Impaired heterologous immunity in aged ferrets during sequential influenza A H1N1 infection

Virology

Volumn 464-465, Issue 1, 2014, Pages 177-183

  Paquette, Stéphane G ^a,b   Huang, Stephen S H ^a,b   Banner, David ^a   Xu, Luoling ^a   Lén, Alberto ^a   Kelvin, Alyson A ^c   Kelvin, David J ^a,b,d,e,f  

^a UNIVERSITY HEALTH NETWORK   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c Immune Diagnostics and Research   (Canada)

^d SHANTOU UNIVERSITY MEDICAL COLLEGE   (China)

^e Guangdong Provincial Key Laboratory of Infectious Diseases and Molecular Immunopathology   (China)

^f UNIVERSITY OF SASSARI   (Italy)

Author keywords

Aging; Ferret model; Heterologous immunity; Humoral response; Immunological senescence; Influenza; Influenza A H1N1; Pandemic influenza; T cells

Indexed keywords

HEMAGGLUTININ; INFLUENZA VACCINE; INFLUENZA VIRUS HEMAGGLUTININ; VIRUS ANTIBODY;

2009 H1N1 INFLUENZA; ADULT; AGED; AGING; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY PRODUCTION; ANTIBODY RESPONSE; ARTICLE; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE SEVERITY; FERRET; IMMUNE RESPONSE; IMMUNOREGULATION; INFECTION RESISTANCE; MALE; MORBIDITY; NONHUMAN; PRIORITY JOURNAL; RESPIRATORY TRACT DISEASE; T LYMPHOCYTE; WEIGHT REDUCTION; YOUNG ADULT; AGE; ANIMAL; DISEASE MODEL; GENETICS; HETEROLOGOUS IMMUNITY; HUMAN; IMMUNOLOGY; INFLUENZA; INFLUENZA VIRUS A H1N1; VIROLOGY;

AGE FACTORS; AGED; AGING; ANIMALS; ANTIBODIES, VIRAL; DISEASE MODELS, ANIMAL; FERRETS; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; HUMANS; IMMUNITY, HETEROLOGOUS; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA VACCINES; INFLUENZA, HUMAN; MALE; T-LYMPHOCYTES;

EID: 84922392070     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2014.07.013     Document Type: Article

References (42)

