Antibody-dependent cellular cytotoxicity is associated with control of pandemic H1N1 influenza virus infection of macaques

Journal of Virology

Volumn 87, Issue 10, 2013, Pages 5512-5522

  Jegaskanda, Sinthujan ^a   Weinfurter, Jason T ^b,c   Friedrich, Thomas C ^b,c   Kenta, Stephen J ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b UNIVERSITY OF WISCONSIN   (United States)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INFLUENZA VIRUS HEMAGGLUTININ; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; NEUTRALIZING ANTIBODY;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ANTIBODY DETECTION; ANTIBODY SPECIFICITY; ANTIGEN EXPRESSION; ARTICLE; CELL EXPANSION; CELL FUNCTION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CROSS REACTION; INFECTION CONTROL; INFLUENZA A (H1N1); LUNG LAVAGE; LYMPHOCYTE ACTIVATION; MOLECULAR DYNAMICS; NATURAL KILLER CELL; NONHUMAN; PANDEMIC INFLUENZA; PRIORITY JOURNAL; RHESUS MONKEY; VIRAL CLEARANCE; VIRUS INHIBITION; VIRUS STRAIN;

ANIMALS; ANTIBODIES, VIRAL; ANTIBODY-DEPENDENT CELL CYTOTOXICITY; BRONCHOALVEOLAR LAVAGE FLUID; CROSS REACTIONS; GENE EXPRESSION; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; INFLUENZA A VIRUS, H1N1 SUBTYPE; INTERFERON-GAMMA; KILLER CELLS, NATURAL; LYSOSOMAL-ASSOCIATED MEMBRANE PROTEIN 1; MACACA MULATTA; ORTHOMYXOVIRIDAE INFECTIONS; PRIMATE DISEASES;

EID: 84877317499     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.03030-12     Document Type: Article

References (58)

1. Osterholm MT, Kelley NS, Sommer A, Belongia EA. 2012. Efficacy and effectiveness of influenza vaccines: a systematic review and meta-analysis. Lancet Infect. Dis. 12:36-44.
2. Eick-Cost AA, Tastad KJ, Guerrero AC, Johns MC, Lee SE, Macintosh VH, Burke RL, Blazes DL, Russell KL, Sanchez JL. 2012. Effectiveness of seasonal influenza vaccines against influenza-associated illnesses among US military personnel in 2010-11: a case-control approach. PLoS One 7:e41435. doi:10.1371/journal.pone.0041435.
3. Johns MC, Eick AA, Blazes DL, Lee SE, Perdue CL, Lipnick R, Vest KG, Russell KL, DeFraites RF, Sanchez JL. 2010. Seasonal influenza vaccine and protection against pandemic (H1N1) 2009-associated illness among US military personnel. PLoS One 5:e10722. doi:10.1371/journal.pone .0010722.
4. Pebody RG, Andrews N, Fleming DM, McMenamin J, Cottrell S, Smyth B, Durnall H, Robertson C, Carman W, Ellis J, Sebastian-Pillai P, Zambon M, Kearns C, Moore C, Thomas DR, Watson JM. 2012. Age-specific vaccine effectiveness of seasonal 2010/2011 and pandemic influenza A(H1N1) 2009 vaccines in preventing influenza in the United Kingdom. Epidemiol. Infect. 2012:1-11.
5. Skowronski DM, Janjua NZ, De Serres G, Purych D, Gilca V, Scheifele DW, Dionne M, Sabaiduc S, Gardy JL, Li G, Bastien N, Petric M, Boivin G, Li Y. 2012. Cross-reactive and vaccine-induced antibody to emerging swine-origin variant of influenza A virus subtype H3N2 (H3N2v). J. Infect. Dis. 206:1852-1861.
6. Centers for Disease Control and Prevention. 2009. Effectiveness of 2008-09 trivalent influenza vaccine against 2009 pandemic influenza A (H1N1)-United States, May-June 2009. MMWR Morb. Mortal. Wkly. Rep. 58:1241-1245.
