Contributions of antinucleoprotein IgG to heterosubtypic immunity against influenza virus

Journal of Immunology

Volumn 186, Issue 7, 2011, Pages 4331-4339

  LaMere, Mark W ^a   Lam, Ho Tak ^a   Moquin, Amy ^b   Haynes, Laura ^b   Lund, Frances E ^a   Randall, Troy D ^a   Kaminski, Denise A ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^b TRUDEAU INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FC RECEPTOR; IMMUNOGLOBULIN G ANTIBODY; INFLUENZA VACCINE; NONSTRUCTURAL PROTEIN 1; UNCLASSIFIED DRUG; VIRUS NUCLEOPROTEIN ANTIBODY;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY RESPONSE; ANTIBODY SPECIFICITY; ANTIGEN ANTIBODY REACTION; ARTICLE; B LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; INFLUENZA; INFLUENZA VIRUS; LYMPHOCYTE DEPLETION; MOUSE; NONHUMAN; PRIORITY JOURNAL; VACCINE PRODUCTION; VIRUS IMMUNITY;

ANIMALS; ANTIBODIES, VIRAL; ANTIBODY DIVERSITY; HUMANS; IMMUNOGLOBULIN G; INFLUENZA A VIRUS; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA A VIRUS, H3N2 SUBTYPE; INFLUENZA VACCINES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, MUTANT STRAINS; ORTHOMYXOVIRIDAE INFECTIONS; RNA-BINDING PROTEINS; VIRAL CORE PROTEINS;

EID: 79955042558     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1003057     Document Type: Article

References (77)

1. Maines, T. R., K. J. Szretter, L. Perrone, J. A. Belser, R. A. Bright, H. Zeng, T. M. Tumpey, and J. M. Katz. 2008. Pathogenesis of emerging avian influenza viruses in mammals and the host innate immune response. Immunol. Rev. 225: 68-84.
2. Subbarao, K., B. R. Murphy, and A. S. Fauci. 2006. Development of effective vaccines against pandemic influenza. Immunity 24: 5-9. (Pubitemid 43077193)
3. Whitley, R. J., and A. S. Monto. 2006. Seasonal and pandemic influenza preparedness: A global threat. J. Infect. Dis. 194(Suppl. 2): S65-S69. (Pubitemid 44630947)
4. Tosh, P. K., R. M. Jacobson, and G. A. Poland. 2010. Influenza vaccines: From surveillance through production to protection. Mayo Clin. Proc. 85: 257-273.
5. Du, L., Y. Zhou, and S. Jiang. 2010. Research and development of universal influenza vaccines. Microbes Infect. 12: 280-286.
6. Karlsson Hedestam, G. B., R. A. Fouchier, S. Phogat, D. R. Burton, J. Sodroski, and R. T. Wyatt. 2008. The challenges of eliciting neutralizing antibodies to HIV-1 and to influenza virus. Nat. Rev. Microbiol. 6: 143-155.
7. Mossad, S. B. 2008. 2008-2009 influenza update: A better vaccine match. Cleve. Clin. J. Med. 75: 865-870.
8. Epstein, S. L., C. Y. Lo, J. A. Misplon, C. M. Lawson, B. A. Hendrickson, E. E. Max, and K. Subbarao. 1997. Mechanisms of heterosubtypic immunity to lethal influenza Avirus infection in fully immunocompetent, T cell-depleted, b2- microglobulin-deficient, and J chain-deficient mice. J. Immunol. 158: 1222-1230. (Pubitemid 127469945)
9. Liang, S., K. Mozdzanowska, G. Palladino, and W. Gerhard. 1994. Heterosubtypic immunity to influenza type A virus in mice: Effector mechanisms and their longevity. J. Immunol. 152: 1653-1661. (Pubitemid 24075695)
10. Nguyen, H. H., M. Zemlin, I. I. Ivanov, J. Andrasi, C. Zemlin, H. L. Vu, R. Schelonka, H. W. Schroeder, Jr., and J. Mestecky. 2007. Heterosubtypic immunity to influenza A virus infection requires a properly diversified antibody repertoire. J. Virol. 81: 9331-9338. (Pubitemid 47311475)
11. Powell, T. J., T. Strutt, J. Reome, J. A. Hollenbaugh, A. D. Roberts, D. L.Woodland, S. L. Swain, and R.W. Dutton. 2007. Priming with cold-adapted influenza A does not prevent infection but elicits long-lived protection against supralethal challenge with heterosubtypic virus. J. Immunol. 178: 1030-1038. (Pubitemid 46095176)
12. Rangel-Moreno, J., D. M. Carragher, R. S. Misra, K. Kusser, L. Hartson, A. Moquin, F. E. Lund, and T. D. Randall. 2008. B cells promote resistance to heterosubtypic strains of influenza via multiple mechanisms. J. Immunol. 180: 454-463.
