J.D., Gibson T.J., Higgins D.G. Clustal W and clustal X version 2.0. Bioinformatics 2007, 23:2947-2948.
38. Lentz M.R., Air G.M., Laver W.G., Webster R.G. Sequence of the neuraminidase gene of influenza virus A/Tokyo/3/67 and previously uncharacterized monoclonal variants. Virology 1984, 135:257-265.
39. Li Q., Qi J., Zhang W., Vavricka C.J., Shi Y., Wei J., Feng E., Shen J., Chen J., Liu D., He J., Yan J., Liu H., Jiang H., Teng M., Li X., Gao G.F. The 2009 pandemic H1N1 neuraminidase N1 lacks the 150-cavity in its active site. Nat. Struct. Mol. Biol. 2010, 17:1266-1268.
40. Li Q., Sun X., Li Z., Liu Y., Vavricka C.J., Qi J., Gao G.F. Structural and functional characterization of neuraminidase-like molecule N10 derived from bat influenza A virus. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:18897-18902.
41. Lu X., Tumpey T.M., Morken T., Zaki S.R., Cox N.J., Katz J.M. A mouse model for the evaluation of pathogenesis and immunity to influenza A (H5N1) viruses isolated from humans. J. Virol. 1999, 73:5903-5911.
42. Malby R.L., Tulip W.R., Harley V.R., McKimm-Breschkin J.L., Laver W.G., Webster R.G., Colman P.M. The structure of a complex between the NC10 antibody and influenza virus neuraminidase and comparison with the overlapping binding site of the NC41 antibody. Structure 1994, 2:733-746.
43. Matrosovich M.N., Matrosovich T.Y., Gray T., Roberts N.A., Klenk H.D. Neuraminidase is important for the initiation of influenza virus infection in human airway epithelium. J. Virol. 2004, 78:12665-12667.
44. Monto A.S., Kendal A.P. Effect of neuraminidase antibody on Hong Kong influenza. Lancet 1973, 1:623-625.
45. Murphy B.R., Kasel J.A., Chanock R.M. Association of serum anti-neuraminidase antibody with resistance to influenza in man. New Engl. J. Med. 1972, 286:1329-1332.
46. Palese P., Tobita K., Ueda M., Compans R.W. Characterization of temperature sensitive influenza virus mutants defective in neuraminidase. Virology 1974, 61:397-410.
47. Powers D.C., Kilbourne E.D., Johansson B.E. Neuraminidase-specific antibody responses to inactivated influenza virus vaccine in young and elderly adults. Clin. Diagn. Lab. Immunol. 1996, 3:511-516.
48. Rott R., Becht H., Orlich M. The significance of influenza virus neuraminidase in immunity. J. General Virol. 1974, 22:35-41.
49. Russell R.J., Haire L.F., Stevens D.J., Collins P.J., Lin Y.P., Blackburn G.M., Hay A.J., Gamblin S.J., Skehel J.J. The structure of H5N1 avian influenza neuraminidase suggests new opportunities for drug design. Nature 2006, 443:45-49.
50. Saito T., Taylor G., Laver W.G., Kawaoka Y., Webster R.G. Antigenicity of the N8 influenza A virus neuraminidase: existence of an epitope at the subunit interface of the neuraminidase. J. Virol. 1994, 68:1790-1796.
51. Sandbulte M.R., Jimenez G.S., Boon A.C., Smith L.R., Treanor J.J., Webby R.J. Cross-reactive neuraminidase antibodies afford partial protection against H5N1 in mice and are present in unexposed humans. PLoS Med. 2007, 4:e59.
52. Schulman J.L., Khakpour M., Kilbourne E.D. Protective effects of specific immunity to viral neuraminidase on influenza virus infection of mice. J. Virol. 1968, 2:778-786.
53. Seto J.T., Rott R. Functional significance of sialidose during influenza virus multiplication. Virology 1966, 30:731-737.