7. Cowling BJ, Ng S, Ma ES, Fang VJ, So HC, Wai W, Cheng CK, Wong JY, Chan KH, Ip DK, Chiu SS, Peiris JS, Leung GM. 2012. Protective efficacy against pandemic influenza of seasonal influenza vaccination in children in Hong Kong: a randomized controlled trial. Clin. Infect. Dis. 55:695-702.
8. Burton DR, Poignard P, Stanfield RL, Wilson IA. 2012. Broadly neutralizing antibodies present new prospects to counter highly antigenically diverse viruses. Science 337:183-186.
9. Ekiert DC, Wilson IA. 2012. Broadly neutralizing antibodies against influenza virus and prospects for universal therapies. Curr. Opin. Virol. 2:134 -141.
10. Terajima M, Cruz J, Co MD, Lee JH, Kaur K, Wrammert J, Wilson PC, Ennis FA. 2011. Complement-dependent lysis of influenza A virusinfected cells by broadly cross-reactive human monoclonal antibodies. J. Virol. 85:13463-13467.
11. Krause JC, Tsibane T, Tumpey TM, Huffman CJ, Basler CF, Crowe JE, Jr. 2011. A broadly neutralizing human monoclonal antibody that recognizes a conserved, novel epitope on the globular head of the influenza H1N1 virus hemagglutinin. J. Virol. 85:10905-10908.
12. Thomson CA, Wang Y, Jackson LM, Olson M, Wang W, Liavonchanka A, Keleta L, Silva V, Diederich S, Jones RB, Gubbay J, Pasick J, Petric M, Jean F, Allen VG, Brown EG, Rini JM, Schrader JW. 2012. Pandemic H1N1 influenza infection and vaccination in humans induces crossprotective antibodies that target the hemagglutinin stem. Front. Immunol. 3:87.
13. Ohshima N, Iba Y, Kubota-Koketsu R, Asano Y, Okuno Y, Kurosawa Y. 2011. Naturally occurring antibodies in humans can neutralize a variety of influenza virus strains, including H3, H1, H2, and H5. J. Virol. 85:11048- 11057.
14. Corti D, Voss J, Gamblin SJ, Codoni G, Macagno A, Jarrossay D, Vachieri SG, Pinna D, Minola A, Vanzetta F, Silacci C, Fernandez- Rodriguez BM, Agatic G, Bianchi S, Giacchetto-Sasselli I, Calder L, Sallusto F, Collins P, Haire LF, Temperton N, Langedijk JP, Skehel JJ, Lanzavecchia A. 2011. A neutralizing antibody selected from plasma cells that binds to group 1 and group 2 influenza A hemagglutinins. Science 333:850-856.
15. Effros RB, Doherty PC, Gerhard W, Bennink J. 1977. Generation of both cross-reactive and virus-specific T-cell populations after immunization with serologically distinct influenza A viruses. J. Exp. Med. 145:557-568.
16. Wilkinson TM, Li CK, Chui CS, Huang AK, Perkins M, Liebner JC, Lambkin-Williams R, Gilbert A, Oxford J, Nicholas B, Staples KJ, Dong T, Douek DC, McMichael AJ, Xu XN. 2012. Preexisting influenzaspecific CD4 T cells correlate with disease protection against influenza challenge in humans. Nat. Med. 18:274 -280.
17. Weinfurter JT, Brunner K, Capuano SV, 3rd, Li C, Broman KW, Kawaoka Y, Friedrich TC. 2011. Cross-reactive T cells are involved in rapid clearance of 2009 pandemic H1N1 influenza virus in nonhuman primates. PLoS Pathog. 7:e1002381. doi:10.1371/journal.ppat.1002381.