13. Sambhara, S., A. Kurichh, R. Miranda, T. Tumpey, T. Rowe, M. Renshaw, R. Arpino, A. Tamane, A. Kandil, O. James, et al. 2001. Heterosubtypic immunity against human influenza A viruses, including recently emerged avian H5 and H9 viruses, induced by FLU-ISCOM vaccine in mice requires both cytotoxic T-lymphocyte and macrophage function. Cell. Immunol. 211: 143-153. (Pubitemid 32977345)
14. Tumpey, T. M., M. Renshaw, J. D. Clements, and J. M. Katz. 2001. Mucosal delivery of inactivated influenza vaccine induces B-cell-dependent heterosubtypic cross-protection against lethal influenza A H5N1 virus infection. J. Virol. 75: 5141-5150. (Pubitemid 32448536)
15. Kreijtz, J. H., R. Bodewes, G. van Amerongen, T. Kuiken, R. A. Fouchier, A. D. Osterhaus, and G. F. Rimmelzwaan. 2007. Primary influenza A virus infection induces cross-protective immunity against a lethal infection with a heterosubtypic virus strain in mice. Vaccine 25: 612-620. (Pubitemid 44856111)
16. Sonoguchi, T., H. Naito, M. Hara, Y. Takeuchi, and H. Fukumi. 1985. Crosssubtype protection in humans during sequential, overlapping, and/or concurrent epidemics caused by H3N2 and H1N1 influenza viruses. J. Infect. Dis. 151: 81-88. (Pubitemid 15192884)
17. Nichol, K. L., J. D. Nordin, D. B. Nelson, J. P. Mullooly, and E. Hak. 2007. Effectiveness of influenza vaccine in the community-dwelling elderly. N. Engl. J. Med. 357: 1373-1381. (Pubitemid 47535592)
18. Ohmit, S. E., J. C. Victor, J. R. Rotthoff, E. R. Teich, R. K. Truscon, L. L. Baum, B. Rangarajan, D.W. Newton, M. L. Boulton, and A. S. Monto. 2006. Prevention of antigenically drifted influenza by inactivated and live attenuated vaccines. N. Engl. J. Med. 355: 2513-2522. (Pubitemid 44917499)
19. Mossad, S. B. 2007. Influenza update 2007-2008: Vaccine advances, pandemic preparation. Cleve. Clin. J. Med. 74: 889-894.
20. Sui, J., W. C. Hwang, S. Perez, G. Wei, D. Aird, L. M. Chen, E. Santelli, B. Stec, G. Cadwell, M. Ali, et al. 2009. Structural and functional bases for broadspectrum neutralization of avian and human influenza A viruses. Nat. Struct. Mol. Biol. 16: 265-273.
21. Wei, C. J., J. C. Boyington, P. M. McTamney, W. P. Kong, M. B. Pearce, L. Xu, H. Andersen, S. Rao, T. M. Tumpey, Z. Y. Yang, and G. J. Nabel. 2010. Induction of broadly neutralizing H1N1 influenza antibodies by vaccination. Science 329: 1060-1064.
