A human CD4+ T cell epitope in the influenza hemagglutinin is cross-reactive to influenza A virus subtypes and to influenza B virus

Journal of Virology

Volumn 86, Issue 17, 2012, Pages 9233-9243

  Babon, Jenny Aurielle B ^a   Cruz, John ^a   Ennis, Francis A ^a   Yin, Liusong ^a   Terajima, Masanori ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; GAMMA INTERFERON; HLA DRB1 ANTIGEN; INFLUENZA VIRUS HEMAGGLUTININ;

ADULT; ALLELE; ARTICLE; CD4+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; CROSS REACTION; CYTOLYSIS; ENZYME LINKED IMMUNOSPOT ASSAY; EPITOPE MAPPING; EX VIVO STUDY; GENETIC CONSERVATION; GENETIC REASSORTMENT; HUMAN; HUMAN CELL; IN VITRO STUDY; INFLUENZA VIRUS A; INFLUENZA VIRUS A H1N1; INFLUENZA VIRUS A H2N2; INFLUENZA VIRUS A H3N2; INFLUENZA VIRUS A H5N1; INFLUENZA VIRUS B; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL;

ANTIBODIES, VIRAL; CD4-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; CROSS REACTIONS; EPITOPES, T-LYMPHOCYTE; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; INFLUENZA A VIRUS; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA A VIRUS, H2N2 SUBTYPE; INFLUENZA A VIRUS, H3N2 SUBTYPE; INFLUENZA B VIRUS; INFLUENZA, HUMAN; LEUKOCYTES, MONONUCLEAR;

AVES; CERCOPITHECINE HERPESVIRUS 1; INFLUENZA A VIRUS; INFLUENZA B VIRUS; ORTHOMYXOVIRIDAE;

EID: 84866184589     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.06325-11     Document Type: Article

References (86)

