Genome-wide screening of human T-cell epitopes in influenza A virus reveals a broad spectrum of CD4+ T-cell responses to internal proteins, hemagglutinins, and neuraminidases

Human Immunology

Volumn 70, Issue 9, 2009, Pages 711-721

  Babon, Jenny Aurielle B ^a   Cruz, John ^a   Orphin, Laura ^a   Pazoles, Pamela ^a   Co, Mary Dawn T ^a   Ennis, Francis A ^a   Terajima, Masanori ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

CD4+ T cells; Hemagglutinin; Human T cell epitopes; Influenza A virus; T cell epitope screening

Indexed keywords

EPITOPE; GAMMA INTERFERON; INFLUENZA VIRUS HEMAGGLUTININ; INFLUENZA VIRUS HEMAGGLUTININ 1; INFLUENZA VIRUS HEMAGGLUTININ 3; INFLUENZA VIRUS HEMAGGLUTININ 5; MATRIX PROTEIN; NEURAMINIDASE 1; NEURAMINIDASE 2; SYNTHETIC PEPTIDE; UNCLASSIFIED DRUG; VIRUS SIALIDASE;

AMINO ACID SEQUENCE; ARTICLE; AVIAN INFLUENZA; CD4+ T LYMPHOCYTE; CELL SPECIFICITY; CONTROLLED STUDY; CROSS REACTION; CYTOTOXIC T LYMPHOCYTE; ENZYME LINKED IMMUNOSPOT ASSAY; EPITOPE MAPPING; GENETIC SCREENING; GENOME ANALYSIS; HUMAN; HUMAN CELL; IMMUNE RESPONSE; INFLUENZA VIRUS A; INFLUENZA VIRUS A H1N1; INFLUENZA VIRUS A H3N2; INFLUENZA VIRUS A H5N1; LYMPHOCYTE FUNCTION; NONHUMAN; NORMAL HUMAN; PEPTIDE ANALYSIS; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; VIRUS STRAIN;

ADULT; CD4-POSITIVE T-LYMPHOCYTES; CELL LINE; CROSS REACTIONS; CYTOTOXICITY, IMMUNOLOGIC; EPITOPE MAPPING; EPITOPES, T-LYMPHOCYTE; GENOME, VIRAL; GENOME-WIDE ASSOCIATION STUDY; HEMAGGLUTININS; HISTOCOMPATIBILITY TESTING; HUMANS; INFLUENZA A VIRUS, H5N1 SUBTYPE; INTERFERON-GAMMA; NEURAMINIDASE; PEPTIDE FRAGMENTS; VIRAL MATRIX PROTEINS; VIRAL PROTEINS;

EID: 68749106802     PISSN: 01988859     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.humimm.2009.06.004     Document Type: Article

References (41)