22. Korteweg, C., and J. Gu. 2008. Pathology, molecular biology, and pathogenesis of avian influenza A (H5N1) infection in humans. Am. J. Pathol. 172: 1155-1170. (Pubitemid 351671530)
23. Koopmans, M., B. Wilbrink, M. Conyn, G. Natrop, H. van der Nat, H. Vennema, A. Meijer, J. van Steenbergen, R. Fouchier, A. Osterhaus, and A. Bosman. 2004. Transmission of H7N7 avian influenza A virus to human beings during a large outbreak in commercial poultry farms in the Netherlands. Lancet 363: 587-593. (Pubitemid 38264175)
24. Peiris, M., K. Y. Yuen, C. W. Leung, K. H. Chan, P. L. Ip, R. W. Lai, W. K. Orr, and K. F. Shortridge. 1999. Human infection with influenza H9N2. Lancet 354: 916-917. (Pubitemid 29424025)
25. Shu, L. L., W. J. Bean, and R. G. Webster. 1993. Analysis of the evolution and variation of the human influenza A virus nucleoprotein gene from 1933 to 1990. J. Virol. 67: 2723-2729. (Pubitemid 23118870)
26. Portela, A., and P. Digard. 2002. The influenza virus nucleoprotein: A multifunctional RNA-binding protein pivotal to virus replication. J. Gen. Virol. 83: 723-734. (Pubitemid 34284855)
27. Wraith, D. C., A. E. Vessey, and B. A. Askonas. 1987. Purified influenza virus nucleoprotein protects mice from lethal infection. J. Gen. Virol. 68: 433-440. (Pubitemid 17007830)
28. Fu, T. M., L. Guan, A. Friedman, T. L. Schofield, J. B. Ulmer, M. A. Liu, and J. J. Donnelly. 1999. Dose dependence of CTL precursor frequency induced by a DNA vaccine and correlation with protective immunity against influenza virus challenge. J. Immunol. 162: 4163-4170. (Pubitemid 29314802)
29. + T cells against influenza virus induced by vaccination with nucleoprotein DNA. J. Virol. 72: 5648-5653. (Pubitemid 28283349)
30. Ulmer, J. B., J. J. Donnelly, S. E. Parker, G. H. Rhodes, P. L. Felgner, V. J. Dwarki, S. H. Gromkowski, R. R. Deck, C. M. DeWitt, A. Friedman, et al. 1993. Heterologous protection against influenza by injection of DNA encoding a viral protein. Science 259: 1745-1749. (Pubitemid 23114660)
31. + T cells can promote survival and recovery after challenge. Int. Immunol. 12: 91-101. (Pubitemid 30045416)
32. Epstein, S. L., W. P. Kong, J. A. Misplon, C. Y. Lo, T. M. Tumpey, L. Xu, and G. J. Nabel. 2005. Protection against multiple influenza A subtypes by vaccination with highly conserved nucleoprotein. Vaccine 23: 5404-5410. (Pubitemid 41579312)
33. Lo, C. Y., Z. Wu, J. A. Misplon, G. E. Price, C. Pappas, W. P. Kong, T. M. Tumpey, and S. L. Epstein. 2008. Comparison of vaccines for induction of heterosubtypic immunity to influenza A virus: Cold-adapted vaccine versus DNA prime-adenovirus boost strategies. Vaccine 26: 2062-2072.
34. Carragher, D. M., D. A. Kaminski, A. Moquin, L. Hartson, and T. D. Randall. 2008. A novel role for non-neutralizing antibodies against nucleoprotein in facilitating resistance to influenza virus. J. Immunol. 181: 4168-4176.
35. Muramatsu, M., K. Kinoshita, S. Fagarasan, S. Yamada, Y. Shinkai, and T. Honjo. 2000. Class switch recombination and hypermutation require activation-induced cytidine deaminase (AID), a potential RNA editing enzyme. Cell 102: 553-563.