1. Alam S, Sant AJ. 2011. Infection with seasonal influenza virus elicits CD4 T cells specific for genetically conserved epitopes that can be rapidly mobilized for protective immunity to pandemic H1N1 influenza virus. J. Virol. 85:13310-13321.
2. Andersson G. 1998. Evolution of the human HLA-DR region. Front. Biosci. 3:d739-d745.
3. Atassi MZ, Webster RG. 1983. Localization, synthesis, and activity of an antigenic site on influenza virus hemagglutinin. Proc. Natl. Acad. Sci. U. S. A. 80:840-844.
4. +T-cell responses to internal proteins, hemagglutinins, and neuraminidases. Hum. Immunol. 70:711-721.
5. Bell JI, et al. 1987. Allelic variation in the DR subregion of the human major histocompatibility complex. Proc. Natl. Acad. Sci. U. S. A. 84:6234-6238.
6. +-T-cell-deficient mice. J. Virol. 76:12388-12393.
7. Bianchi E, et al. 2005. Universal influenza B vaccine based on the maturational cleavage site of the hemagglutinin precursor. J. Virol. 79:7380-7388.
8. Brown DM, Dilzer AM, Meents DL, Swain SL. 2006. CD4 T cellmediated protection from lethal influenza: perforin and antibody-mediated mechanisms give a one-two punch. J. Immunol. 177:2888-2898.
9. Brown DM, Roman E, Swain SL. 2004. CD4 T cell responses to influenza infection. Semin. Immunol. 16:171-177.
10. Bui HH, Peters B, Assarsson E, Mbawuike I, Sette A. 2007. Ab and T cell epitopes of influenza A virus, knowledge and opportunities. Proc. Natl. Acad. Sci. U. S. A. 104:246-251.
11. + T cells by HLA-DR1 oligomers is dependent on the T cell activation state. J. Immunol. 166:741-745.
12. Chun S, et al. 2008. Universal antibodies and their applications to the quantitative determination of virtually all subtypes of the influenza A viral hemagglutinins. Vaccine 26:6068-6076.
13. Corti D, et al. 2010. Heterosubtypic neutralizing antibodies are produced by individuals immunized with a seasonal influenza vaccine. J. Clin. Invest. 120:1663-1673.
14. Corti D, et al. 2011. A neutralizing antibody selected from plasma cells that binds to group 1 and group 2 influenza A hemagglutinins. Science 333:850-856.
15. Cross KJ, Langley WA, Russell RJ, Skehel JJ, Steinhauer DA. 2009. Composition and functions of the influenza fusion peptide. Protein Pept. Lett. 16:766-778.
16. Cusick MF, Wang S, Eckels DD. 2009. In vitro responses to avian influenza H5 by human CD4 T cells. J. Immunol. 183:6432-6441.
17. Danke NA, Kwok WW. 2003. HLA class II-restricted CD4+ T cell responses directed against influenza viral antigens postinfluenza vaccination. J. Immunol. 171:3163-3169.
18. De Groot AS, Ardito M, McClaine EM, Moise L, Martin WD. 2009. Immunoinformatic comparison of T-cell epitopes contained in novel swine-origin influenza A (H1N1) virus with epitopes in 2008-2009 conventional influenza vaccine. Vaccine 27:5740-5747.
19. Doytchinova IA, Flower DR. 2005. In silico identification of supertypes for class II MHCs. J. Immunol. 174:7085-7095.
20. Duvvuri VR, et al. 2010. Highly conserved cross-reactive CD4+ T-cell HA-epitopes of seasonal and the 2009 pandemic influenza viruses. Influenza Other Respi. Viruses 4:249-258.
21. Ekiert DC, et al. 2009. Antibody recognition of a highly conserved influenza virus epitope. Science 324:246-251.
22. Ennis FA, et al. 1997. Hantavirus pulmonary syndrome: CD8+ and CD4+ cytotoxic T lymphocytes to epitopes on sin nombre virus nucleocapsid protein isolated during acute illness. Virology 238:380-390.
23. Epstein S. 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.
24. Federal Register. 2009. Notice of changes to the NIH guidelines. Fed. Regist. 74:48275-48280. http://oba.od.nih.gov/oba/rac/fractions/74_FR_48275.pdf
25. Fiore AE, et al. 2009. Prevention and control of seasonal influenza with vaccines: recommendations of the Advisory Committee on Immunization Practices (ACIP), 2009. MMWR Recommend Rep. 58:1-52.
26. Fouchier RAM, et al. 2005. Characterization of a novel influenza A virus hemagglutinin subtype (H16) obtained from black-headed gulls. J. Virol. 79:2814-2822.