1. The Writing Committee of the World Health Organization Consultation on Human Influenza AH. Avian influenza A (H5N1) infection in humans. N Engl J Med 353 (2005) 1374-1385
2. Doherty P.C., Turner S.J., Webby R.G., and Thomas P.G. Influenza and the challenge for immunology. Nat Immunol 7 (2006) 449-455
3. Epstein S. 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 (2006) 49-53
4. McElhaney J.E., Xie D., Hager W.D., Barry M.B., Wang Y., Kleppinger A., et al. T cell responses are better correlates of vaccine protection in the elderly. J Immunol 176 (2006) 6333-6339
5. Gotch F., Rothbard J., Howland K., Townsend A., and McMichael A. Cytotoxic T lymphocytes recognize a fragment of influenza virus matrix protein in association with HLA-A2. Nature 326 (1987) 881-882
6. Yewdell J.W., Bennink J.R., Smith G.L., and Moss B. Influenza A virus nucleoprotein is a major target for cross-reactive anti-influenza A virus cytotoxic T lymphocytes. Proc Natl Acad Sci 82 (1985) 1785-1789
7. Lamb J.R., and Green N. Analysis of the antigen specificity of influenza haemagglutinin-immune human T lymphocyte clones: identification of an immunodominant region for T cells. Immunology 50 (1983) 659-666
8. Jameson J., Cruz J., and Ennis F.A. Human cytotoxic T-lymphocyte repertoire to influenza A viruses. J Virol 72 (1998) 8682-8689
9. Jameson J., Cruz J., Terajima M., and Ennis F.A. Human CD8+ and CD4+ T lymphocyte memory to influenza A viruses of swine and avian species. J Immunol 162 (1999) 7578-7583
10. Boon A.C.M., de Mutsert G., Graus Y.M.F., Fouchier R.A.M., Sintnicolaas K., Osterhaus A.D.M.E., et al. The Magnitude and specificity of influenza A virus-specific cytotoxic T-lymphocyte responses in humans is related to HLA-A and -B phenotype. J Virol 76 (2002) 582-590
11. Gianfrani C., Oseroff C., Sidney J., Chesnut R.W., and Sette A. Human memory CTL response specific for influenza A virus is broad and multispecific. Hum Immunol 61 (2000) 438-452
12. Wang M., Lamberth K., Harndahl M., Roder G., Stryhn A., Larsen M.V., et al. CTL epitopes for influenza A including the H5N1 bird flu; genome-, pathogen-, and HLA-wide screening. Vaccine 25 (2007) 2823-2831
13. Assarsson E., Bui H.-H., Sidney J., Zhang Q., Glenn J., Oseroff C., et al. Immunomic analysis of the repertoire of T-cell specificities for influenza A virus in humans. J Virol 82 (2008) 12241-12251
14. Currier J.R., Kuta E.G., Turk E., Earhart L.B., Loomis-Price L., Janetzki S., et al. A panel of MHC class I restricted viral peptides for use as a quality control for vaccine trial ELISPOT assays. J Immunol Methods 260 (2002) 157-172
15. Boyam A. Isolation of mononuclear cells and granulocytes from human blood. Scand J Clin Lab Invest 21 (1968) 77
16. Co M.D.T., Orphin L., Cruz J., Pazoles P., Rothman A.L., Ennis F.A., et al. Discordance between antibody and T cell responses in recipients of trivalent inactivated influenza vaccine. Vaccine 26 (2008) 1990-1998
17. Green S., Kurane I., Edelman R., Tacket C.O., Eckels K.H., Vaughn D.W., et al. Dengue virus-specific human CD4+ T-lymphocyte responses in a recipient of an experimental live-attenuated dengue virus type 1 vaccine: bulk culture proliferation, clonal analysis, and precursor frequency determination. J Virol 67 (1993) 5962-5967
18. Anthony D.D., and Lehmann P.V. T-cell epitope mapping using the ELISPOT approach. Methods 29 (2003) 260-269
19. Oseroff C., Kos F., Bui H.-H., Peters B., Pasquetto V., Glenn J., et al. HLA class I-restricted responses to vaccinia recognize a broad array of proteins mainly involved in virulence and viral gene regulation. Proc Natl Acad Sci USA 102 (2005) 13980-13985
20. McMichael A.J., Gotch F.M., Santos-Aguado J., and Strominger J.L. Effect of mutations and variations of HLA-A2 on recognition of a virus peptide epitope by cytotoxic T lymphocytes. Proc Natl Acad Sci USA 85 (1988) 9194-9198
21. Bui H.-H., Peters B., Assarsson E., Mbawuike I., and Sette A. Ab and T cell epitopes of influenza A virus, knowledge and opportunities. Proc Natl Acad Sci 104 (2007) 246-251