36. Mozdzanowska, K., K. Maiese, M. Furchner, and W. Gerhard. 1999. Treatment of influenza virus-infected SCID mice with nonneutralizing antibodies specific for the transmembrane proteins matrix 2 and neuraminidase reduces the pulmonary virus titer but fails to clear the infection. Virology 254: 138-146. (Pubitemid 29391721)
37. Gerhard, W., K. Mozdzanowska, M. Furchner, G. Washko, and K. Maiese. 1997. Role of the B-cell response in recovery of mice from primary influenza virus infection. Immunol. Rev. 159: 95-103. (Pubitemid 27499862)
38. Nimmerjahn, F., and J. V. Ravetch. 2005. Divergent immunoglobulin g subclass activity through selective Fc receptor binding. Science 310: 1510-1512. (Pubitemid 41746349)
39. Nimmerjahn, F., and J. V. Ravetch. 2006. Fcg receptors: Old friends and new family members. Immunity 24: 19-28. (Pubitemid 43077197)
40. Barrington, R., M. Zhang, M. Fischer, and M. C. Carroll. 2001. The role of complement in inflammation and adaptive immunity. Immunol. Rev. 180: 5-15. (Pubitemid 32472848)
41. Lau, C. M., C. Broughton, A. S. Tabor, S. Akira, R. A. Flavell, M. J. Mamula, S. R. Christensen, M. J. Shlomchik, G. A. Viglianti, I. R. Rifkin, and A. Marshak-Rothstein. 2005. RNA-associated autoantigens activate B cells by combined B cell antigen receptor/Toll-like receptor 7 engagement. J. Exp. Med. 202: 1171-1177. (Pubitemid 41586947)
42. Yasuda, K., C. Richez, J. W. Maciaszek, N. Agrawal, S. Akira, A. Marshak- Rothstein, and I. R. Rifkin. 2007. Murine dendritic cell type I IFN production induced by human IgG-RNA immune complexes is IFN regulatory factor (IRF)5 and IRF7 dependent and is required for IL-6 production. J. Immunol. 178: 6876-6885. (Pubitemid 46847413)
43. Palmer, P., B. Charley, B. Rombaut, M. Daëron, and P. Lebon. 2000. Antibodydependent induction of type I interferons by poliovirus in human mononuclear blood cells requires the type II fcg receptor (CD32). Virology 278: 86-94. (Pubitemid 32002597)
44. Hober, D., W. Chehadeh, A. Bouzidi, and P. Wattré. 2001. Antibody-dependent enhancement of coxsackievirus B4 infectivity of human peripheral blood mononuclear cells results in increased interferon-a synthesis. J. Infect. Dis. 184: 1098-1108. (Pubitemid 33010461)
45. Chehadeh, W., A. Bouzidi, G. Alm, P. Wattré, and D. Hober. 2001. Human antibodies isolated from plasma by affinity chromatography increase the coxsackievirus B4-induced synthesis of interferon-a by human peripheral blood mononuclear cells in vitro. J. Gen. Virol. 82: 1899-1907. (Pubitemid 32707554)
46. Basler, C. F., and P. V. Aguilar. 2008. Progress in identifying virulence determinants of the 1918 H1N1 and the Southeast Asian H5N1 influenza A viruses. Antiviral Res. 79: 166-178.
47. Harada, Y., M. Muramatsu, T. Shibata, T. Honjo, and K. Kuroda. 2003. Unmutated immunoglobulin M can protect mice from death by influenza virus infection. J. Exp. Med. 197: 1779-1785. (Pubitemid 36745352)
48. Tsuji, R. F., M. Szczepanik, I. Kawikova, V. Paliwal, R. A. Campos, A. Itakura, M. Akahira-Azuma, N. Baumgarth, L. A. Herzenberg, and P.W. Askenase. 2002. B cell-dependent T cell responses: IgM antibodies are required to elicit contact sensitivity. J. Exp. Med. 196: 1277-1290. (Pubitemid 35375548)
49. Hutchinson, E. C., J. C. von Kirchbach, J. R. Gog, and P. Digard. 2010. Genome packaging in influenza A virus. J. Gen. Virol. 91(Pt. 2): 313-328.