18. Laurie KL, Carolan LA, Middleton D, Lowther S, Kelso A, Barr IG. 2010. Multiple infections with seasonal influenza A virus induce crossprotective immunity against A(H1N1) pandemic influenza virus in a ferret model. J. Infect. Dis. 202:1011-1020.
19. Epstein SL. 2006. Prior H1N1 influenza infection and susceptibility of Cleveland Family Study participants during the H2N2 pandemic of 1957: an experiment of nature. J. Infect. Dis. 193:49 -53.
20. McMichael AJ, Gotch FM, Noble GR, Beare PA. 1983. Cytotoxic T-cell immunity to influenza. N. Engl. J. Med. 309:13-17.
21. Yap KL, Ada GL, McKenzie IF. 1978. Transfer of specific cytotoxic T lymphocytes protects mice inoculated with influenza virus. Nature 273: 238-239.
22. Kreijtz JH, Bodewes R, van Amerongen G, Kuiken T, Fouchier RA, Osterhaus AD, Rimmelzwaan GF. 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.
23. O'Donnell CD, Wright A, Vogel LN, Wei CJ, Nabel GJ, Subbarao K. 2012. Effect of priming with H1N1 influenza viruses of variable antigenic distances on challenge with 2009 pandemic H1N1 virus. J. Virol. 86:8625- 8633.
24. Min JY, Chen GL, Santos C, Lamirande EW, Matsuoka Y, Subbarao K. 2010. Classical swine H1N1 influenza viruses confer cross protection from swine-origin 2009 pandemic H1N1 influenza virus infection in mice and ferrets. Virology 408:128 -133.
25. Chen GL, Lau YF, Lamirande EW, McCall AW, Subbarao K. 2011. Seasonal influenza infection and live vaccine prime for a response to the 2009 pandemic H1N1 vaccine. Proc. Natl. Acad. Sci. U. S. A. 108:1140- 1145.
26. Manicassamy B, Medina RA, Hai R, Tsibane T, Stertz S, Nistal-Villan E, Palese P, Basler CF, Garcia-Sastre A. 2010. Protection of mice against lethal challenge with 2009 H1N1 influenza A virus by 1918-like and classical swine H1N1 based vaccines. PLoS Pathog. 6:e1000745. doi:10.1371 /journal.ppat.1000745.
27. Tu W, Mao H, Zheng J, Liu Y, Chiu SS, Qin G, Chan PL, Lam KT, Guan J, Zhang L, Guan Y, Yuen KY, Peiris JS, Lau YL. 2010. Cytotoxic T lymphocytes established by seasonal human influenza cross-react against 2009 pandemic H1N1 influenza virus. J. Virol. 84:6527- 6535.
28. Scheible K, Zhang G, Baer J, Azadniv M, Lambert K, Pryhuber G, Treanor JJ, Topham DJ. 2011. CD8+ T cell immunity to 2009 pandemic and seasonal H1N1 influenza viruses. Vaccine 29:2159 -2168.
29. Fang Y, Banner D, Kelvin AA, Huang SS, Paige CJ, Corfe SA, Kane KP, Bleackley RC, Rowe T, Leon AJ, Kelvin DJ. 2012. Seasonal H1N1 influenza virus infection induces cross-protective pandemic H1N1 virus immunity through a CD8-independent, B cell-dependent mechanism. J. Virol. 86:2229 -2238.
30. Huber VC, Lynch JM, Bucher DJ, Le J, Metzger DW. 2001. Fc receptormediated phagocytosis makes a significant contribution to clearance of influenza virus infections. J. Immunol. 166:7381-7388.
31. El Bakkouri K, Descamps F, De Filette M, Smet A, Festjens E, Birkett A, Van Rooijen N, Verbeek S, Fiers W, Saelens X. 2011. Universal vaccine based on ectodomain of matrix protein 2 of influenza A: Fc receptors and alveolar macrophages mediate protection. J. Immunol. 186: 1022-1031.
