Vaccine-Induced Boosting of Influenza Virus-Specific CD4 T Cells in Younger and Aged Humans

PLoS ONE

Volumn 8, Issue 10, 2013, Pages

  Dolfi, Douglas V ^a   Mansfield, Kathleen D ^a   Kurupati, Raj K ^b   Kannan, Senthil ^b,d   Doyle, Susan A ^c   Ertl, Hildegund C J ^b   Schmader, Kenneth E ^c   Wherry, E John ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b WISTAR INSTITUTE   (United States)

^c DURHAM VA MEDICAL CENTER   (United States)

^d UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INFLUENZA VACCINE; INFLUENZA VIRUS HEMAGGLUTININ; NEUTRALIZING ANTIBODY; NUCLEOCAPSID PROTEIN; VIRUS PROTEIN;

ADULT; AGED; ANTIGEN SPECIFICITY; ARTICLE; CD4+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; CROSS REACTION; DRUG RESPONSE; FEMALE; HUMAN; HUMAN CELL; INFLUENZA; INFLUENZA VACCINATION; MALE; VIRUS STRAIN;

ADULT; AGED; AGING; ANTIBODIES, NEUTRALIZING; CD4-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; CELL PROLIFERATION; DEMOGRAPHY; FEMALE; HUMANS; INFLUENZA VACCINES; KINETICS; MALE; ORTHOMYXOVIRIDAE; SPECIES SPECIFICITY; VACCINES, INACTIVATED; VIRAL PROTEINS;

EID: 84885416699     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0077164     Document Type: Article

References (42)