54. Shil P., Chavan S.S., Cherian S.S. Antigenic variability in neuraminidase protein of influenza A/H3N2 vaccine strains (1968-2009). Bioinformation 2011, 7:76-81.
55. Smith A.J., Davies J.R. Natural infection with influenza A (H3N2). The development, persistance and effect of antibodies to the surface antigens. J. Hyg. 1976, 77:271-282.
56. Sylte M.J., Hubby B., Suarez D.L. Influenza neuraminidase antibodies provide partial protection for chickens against high pathogenic avian influenza infection. Vaccine 2007, 25:3763-3772.
57. Tulip W.R., Varghese J.N., Baker A.T., van Donkelaar A., Laver W.G., Webster R.G., Colman P.M. Refined atomic structures of N9 subtype influenza virus neuraminidase and escape mutants. J. Mol. Biol. 1991, 221:487-497.
58. Tumpey T.M., Basler C.F., Aguilar P.V., Zeng H., Solorzano A., Swayne D.E., Cox N.J., Katz J.M., Taubenberger J.K., Palese P., Garcia-Sastre A. Characterization of the reconstructed 1918 Spanish influenza pandemic virus. Science 2005, 310:77-80.
59. Varghese J.N., Laver W.G., Colman P.M. Structure of the influenza virus glycoprotein antigen neuraminidase at 2.9 A resolution. Nature 1983, 303:35-40.
60. Venkatramani L., Bochkareva E., Lee J.T., Gulati U., Graeme Laver W., Bochkarev A., Air G.M. An epidemiologically significant epitope of a 1998 human influenza virus neuraminidase forms a highly hydrated interface in the NA-antibody complex. J. Mol. Biol. 2006, 356:651-663.
61. Wan H., Gao J., Xu K., Chen H., Couzens L.K., Rivers K.H., Easterbrook J.D., Yang K., Zhong L., Rajabi M., Ye J., Sultana I., Wan X.F., Liu X., Perez D.R., Taubenberger J.K., Eichelberger M.C. Molecular basis for broad neuraminidase immunity: conserved epitopes in seasonal and pandemic H1N1 as well as H5N1 influenza viruses. J. Virol. 2013, 87:9290-9300.
62. Wang M., Qi J., Liu Y., Vavricka C.J., Wu Y., Li Q., Gao G.F. Influenza A virus N5 neuraminidase has an extended 150-cavity. J. Virol. 2011, 85:8431-8435.
63. Webster R.G., Air G.M., Metzger D.W., Colman P.M., Varghese J.N., Baker A.T., Laver W.G. Antigenic structure and variation in an influenza virus N9 neuraminidase. J. Virol. 1987, 61:2910-2916.
64. Webster R.G., Reay P.A., Laver W.G. Protection against lethal influenza with neuraminidase. Virology 1988, 164:230-237.
65. WHO, 2013. Influenza at the Human-Animal Interface (HAI).
66. Wilson I.A., Cox N.J. Structural basis of immune recognition of influenza virus hemagglutinin. Annu. Rev. Immunol. 1990, 8:737-771.
67. Smith Wilson, Andrewes C.H., Laidlaw P.P. A virus obtained from influenza patients. Lancet 1933, 222:66-68.
68. Xu X., Cox N.J., Bender C.A., Regnery H.L., Shaw M.W. Genetic variation in neuraminidase genes of influenza A (H3N2) viruses. Virology 1996, 224:175-183.
69. Xu X., Zhu X., Dwek R.A., Stevens J., Wilson I.A. Structural characterization of the 1918 influenza virus H1N1 neuraminidase. J. Virol. 2008, 82:10493-10501.
70. Zhu X., Yang H., Guo Z., Yu W., Carney P.J., Li Y., Chen L.M., Paulson J.C., Donis R.O., Tong S., Stevens J., Wilson I.A. Crystal structures of two subtype N10 neuraminidase-like proteins from bat influenza A viruses reveal a diverged putative active site. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:18903-18908.