32. Jegerlehner A, Schmitz N, Storni T, Bachmann MF. 2004. Influenza A vaccine based on the extracellular domain of M2: weak protection mediated via antibody-dependent NK cell activity. J. Immunol. 172:5598- 5605.
33. Hashimoto G, Wright PF, Karzon DT. 1983. Antibody-dependent cellmediated cytotoxicity against influenza virus-infected cells. J. Infect. Dis. 148:785-794.
34. Hashimoto G, Wright PF, Karzon DT. 1983. Ability of human cord blood lymphocytes to mediate antibody-dependent cellular cytotoxicity against influenza virus-infected cells. Infect. Immun. 42:214 -218.
35. Ge MQ, Ho AW, Tang Y, Wong KH, Chua BY, Gasser S, Kemeny DM. 2012. NK cells regulate CD8T cell priming and dendritic cell migration during influenza A infection by IFN-α and perforin-dependent mechanisms. J. Immunol. 189:2099 -2109.
36. Fox A, Le NM, Horby P, van Doorn HR, Nguyen VT, Nguyen HH, Nguyen TC, Vu DP, Nguyen MH, Diep NT, Bich VT, Huong HT, Taylor WR, Farrar J, Wertheim H, Nguyen VK. 2012. Severe pandemic H1N1 2009 infection is associated with transient NK and T deficiency and aberrant CD8 responses. PLoS One 7:e31535. doi:10.1371/journal.pone .0031535.
37. Beli E, Clinthorne JF, Duriancik DM, Hwang I, Kim S, Gardner EM. 2011. Natural killer cell function is altered during the primary response of aged mice to influenza infection. Mech. Ageing Dev. 132:503-510.
38. Chung AW, Isitman G, Navis M, Kramski M, Center RJ, Kent SJ, Stratov I. 2011. Immune escape from HIV-specific antibody-dependent cellular cytotoxicity (ADCC) pressure. Proc. Natl. Acad. Sci. U. S. A. 108: 7505-7510.
39. Isitman G, Chung AW, Navis M, Kent SJ, Stratov I. 2011. Pol as a target for antibody dependent cellular cytotoxicity responses in HIV-1 infection. Virology 412:110 -116.
40. Shinya K, Gao Y, Cilloniz C, Suzuki Y, Fujie M, Deng G, Zhu Q, Fan S, Makino A, Muramoto Y, Fukuyama S, Tamura D, Noda T, Eisfeld AJ, Katze MG, Chen H, Kawaoka Y. 2012. Integrated clinical, pathologic, virologic, and transcriptomic analysis of H5N1 influenza virusinduced viral pneumonia in the rhesus macaque. J. Virol. 86:6055- 6066.
41. Giles BM, Crevar CJ, Carter DM, Bissel SJ, Schultz-Cherry S, Wiley CA, Ross TM. 2012. A computationally optimized hemagglutinin virus-like particle vaccine elicits broadly reactive antibodies that protect nonhuman primates from H5N1 infection. J. Infect. Dis. 205:1562-1570.
42. Jegaskanda S, Reece JC, De Rose R, Stambas J, Sullivan L, Brooks AG, Kent SJ, Sexton A. 2012. Comparison of influenza and SIV specific CD8 T cell responses in macaques. PLoS One 7:e32431. doi:10.1371/journal .pone.0032431.
43. National Research Council. 2011. Guide for the care and use of laboratory animals, 8th ed. National Academies Press, Washington, DC.
44. Weatherall D. 2006. The use of non-human primates in research: a working group report. Medical Research Council, London, United Kingdom.
45. Sexton A, De Rose R, Reece JC, Alcantara S, Loh L, Moffat JM, Laurie K, Hurt A, Doherty PC, Turner SJ, Kent SJ, Stambas J. 2009. Evaluation of recombinant influenza virus-simian immunodeficiency virus vaccines in macaques. J. Virol. 83:7619 -7628.