1. Centers for Disease Control and Prevention (CDC) (2013) Interim adjusted estimates of seasonal influenza vaccine effectiveness- United States, February 2013. MMWR Morb Mortal Wkly Rep 62: 119-123. PubMed: 23425960.
2. Richards KA, Chaves FA, Alam S, Sant AJ, (2012) Trivalent inactivated influenza vaccines induce broad immunological reactivity to both internal virion components and influenza surface proteins. Vaccine 31: 219-225. doi:10.1016/j.vaccine.2012.10.039. PubMed: 23099328.
3. Berthoud TK, Hamill M, Lillie PJ, Hwenda L, Collins KA, et al. (2011) Potent CD8+ T-cell immunogenicity in humans of a novel heterosubtypic influenza A vaccine, MVA-NP+M1. Clin Infect Dis 52: 1-7. doi:10.1093/cid/ciq039. PubMed: 21148512.
4. Luo J, Zheng D, Zhang W, Fang F, Wang H, et al. (2012) Induction of cross-protection against influenza A virus by DNA prime-intranasal protein boost strategy based on nucleoprotein. Virol J 9: 286. doi:10.1186/1743-422X-9-286. PubMed: 23173785.
5. McKinstry KK, Strutt TM, Kuang Y, Brown DM, Sell S, et al. (2012) Memory CD4+ T cells protect against influenza through multiple synergizing mechanisms. J Clin Invest 122: 2847-2856. doi:10.1172/JCI63689. PubMed: 22820287.
6. Teijaro JR, Turner D, Pham Q, Wherry EJ, Lefrançois L, et al. (2011) Cutting edge: Tissue-retentive lung memory CD4 T cells mediate optimal protection to respiratory virus infection. J Immunol 187: 5510-5514. doi:10.4049/jimmunol.1102243. PubMed: 22058417.
7. Wilkinson TM, Li CK, Chui CS, Huang AK, Perkins M, et al. (2012) Preexisting influenza-specific CD4+ T cells correlate with disease protection against influenza challenge in humans. Nat Med 18: 274-280. doi:10.1038/nm.2612. PubMed: 22286307.
8. Wagar LE, Gentleman B, Pircher H, McElhaney JE, Watts TH, (2011) Influenza-specific T cells from older people are enriched in the late effector subset and their presence inversely correlates with vaccine response. PLOS ONE 6: e23698. doi:10.1371/journal.pone.0023698. PubMed: 21887299.
9. Bethell D, Saunders D, Jongkaewwattana A, Kramyu J, Thitithayanont A, et al. (2013) Evaluation of in vitro cross-reactivity to avian H5N1 and pandemic H1N1 2009 influenza following prime boost regimens of seasonal influenza vaccination in healthy human subjects: a randomised trial. PLOS ONE 8: e59674. doi:10.1371/journal.pone.0059674. PubMed: 23555741.
10. Nayak JL, Fitzgerald TF, Richards KA, Yang H, Treanor JJ, et al. (2013) CD4+ T-cell expansion predicts neutralizing antibody responses to monovalent, inactivated 2009 pandemic influenza A(H1N1) virus subtype H1N1 vaccine. J Infect Dis 207: 297-305. doi:10.1093/infdis/jis684. PubMed: 23148285.
11. Bentebibel SE, Lopez S, Obermoser G, Schmitt N, Mueller C, et al. (2013) Induction of ICOS+CXCR3+CXCR5+ TH cells correlates with antibody responses to influenza vaccination. Sci Transl Med 5: 176ra132. PubMed: 23486778.
12. Strutt TM, McKinstry KK, Kuang Y, Bradley LM, Swain SL, (2012) Memory CD4+ T-cell-mediated protection depends on secondary effectors that are distinct from and superior to primary effectors. Proc Natl Acad Sci U S A 109: E2551-E2560. doi:10.1073/pnas.1205894109. PubMed: 22927425.
13. Mahnke YD, Saqr A, Hazenfeld S, Brady RC, Roederer M, et al. (2011) Age-related changes in durability and function of vaccine-elicited influenza-specific CD4(+) T-cell responses. Vaccine 29: 8606-8614. doi:10.1016/j.vaccine.2011.09.019. PubMed: 21939709.
14. McElhaney JE, (2011) Influenza vaccine responses in older adults. Ageing Res Rev 10: 379-388. doi:10.1016/j.arr.2010.10.008. PubMed: 21055484.
15. Koch S, Larbi A, Derhovanessian E, Ozcelik D, Naumova E, et al. (2008) Multiparameter flow cytometric analysis of CD4 and CD8 T cell subsets in young and old people. Immun Ageing 5: 6. doi:10.1186/1742-4933-5-6. PubMed: 18657274.
16. Zhou X, McElhaney JE, (2011) Age-related changes in memory and effector T cells responding to influenza A/H3N2 and pandemic A/H1N1 strains in humans. Vaccine 29: 2169-2177. doi:10.1016/j.vaccine.2010.12.029. PubMed: 21353149.
17. Vezys V, Yates A, Casey KA, Lanier G, Ahmed R, et al. (2009) Memory CD8 T-cell compartment grows in size with immunological experience. Nature 457: 196-199. doi:10.1038/nature07486. PubMed: 19005468.
18. Tsukamoto H, Clise-Dwyer K, Huston GE, Duso DK, Buck AL, et al. (2009) Age-associated increase in lifespan of naive CD4 T cells contributes to T-cell homeostasis but facilitates development of functional defects. Proc Natl Acad Sci USA 106: 18333-18338. doi:10.1073/pnas.0910139106. PubMed: 19815516.
19. Tsukamoto H, Huston GE, Dibble J, Duso DK, Swain SL, (2010) Bim dictates naive CD4 T cell lifespan and the development of age-associated functional defects. J Immunol (Baltimore, Md: 1950) 185: 4535-4544. PubMed: 20844198.
20. McElhaney JE, Xie D, Hager WD, Barry MB, Wang Y, et al. (2006) T cell responses are better correlates of vaccine protection in the elderly. J Immunol (Baltimore, Md: 1950) 176: 6333-6339. PubMed: 16670345.
21. Kang I, Hong MS, Nolasco H, Park SH, Dan JM, et al. (2004) Age-associated change in the frequency of memory CD4+ T cells impairs long term CD4+ T cell responses to influenza vaccine. J Immunol 173: 673-681. PubMed: 15210831.