50. Virelizier, J. L., A. C. Allison, J. S. Oxford, and G. C. Schild. 1977. Early presence of ribonucleoprotein antigen on surface of influenza virus-infected cells. Nature 266: 52-54. (Pubitemid 8050009)
51. Yewdell, J. W., E. Frank, and W. Gerhard. 1981. Expression of influenza A virus internal antigens on the surface of infected P815 cells. J. Immunol. 126: 1814-1819. (Pubitemid 11120964)
52. Sukeno, N., Y. Otsuki, J. Konno, N. Yamane, T. Odagiri, J. Arikawa, and N. Ishida. 1979. Anti-nucleoprotein antibody response in influenza A infection. Tohoku J. Exp. Med. 128: 241-249. (Pubitemid 9222505)
53. Yamane, N., T. Odagiri, J. Arikawa, and N. Ishida. 1981. Reversed single-radialimmunodiffusion test: The method for the assay of the antibody to influenza A nucleoprotein. Tohoku J. Exp. Med. 133: 245-255. (Pubitemid 11079918)
54. Ennis, F. A., Q. Yi-Hua, and G. C. Schild. 1982. Antibody and cytotoxic T lymphocyte responses of humans to live and inactivated influenza vaccines. J. Gen. Virol. 58: 273-281. (Pubitemid 12151943)
55. Huber, V. C., J. M. Lynch, D. J. Bucher, J. Le, and D. W. Metzger. 2001. Fc receptor-mediated phagocytosis makes a significant contribution to clearance of influenza virus infections. J. Immunol. 166: 7381-7388. (Pubitemid 32525614)
56. Stratov, I., A. Chung, and S. J. Kent. 2008. Robust NK cell-mediated human immunodeficiency virus (HIV)-specific antibody-dependent responses in HIVinfected subjects. J. Virol. 82: 5450-5459. (Pubitemid 351705252)
57. Forthal, D. N., G. Landucci, and E. S. Daar. 2001. Antibody from patients with acute human immunodeficiency virus (HIV) infection inhibits primary strains of HIV type 1 in the presence of natural-killer effector cells. J. Virol. 75: 6953-6961. (Pubitemid 32641582)
58. Ahmad, R., S. T. Sindhu, E. Toma, R. Morisset, J. Vincelette, J. Menezes, and A. Ahmad. 2001. Evidence for a correlation between antibody-dependent cellular cytotoxicity-mediating anti-HIV-1 antibodies and prognostic predictors of HIV infection. J. Clin. Immunol. 21: 227-233. (Pubitemid 32434310)
59. Gómez-Román, V. R., L. J. Patterson, D. Venzon, D. Liewehr, K. Aldrich, R. Florese, and M. Robert-Guroff. 2005. Vaccine-elicited antibodies mediate antibody-dependent cellular cytotoxicity correlated with significantly reduced acute viremia in rhesus macaques challenged with SIVmac251. J. Immunol. 174: 2185-2189. (Pubitemid 40223963)
60. Hessell, A. J., L. Hangartner, M. Hunter, C. E. Havenith, F. J. Beurskens, J. M. Bakker, C. M. Lanigan, G. Landucci, D. N. Forthal, P. W. Parren, et al. 2007. Fc receptor but not complement binding is important in antibody protection against HIV. Nature 449: 101-104. (Pubitemid 47373775)
61. Ravetch, J. V., and S. Bolland. 2001. IgG Fc receptors. Annu. Rev. Immunol. 19: 275-290. (Pubitemid 32368037)
62. Regnault, A., D. Lankar, V. Lacabanne, A. Rodriguez, C. Théry, M. Rescigno, T. Saito, S. Verbeek, C. Bonnerot, P. Ricciardi-Castagnoli, and S. Amigorena. 1999. Fcg receptor-mediated induction of dendritic cell maturation and major histocompatibility complex class I-restricted antigen presentation after immune complex internalization. J. Exp. Med. 189: 371-380. (Pubitemid 29063258)
63. Rodriguez, A., A. Regnault, M. Kleijmeer, P. Ricciardi-Castagnoli, and S. Amigorena. 1999. Selective transport of internalized antigens to the cytosol for MHC class I presentation in dendritic cells. Nat. Cell Biol. 1: 362-368. (Pubitemid 129493579)