27. Frayser M, Sato AK, Xu L, Stern LJ. 1999. Empty and peptide-loaded class II major histocompatibility complex proteins produced by expression in Escherichia coli and folding in vitro. Protein Expr. Purif. 15:105-114.
28. Gagnon SJ, Ennis FA, Rothman AL. 1999. Bystander target cell lysis and cytokine production by dengue virus-specific human CD4+ cytotoxic T-lymphocyte clones. J. Virol. 73:3623-3629.
29. Ge X, et al. 2010. Assessment of seasonal influenza A virus-specific CD4 T-cell responses to 2009 pandemic H1N1 swine-origin influenza A virus. J. Virol. 84:3312-3319.
30. Gelder C, et al. 1998. 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. 10:211-222.
31. Gelder CM, Welsh KI, Faith A, Lamb JR, Askonas BA. 1995. Human CD4+ T-cell repertoire of responses to influenza A virus hemagglutinin after recent natural infection. J. Virol. 69:7497-7506.
32. Gerhard W. 2001. The role of the antibody response in influenza virus infection. Curr. Top. Microbiol. Immunol. 260:171-190.
33. Gianfrani C, Oseroff C, Sidney J, Chesnut RW, Sette A. 2000. Human memory CTL response specific for influenza A virus is broad and multispecific. Hum. Immunol. 61:438-452.
34. Grebe KM, Yewdell JW, Bennink JR. 2008. Heterosubtypic immunity to influenza A virus: where do we stand? Microbes Infect. 10:1024-1029.
35. Green S, et al. 1993. 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. 67:5962-5967.
36. Green S, Kurane I, Pincus S, Paoletti E, Ennis FA. 1997. Recognition of dengue virus NS1-NS2a proteins by human CD4+ cytotoxic T lymphocyte clones. Virology 234:383-386.
37. Greenbaum J, et al. 2011. Functional classification of class II human leukocyte antigen (HLA) molecules reveals seven different supertypes and a surprising degree of repertoire sharing across supertypes. Immunogenetics 63:325-335.
38. Gregersen PK, et al. 1986. Polymorphism of HLA-DR beta chains in DR4,-7, and -9 haplotypes: implications for the mechanisms of allelic variation. Proc. Natl. Acad. Sci. U. S. A. 83:9149-9153.
39. Hancock K, et al. 2009. Cross-reactive antibody responses to the 2009 pandemic H1N1 influenza virus. N. Engl. J. Med. 361:1945-1952.
40. Heiny AT, et al. 2007. Evolutionarily conserved protein sequences of influenza A viruses, avian and human, as vaccine targets. PLoS One 2:e1190. doi:10.1371/journal.pone.0001190.
41. Jameson J, Cruz J, Ennis FA. 1998. Human cytotoxic T-lymphocyte repertoire to influenza A viruses. J. Virol. 72:8682-8689.
42. Jameson J, Cruz J, Terajima M, Ennis FA. 1999. Human CD8+ and CD4+ T lymphocyte memory to influenza A viruses of swine and avian species. J. Immunol. 162:7578-7583.
43. Jonges M, et al. 2010. Influenza virus inactivation for studies of antige-nicity and phenotypic neuraminidase inhibitor resistance profiling. J. Clin. Microbiol. 48:928-940.
44. Kashyap AK, et al. 2008. Combinatorial antibody libraries from survivors of the Turkish H5N1 avian influenza outbreak reveal virus neutralization strategies. Proc. Natl. Acad. Sci. U. S. A. 105:5986-5991.
45. Kobayashi H, et al. 1996. Analysis of anchor residues in a naturally processed HLA-DR53 ligand. Immunogenetics 44:366-371.
46. Lamb JR, Eckels DD, Lake P, Woody JN, Green N. 1982. Human T-cell clones recognize chemically synthesized peptides of influenza haemagglutinin. Nature 300:66-69.
47. Lamb JR, Green N. 1983. Analysis of the antigen specificity of influenza haemagglutinin-immune human T lymphocyte clones: identification of an immunodominant region for T cells. Immunology 50:659-666.
48. Lee LY, et al. 2008. Memory T cells established by seasonal human influenza A infection cross-react with avian influenza A (H5N1) in healthy individuals. J. Clin. Invest. 118:3478-3490.
49. Lucas M, et al. 2004. Ex Vivo phenotype and frequency of influenza virus-specific CD4 memory T cells. J. Virol. 78:7284-7287.
50. McKinstry KK, Strutt TM, Swain SL. 2011. Hallmarks of CD4 T cell immunity against influenza. J. Intern. Med. 269:507-518.
51. Mitra-Kaushik S, Cruz J, Stern LJ, Ennis FA, Terajima M. 2007. Human cytotoxic CD4+ T cells recognize HLA-DR1-restricted epitopes on vaccinia virus proteins A24R and D1R conserved among poxviruses. J. Immunol. 179:1303-1312.