22. Peters B., Sidney J., Bourne P., Bui H.-H., Buus S., Doh G., et al. The Immune Epitope Database and Analysis Resource: From vision to blueprint. PLoS Biol 3 (2005) e91
23. Parker K.C., Bednarek M.A., and Coligan J.E. Scheme for ranking potential HLA-A2 binding peptides based on independent binding of individual peptide side-chains. J Immunol 152 (1994) 163-175
24. Rammensee H.G., Bachmann J., Emmerich N.P.N., Bachor O.A., and Stevanović S. SYFPEITHI: database for MHC ligands and peptide motifs. Immunogenetics 50 (1999) 213-219
25. Terajima M., Cruz J., Leporati A.M., Orphin L., Babon J.A.B., Co M.D.T., et al. Influenza A Virus matrix protein 1-specific human CD8+ T-cell response induced in trivalent inactivated vaccine recipients. J Virol 82 (2008) 9283-9287
26. He X.-S., Holmes T.H., Zhang C., Mahmood K., Kemble G.W., Lewis D.B., et al. Cellular immune responses in children and adults receiving inactivated or live attenuated influenza vaccines. J Virol 80 (2006) 11756-11766
27. Roti M., Yang J., Berger D., Huston L., James E.A., and Kwok W.W. Healthy human subjects have CD4+ T cells directed against H5N1 influenza virus. J Immunol 180 (2008) 1758-1768
28. Lee L.Y., Ha do L.A., Simmons C., de Jong M.D., Chau N.V., Schumacher R., et al. Memory T cells established by seasonal human influenza A infection cross-react with avian influenza A (H5N1) in healthy individuals. J Clin Invest 118 (2008) 3478-3490
29. Kreijtz J.H.C.M., de Mutsert G., van Baalen C.A., Fouchier R.A.M., Osterhaus A.D.M.E., and Rimmelzwaan G.F. Cross-recognition of avian H5N1 influenza virus by human cytotoxic T-lymphocyte populations directed to human influenza A virus. J Virol 82 (2008) 5161-5166
30. Gioia C., Castilletti C., Tempestilli M., Piacentini P., Bordi L., Chiappini R., et al. Cross-subtype immunity against avian influenza in persons recently vaccinated for influenza. Emerg Infect Dis 14 (2008) 121-128 Jan
31. Landry S.J. Three-dimensional structure determines the pattern of CD4+ T-cell epitope dominance in influenza virus hemagglutinin. J Virol 82 (2008) 1238-1248
32. Richards K.A., Chaves F.A., Krafcik F.R., Topham D.J., Lazarski C.A., and Sant A.J. Direct ex vivo analyses of HLA-DR1 transgenic mice reveal an exceptionally broad pattern of immunodominance in the primary HLA-DR1-restricted CD4 T-cell response to influenza virus hemagglutinin. J Virol 81 (2007) 7608-7619
33. Brown D.M., Roman E., and Swain S.L. CD4 T cell responses to influenza infection. Semin Immunol 16 (2004) 171-177
34. Swain S.L., Agrewala J.N., Brown D.M., Jelley-Gibbs D.M., Golech S., Huston G., et al. CD4+ T-cell memory: generation and multi-faceted roles for CD4+ T cells in protective immunity to influenza. Immunol Rev 211 (2006) 8-22
35. Gelder C., Davenport M., Barnardo M., Bourne T., Lamb J., Askonas B., et al. Six unrelated HLA-DR-matched adults recognize identical CD4+ T cell epitopes from influenza A haemagglutinin that are not simply peptides with high HLA-DR binding affinities. Int Immunol 10 (1998) 211-222
36. Gelder C.M., Lamb J.R., and Askonas B.A. Human CD4+ T-cell recognition of influenza A virus hemagglutinin after subunit vaccination. J Virol 70 (1996) 4787-4790
37. Gelder C.M., Welsh K.I., Faith A., Lamb J.R., and Askonas B.A. Human CD4+ T-cell repertoire of responses to influenza A virus hemagglutinin after recent natural infection. J Virol 69 (1995) 7497-7506
38. Yang J., James E.A., Huston L., Danke N.A., Liu A.W., and Kwok W.W. Multiplex mapping of CD4 T cell epitopes using class II tetramers. Clin Immunol 120 (2006) 21-32
39. Scherle P.A., and Gerhard W. Differential ability of B cells specific for external vs. internal influenza virus proteins to respond to help from influenza virus-specific T-cell clones in vivo. Proc Natl Acad Sci USA 85 (1988) 4446-4450
40. Brown D.M., Dilzer A.M., Meents D.L., and Swain S.L. CD4 T cell-mediated protection from lethal influenza: perforin and antibody-mediated mechanisms give a one-two punch. J Immunol 177 (2006) 2888-2898
41. Chapman T.J., Castrucci M.R., Padrick R.C., Bradley L.M., and Topham D.J. Antigen-specific and non-specific CD4+ T cell recruitment and proliferation during influenza infection. Virology 340 (2005) 296-306