1. Anthony D.A., Andrews D.M., Watt S.V., Trapani J.A., Smyth M.J. Functional dissection of the granzyme family: cell death and inflammation. Immunol. Rev. 2010, 235:73-92.
2. Aw D., Palmer D.B. The origin and implication of thymic involution. Aging Dis. 2011, 2:437-443.
3. Banner D., Kelvin A.A. The current state of H5N1 vaccines and the use of the ferret model for influenza therapeutic and prophylactic development. J. Infect. Dev. Ctries. 2012, 6:465-469.
4. Behzad H., Huckriede A.L., Haynes L., Gentleman B., Coyle K., Wilschut J.C., Kollmann T.R., Reed S.G., McElhaney J.E. GLA-SE, a synthetic toll-like receptor 4 agonist, enhances T-cell responses to influenza vaccine in older adults. J. Infect. Dis. 2012, 205:466-473.
5. Belser J.A., Katz J.M., Tumpey T.M. The ferret as a model organism to study influenza A virus infection. Dis. Models Mech. 2011, 4:575-579.
6. Bender B.S., Small P.A.S. Heterotypic immune mice lose protection against influenza virus infection with senescence. J. Infect. Dis. 1993, 168:873-880.
7. Bridges C., Winquist A., Fukuda K., Cox N.J., Singleton J., Strikas R. Prevention and control of influenza: recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWR Recomm. Rep. 2000, 49:1-38.
8. Buchholz V.R., Neuenhahn M., Busch D.H. CD8+ T cell differentiation in the aging immune system: until the last clone standing. Curr. Opin. Immunol. 2011, 23:549-554.
9. Castle S.C. Clinical relevance of age-related immune dysfunction. Clin. Infect. Dis. 2000, 31:578-585.
10. Centers for Disease Control and Prevention (CDC) Influenza activity-United States, 2012-13 season and composition of the 2013-14 influenza vaccine. MMWR Morb. Mortal. Wkly. Rep. 2013, 62:473-479.
11. Cheng X., Zengel J.R., Suguitan A.L., Xu Q., Wang W., Lin J., Jin H. Evaluation of the humoral and cellular immune responses elicited by the live attenuated and inactivated influenza vaccines and their roles in heterologous protection in ferrets. J. Infect. Dis. 2013, 208:594-602.
12. Dao C.N., Kamimoto L., Nowell M., Reingold A., Gershman K., Meek J., Arnold K.E., Farley M., Ryan P., Lynfield R. Adult hospitalizations for laboratory-positive influenza during the 2005-2006 through 2007-2008 seasons in the United States. J. Infect. Dis. 2010, 202:881-888.
13. Decman V., Laidlaw B.J., DiMenna L.J., Abdulla S., Mozdzanowska K., Erikson J., Ertl H.C., Wherry E.J. Cell-intrinsic defects in the proliferative response of antiviral memory CD8 T cells in aged mice upon secondary infection. J. Immunol. 2010, 184:5151-5159.
14. Deng Y., Jing Y., Campbell A.E., Gravenstein S. Age-related impaired type 1 T cell responses to influenza: reduced activation ex vivo, decreased expansion in CTL culture in vitro, and blunted response to influenza vaccination in vivo in the elderly. J. Immunol. 2004, 172:3437-3446.
15. Eaton S.M., Burns E.M., Kusser K., Randall T.D., Haynes L. Age-related defects in CD4 T cell cognate helper function lead to reductions in humoral responses. J. Exp. Med. 2004, 200:1613-1622.
16. Effros R.B., Cai Z., Linton P.-J. CD8 T cells and aging. Crit. Rev. Immunol. 2003, 23:45-64.
17. Fang Y., Banner D., Kelvin A.A., Huang S.S., Paige C.J., Corfe S.A., Kane K.P., Bleackley R.C., Rowe T., Leon A.J., Kelvin D.J. Seasonal H1N1 influenza virus infection induces cross-protective pandemic H1N1 virus immunity through a CD8-independent, B cell-dependent mechanism. J. Virol. 2012, 86:2229-2238.
18. Grivennikov S.I., Tumanov A.V., Liepinsh D.J., Kruglov A.A., Marakusha B.I., Shakhov A.N., Murakami T., Drutskaya L.N., Förster I., Clausen B.E. Distinct and nonredundant in vivo functions of TNF produced by t cells and macrophages/neutrophils: protective and deleterious effects. Immunity 2005, 22:93-104.
19. Guo H., Santiago F., Lambert K., Takimoto T., Topham D.J. T cell-mediated protection against lethal 2009 pandemic H1N1 influenza virus infection in a mouse model. J. Virol. 2011, 85:448-455.
20. Guo J., Feng Y., Barnes P., Huang F.-F., Idell S., Su D.-M., Shams H. Deletion of FoxN1 in the thymic medullary epithelium reduces peripheral T cell responses to infection and mimics changes of aging. PLoS One 2012, 7:e34681.
21. Haynes L., Eaton S.M., Burns E.M., Randall T.D., Swain S.L. Newly generated CD4 T cells in aged animals do not exhibit age-related defects in response to antigen. J. Exp. Med. 2005, 201:845-851.
22. Huang S.S., Banner D., Degousee N., Leon A.J., Xu L., Paquette S.G., Kanagasabai T., Fang Y., Rubino S., Rubin B., Kelvin D.J., Kelvin A.A. Differential pathological and immune responses in newly weaned ferrets are associated with a mild clinical outcome of pandemic 2009 H1N1 infection. J. Virol. 2012, 86:13187-13201.