22. Cai G, Anumanthan A, Brown JA, Greenfield EA, Zhu B, et al. (2008) CD160 inhibits activation of human CD4+ T cells through interaction with herpesvirus entry mediator. Nat Immunol 9: 176-185. doi:10.1038/ni1554. PubMed: 18193050.
23. Dolfi DV, Mansfield KD, Polley AM, Doyle SA, Freeman GJ, et al. (2013) Increased T-bet is associated with senescence of influenza virus-specific CD8 T cells in aged humans. J Leukoc Biol, 93: 825-36. PubMed: 23440501.
24. Weaver JM, Yang H, Roumanes D, Lee FE, Wu H, et al. (2013) Increase in IFNgamma(-)IL-2(+) cells in recent human CD4 T cell responses to 2009 pandemic H1N1 influenza. PLOS ONE 8: e57275. doi:10.1371/journal.pone.0057275. PubMed: 23526940.
25. Lucas M, Day CL, Wyer JR, Cunliffe SL, Loughry A, et al. (2004) Ex vivo phenotype and frequency of influenza virus-specific CD4 memory T cells. J Virol 78: 7284-7287. doi:10.1128/JVI.78.13.7284-7287.2004. PubMed: 15194806.
26. Garcia-Cañas V, Lorbetskie B, Girard M, (2006) Rapid and selective characterization of influenza virus constituents in monovalent and multivalent preparations using non-porous reversed-phase high performance liquid chromatography columns. J Chromatogr A 1123: 225-232. doi:10.1016/j.chroma.2006.04.003. PubMed: 16677659.
27. García-Cañas V, Lorbetskie B, Bertrand D, Cyr TD, Girard M, (2007) Selective and quantitative detection of influenza virus proteins in commercial vaccines using two-dimensional high-performance liquid chromatography and fluorescence detection. Anal Chem 79: 3164-3172. doi:10.1021/ac0621120. PubMed: 17361989.
28. Co MD, Orphin L, Cruz J, Pazoles P, Rothman AL, et al. (2008) Discordance between antibody and T cell responses in recipients of trivalent inactivated influenza vaccine. Vaccine 26: 1990-1998. doi:10.1016/j.vaccine.2008.02.024. PubMed: 18339461.
29. Kang KS, Lee N, Shin MS, Kim SD, Yu Y, et al. (2013) An altered relationship of influenza vaccine-specific IgG responses with T cell immunity occurs with aging in humans. Clin Immunol 147: 79-88. doi:10.1016/j.clim.2013.02.022. PubMed: 23578549.
30. Miller JD, van der Most RG, Akondy RS, Glidewell JT, Albott S, et al. (2008) Human effector and memory CD8+ T cell responses to smallpox and yellow fever vaccines. Immunity 28: 710-722. doi:10.1016/j.immuni.2008.02.020. PubMed: 18468462.
31. Badovinac VP, Messingham KAN, Hamilton SE, Harty JT, (2003) Regulation of CD8+ T cells undergoing primary and secondary responses to infection in the same host. J Immunol (Baltimore, Md: 1950) 170: 4933-4942. PubMed: 12734336.
32. Obar JJ, Khanna KM, Lefrançois L, (2008) Endogenous naive CD8+ T cell precursor frequency regulates primary and memory responses to infection. Immunity 28: 859-869. doi:10.1016/j.immuni.2008.04.010. PubMed: 18499487.
33. Ernst DN, Hobbs MV, Torbett BE, Glasebrook AL, Rehse MA, et al. (1990) Differences in the expression profiles of CD45RB, Pgp-1, and 3G11 membrane antigens and in the patterns of lymphokine secretion by splenic CD4+ T cells from young and aged mice. J Immunol 145: 1295-1302. PubMed: 1974562.
34. Naylor K, Li G, Vallejo AN, Lee WW, Koetz K, et al. (2005) The influence of age on T cell generation and TCR diversity. J Immunol 174: 7446-7452. PubMed: 15905594.
35. Co MD, Orphin L, Cruz J, Pazoles P, Green KM, et al. (2009) In vitro evidence that commercial influenza vaccines are not similar in their ability to activate human T cell responses. Vaccine 27: 319-327. doi:10.1016/j.vaccine.2008.09.092. PubMed: 18977404.
36. Terajima M, Cruz J, Leporati AM, Orphin L, Babon JA, et al. (2008) Influenza A virus matrix protein 1-specific human CD8+ T-cell response induced in trivalent inactivated vaccine recipients. J Virol 82: 9283-9287. doi:10.1128/JVI.01047-08. PubMed: 18614638.
37. Mbawuike I, Zang Y, Couch RB, (2007) Humoral and cell-mediated immune responses of humans to inactivated influenza vaccine with or without QS21 adjuvant. Vaccine 25: 3263-3269. doi:10.1016/j.vaccine.2007.01.073. PubMed: 17280748.
38. Ashraf S, Kong W, Wang S, Yang J, Curtiss R 3rd, (2011) Protective cellular responses elicited by vaccination with influenza nucleoprotein delivered by a live recombinant attenuated Salmonella vaccine. Vaccine 29: 3990-4002. doi:10.1016/j.vaccine.2011.03.066. PubMed: 21466806.
39. Bodewes R, Fraaij PLA, Geelhoed-Mieras MM, van Baalen CA, Hawm Tiddenset al. (2011) Annual vaccination against influenza virus hampers development of virus-specific CD8? T cell immunity in children. Journal of virology 85: 11995-12000.
40. Brown DM, Dilzer AM, Meents DL, Swain SL, (2006) CD4 T cell-mediated protection from lethal influenza: perforin and antibody-mediated mechanisms give a one-two punch. J Immunol (Baltimore, Md: 1950) 177: 2888-2898. PubMed: 16920924.
41. Laidlaw BJ, Decman V, Ali M-AA, Abt MC, Wolf AI, et al. (2013) Cooperativity Between CD8+ T Cells, Non-Neutralizing Antibodies, and Alveolar Macrophages Is Important for Heterosubtypic Influenza Virus Immunity. PLOS Pathog 9: e1003207. PubMed: 23516357.
42. Teijaro JR, Verhoeven D, Page CA, Turner D, Farber DL, (2010) Memory CD4 T cells direct protective responses to influenza virus in the lungs through helper-independent mechanisms. J Virol 84: 9217-9226. doi:10.1128/JVI.01069-10. PubMed: 20592069.