46. Neumann G, Watanabe T, Ito H, Watanabe S, Goto H, Gao P, Hughes M, Perez DR, Donis R, Hoffmann E, Hobom G, Kawaoka Y. 1999. Generation of influenza A viruses entirely from cloned cDNAs. Proc. Natl. Acad. Sci. U. S. A. 96:9345-9350.
47. Hoffmann E, Neumann G, Kawaoka Y, Hobom G, Webster RG. 2000. A DNA transfection system for generation of influenza A virus from eight plasmids. Proc. Natl. Acad. Sci. U. S. A. 97:6108-6113.
48. Cox N. 2002. WHO manual on animal influenza diagnosis and surveillance. WHO, Geneva, Switzerland.
49. Pica N, Hai R, Krammer F, Wang TT, Maamary J, Eggink D, Tan GS, Krause JC, Moran T, Stein CR, Banach D, Wrammert J, Belshe RB, Garcia-Sastre A, Palese P. 2012. Hemagglutinin stalk antibodies elicited by the 2009 pandemic influenza virus as a mechanism for the extinction of seasonal H1N1 viruses. Proc. Natl. Acad. Sci. U. S. A. 109:2573-2578.
50. Chung AW, Navis M, Isitman G, Wren L, Silvers J, Amin J, Kent SJ, Stratov I. 2011. Activation of NK cells by ADCC antibodies and HIV disease progression. J. Acquir. Immune Defic. Syndr. 58:127-131.
51. Ellebedy AH, Ducatez MF, Duan S, Stigger-Rosser E, Rubrum AM, Govorkova EA, Webster RG, Webby RJ. 2011. Impact of prior seasonal influenza vaccination and infection on pandemic A (H1N1) influenza virus replication in ferrets. Vaccine 29:3335-3339.
52. Chung AW, Rollman E, Center RJ, Kent SJ, Stratov I. 2009. Rapid degranulation ofNKcells following activation by HIV-specific antibodies. J. Immunol. 182:1202-1210.
53. Lillie PJ, Berthoud TK, Powell TJ, Lambe T, Mullarkey C, Spencer AJ, Hamill M, Peng Y, Blais ME, Duncan CJ, Sheehy SH, Havelock T, Faust SN, Williams RL, Gilbert A, Oxford J, Dong T, Hill AV, Gilbert SC. 2012. Preliminary assessment of the efficacy of a T-cell-based influenza vaccine, MVA-NPM1, in humans. Clin. Infect. Dis. 55:19 -25.
54. Budde ML, Wiseman RW, Karl JA, Hanczaruk B, Simen BB, O'Connor DH. 2010. Characterization of Mauritian cynomolgus macaque major histocompatibility complex class I haplotypes by high-resolution pyrosequencing. Immunogenetics 62:773-780.
55. Fernandez CS, Reece JC, Saepuloh U, De Rose R, Ishkandriati D, O'Connor DH, Wiseman RW, Kent SJ. 2011. Screening and confirmatory testing of MHC class I alleles in pig-tailed macaques. Immunogenetics 63:511-521.
56. Shen X, Soderholm J, Lin F, Kobinger G, Bello A, Gregg DA, Broderick KE, Sardesai NY. 2012. Influenza A vaccines using linear expression cassettes delivered via electroporation afford full protection against challenge in a mouse model. Vaccine 30:6946-6954.
57. Jegaskanda S, Job ER, Kramski M, Laurie K, Isitman G, de Rose R, Winnall WR, Stratov I, Brooks AG, Reading PC, Kent SJ. 2013. Crossreactive influenza-specific antibody-dependent cellular cytotoxicity antibodies in the absence of neutralizing antibodies. J. Immunol. 190:1837- 1848.
58. Jegaskanda S, Laurie K, Amarasena T, Winnall W, Kramski M, De Rose R, Barr I, Brooks A, Reading PC, Kent SJ. Age-associated cross-reactive ADCC toward 2009-pandemic influenza. J. Infect. Dis., in press.