23. Huang S.S., Banner D., Fang Y., Ng D.C., Kanagasabai T., Kelvin D.J., Kelvin A.A. Comparative analyses of pandemic H1N1 and seasonal H1N1, H3N2, and influenza B infections depict distinct clinical pictures in ferrets. PLoS One 2011, 6:e27512.
24. Huang S.S., Lin Z., Banner D., León A.J., Paquette S.G., Rubin B., Rubino S., Guan Y., Kelvin D.J., Kelvin A.A. Immunity toward H1N1 influenza hemagglutinin of historical and contemporary strains suggests protection and vaccine failure. Sci. Rep. 2013, 3:1698.
25. Jang Y.H., Byun Y.H., Lee D.-H., Lee K.-H., Lee Y.J., Lee Y.H., Park J.-K., Song C.-S., Seong B.L. Cold-adapted X-31 live attenuated 2009 pandemic H1N1 influenza vaccine elicits protective immune responses in mice and ferrets. Vaccine 2013, 31:1320-1327.
26. Jones S.C., Brahmakshatriya V., Huston G., Dibble J., Swain S.L. TLR-activated dendritic cells enhance the response of aged naive CD4 T cells via an IL-6-dependent mechanism. J. Immunol. 2010, 185:6783-6794.
27. Josset L., Engelmann F., Haberthur K., Kelly S., Park B., Kawoaka Y., García-Sastre A., Katze M.G., Messaoudi I. Increased viral loads and exacerbated innate host responses in aged macaques infected with the 2009 pandemic H1N1 influenza A virus. J. Virol. 2012, 86:11115-11127.
28. Kelvin A.A., Degousee N., Banner D., Stefanski E., Leon A.J., Angoulvant D., Paquette S.G., Huang S.S., Danesh A., Robbins C.S., Noyan H., Husain M., Lambeau G., Gelb M., Kelvin D.J., Rubin B.B. Lack of group X secreted phospholipase A2 increases survival following pandemic H1N1 influenza infection. Virology 2014, 454-455:78-92.
29. McElhaney J.E. The unmet need in the elderly: designing new influenza vaccines for older adults. Vaccine 2005, 23:S10-S25.
30. Muto N.A., Sunden Y., Hattori T., Fujikura D., Nakayama Y., Miyazaki T., Maruyama M., Kimura T., Sawa H. Pathological examination of lung tissues in influenza A virus-infected mice. Jpn. J. Infect. Dis. 2012, 65:383-391.
31. Naylor K., Li G., Vallejo A.N., Lee W.-W., Koetz K., Bryl E., Witkowski J., Fulbright J., Weyand C.M., Goronzy J.J. The influence of age on T cell generation and TCR diversity. J. Immunol. 2005, 174:7446-7452.
32. O'Donnell C.D., Wright A., Vogel L.N., Wei C.-J., Nabel G.J., Subbarao K. Effect of priming with H1N1 influenza viruses of variable antigenic distances on challenge with 2009 pandemic H1N1 virus. J. Virol. 2012, 86:8625-8633.
33. Paquette S.G., Banner D., Chi L.T.B., Lén A.J., Xu L., Ran L., Huang S.S., Farooqui A., Kelvin D.J., Kelvin A.A. Pandemic H1N1 influenza A directly induces a robust and acute inflammatory gene signature in primary human bronchial epithelial cells downstream of membrane fusion. Virology 2014, 448:91-103.
34. Pica N., Langlois R.A., Krammer F., Margine I., Palese P. NS1-truncated live attenuated virus vaccine provides robust protection to aged mice from viral challenge. J. Virol. 2012, 86:10293-10301.
35. Rowe T., León A.J., Crevar C.J., Carter D.M., Xu L., Ran L., Fang Y., Cameron C.M., Cameron M.J., Banner D., Ng D.C., Ran R., Weirback H.K., Wiley C.A., Kelvin D.J., Ross T.M. Modeling host responses in ferrets during A/California/07/2009 influenza infection. Virology 2010, 401:257-265.
36. Rudd B.D., Venturi V., Li G., Samadder P., Ertelt J.M., Way S.S., Davenport M.P., Nikolich-Žugich J. Nonrandom attrition of the naive CD8+ T-cell pool with aging governed by T-cell receptor: pMHC interactions. Proc. Natl. Acad. Sci. USA 2011, 108:13694-13699.
37. Sullivan B.M., Juedes A., Szabo S.J., von Herrath M., Glimcher L.H. Antigen-driven effector CD8 T cell function regulated by T-bet. Proc. Natl. Acad. Sci. USA 2003, 100:15818-15823.
38. Szabo S.J., Kim S.T., Costa G.L., Zhang X., Fathman C.G., Glimcher L.H. .1A novel transcription factor, T-bet, directs Th1 lineage commitment. Cell 2000, 100:655-669.
39. Thompson W.W., Shay D.K., Weintraub E., Brammer L., Cox N., Anderson L.J., Fukuda K. Mortality associated with influenza and respiratory syncytial virus in the United States. J. Am. Med. Assoc. 2003, 289:179-186.
40. Tu W., Mao H., Zheng J., Liu Y., Chiu S.S., Qin G., Chan P.-L., Lam K.-T., Guan J., Zhang L. Cytotoxic T lymphocytes established by seasonal human influenza cross-react against 2009 pandemic H1N1 influenza virus. J. Virol. 2010, 84:6527-6535.
41. Xu L., Yoon H., Zhao M.Q., Liu J., Ramana C.V., Enelow R.I. Cutting edge: pulmonary immunopathology mediated by antigen-specific expression of TNF-α by antiviral CD8+ T cells. J. Immunol. 2004, 173:721-725.
42. Yager E.J., Ahmed M., Lanzer K., Randall T.D., Woodland D.L., Blackman M.A. Age-associated decline in T cell repertoire diversity leads to holes in the repertoire and impaired immunity to influenza virus. J. Exp. Med. 2008, 205:711-723.