64. Bergtold, A., D. D. Desai, A. Gavhane, and R. Clynes. 2005. Cell surface recycling of internalized antigen permits dendritic cell priming of B cells. Immunity 23: 503-514. (Pubitemid 41587890)
65. Dhodapkar, K. M., J. Krasovsky, B. Williamson, and M. V. Dhodapkar. 2002. Antitumor monoclonal antibodies enhance cross-presentation of cellular antigens and the generation of myeloma-specific killer T cells by dendritic cells. J. Exp. Med. 195: 125-133. (Pubitemid 34074502)
66. Groh, V., Y. Q. Li, D. Cioca, N. N. Hunder, W. Wang, S. R. Riddell, C. Yee, and T. Spies. 2005. Efficient cross-priming of tumor antigen-specific T cells by dendritic cells sensitized with diverse anti-MICA opsonized tumor cells. Proc. Natl. Acad. Sci. USA 102: 6461-6466. (Pubitemid 40617465)
67. Harbers, S. O., A. Crocker, G. Catalano, V. D'Agati, S. Jung, D. D. Desai, and R. Clynes. 2007. Antibody-enhanced cross-presentation of self antigen breaks T cell tolerance. J. Clin. Invest. 117: 1361-1369. (Pubitemid 46718424)
68. Machy, P., K. Serre, and L. Leserman. 2000. Class I-restricted presentation of exogenous antigen acquired by Fcg receptor-mediated endocytosis is regulated in dendritic cells. Eur. J. Immunol. 30: 848-857. (Pubitemid 30216258)
69. Zheng, B., Y. Zhang, H. He, E. Marinova, K. Switzer, D. Wansley, I. Mbawuike, and S. Han. 2007. Rectification of age-associated deficiency in cytotoxic T cell response to influenza A virus by immunization with immune complexes. J. Immunol. 179: 6153-6159.
70. Yager, E. J., M. Ahmed, K. Lanzer, T. D. Randall, D. L. Woodland, and M. A. Blackman. 2008. Age-associated decline in T cell repertoire diversity leads to holes in the repertoire and impaired immunity to influenza virus. J. Exp. Med. 205: 711-723. (Pubitemid 351439315)
71. La Gruta, N. L., W. T. Rothwell, T. Cukalac, N. G. Swan, S. A. Valkenburg, K. Kedzierska, P. G. Thomas, P. C. Doherty, and S. J. Turner. 2010. Primary CTL response magnitude in mice is determined by the extent of naive T cell recruitment and subsequent clonal expansion. J. Clin. Invest. 120: 1885-1894.
72. Crowe, S. R., S. C. Miller, R. M. Shenyo, and D. L. Woodland. 2005. Vaccination with an acidic polymerase epitope of influenza virus elicits a potent antiviral T cell response but delayed clearance of an influenza virus challenge. J. Immunol. 174: 696-701. (Pubitemid 40094262)
73. Crowe, S. R., S. C. Miller, and D. L. Woodland. 2006. Identification of protective and non-protective T cell epitopes in influenza. Vaccine 24: 452-456. (Pubitemid 41832548)
74. Endo, A., S. Itamura, H. Iinuma, S. Funahashi, H. Shida, F. Koide, K. Nerome, and A. Oya. 1991. Homotypic and heterotypic protection against influenza virus infection in mice by recombinant vaccinia virus expressing the haemagglutinin or nucleoprotein of influenza virus. J. Gen. Virol. 72: 699-703.
75. + T cell immunodominance in primary and secondary influenza virus infections. J. Exp. Med. 198: 399-410. (Pubitemid 36980611)
76. Amanna, I. J., N. E. Carlson, and M. K. Slifka. 2007. Duration of humoral immunity to common viral and vaccine antigens. N. Engl. J. Med. 357: 1903-1915. (Pubitemid 350074686)
77. Hammarlund, E., M. W. Lewis, S. G. Hansen, L. I. Strelow, J. A. Nelson, G. J. Sexton, J. M. Hanifin, and M. K. Slifka. 2003. Duration of antiviral immunity after smallpox vaccination. Nat. Med. 9: 1131-1137. (Pubitemid 37173696)