52. Palese P, Shaw ML. 2007. Orthomyxoviridae: the viruses and their replication, p 1648-1689. In Knipe DM, et al (ed), Fields virology. Lippincott Williams & Wilkins, Philadelphia, PA.
53. Pan QQ, et al. 2011. The distribution of human leukocyte antigen-A,-B, and -DRB1 alleles and haplotypes based on high-resolution genotyping of 167 families from Jiangsu Province, China. Hum. Immunol. 72:672-676.
54. Peters B, et al. 2005. The immune epitope database and analysis resource: from vision to blueprint. PLoS Biol. 3:e91. doi:10.1371/journal.p-bio. 0030091.
55. Prevost-Blondel A, et al. 1995. Preferential usage of the T-cell receptor by influenza virus hemagglutinin-specific human CD4+ T lymphocytes: in vitro life span of clonotypic T cells. J. Virol. 69:8046-8050.
56. Qin Qin P, et al. 2011. Distribution of human leucocyte antigen-A, -B and -DR alleles and haplotypes at high resolution in the population from Jiangsu province of China. Int. J. Immunogenet. 38:475-481.
57. Rajnavolgyi E, et al. 1997. Characterizing immunodominant and protective influenza hemagglutinin epitopes by functional activity and relative binding to major histocompatibility complex class II sites. Eur. J. Immunol. 27:3105-3114.
58. Richards KA, et al. 2007. 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. 81:7608-7619.
59. Richards KA, Chaves FA, Sant AJ. 2011. The memory phase of the CD4 T-cell response to influenza virus infection maintains its diverse antigen specificity. Immunology 133:246-256.
60. Richards KA, Topham D, Chaves FA, Sant AJ. 2010. Cutting edge: CD4 T cells generated from encounter with seasonal influenza viruses and vaccines have broad protein specificity and can. directly recognize naturally generated epitopes derived from the live pandemic H1N1 virus. J. Immunol. 185:4998-5002.
61. Robbins PA, Garboczi DN, Strominger JL. 1995. HLA-A*0201 complexes with two 10-mer peptides differing at the P2 anchor residue have distinct refolding kinetics. J. Immunol. 154:703-709.
62. Robbins PA, et al. 1989. Comparison between two peptide epitopes presented to cytotoxic T lymphocytes by HLA-A2. Evidence for discrete locations within HLA-A2. J. Immunol. 143:4098-4103.
63. Robbins PA, Rota PA, Shapiro SZ. 1997. A broad cytotoxic T lymphocyte response to influenza type B virus presented by multiple HLA molecules. Int. Immunol. 9:815-823.
64. Romphruk AV, et al. 2010. HLA class I and II alleles and haplotypes in ethnic Northeast Thais. Tissue Antigens 75:701-711.
65. Roti M, et al. 2008. Healthy human subjects have CD4+ T cells directed against H5N1 influenza virus. J. Immunol. 180:1758-1768.
66. Ruigrok RW. 1998. Structure of influenza A, B and C viruses, p 29-42. In Nicholson K, Webster RG, Hay AJ (ed), Textbook of influenza. Blackwell Science Ltd, Oxford, United Kingdom.
67. Scriba TJ, et al. 2005. Ultrasensitive detection and phenotyping of CD4+T cells with optimized HLA class II tetramer staining. J. Immunol. 175:6334-6343.
68. Silver ML, Parker KC, Wiley DC. 1991. Reconstitution by MHC-restricted peptides of HLA-A2 heavy chain with [beta]2-microglobulin, in vitro. Nature 350:619-622.
69. Skehel JJ, Wiley DC. 2000. Receptor binding and membrane fusion in virus entry: the influenza hemagglutinin. Annu. Rev. Biochem. 69:531-569.
70. Slepushkin AN. 1959. The effect of a previous attack of A1 influenza on susceptibility to A2 virus during the 1957 outbreak. Bull. World Health Organ. 20:297-301.
71. Southwood S, et al. 1998. Several common HLA-DR types share largely overlapping peptide binding repertoires. J. Immunol. 160:3363-3373.
72. Stanekova Z, et al. 2012. Epitope specificity of anti-HA2 antibodies induced in humans during influenza infection. Influenza Other Respi. Viruses doi:10.1111/j.1750-2659.2011.00328.x.
73. Steel J, et al. 2010. Influenza virus vaccine based on the conserved hemagglutinin stalk domain. mBio 1:e00018-00010. doi:10.1128/mBio.00018-10.
74. Strutt TM, et al. 2010. Memory CD4+ T cells induce innate responses independently of pathogen. Nat. Med. 16:558-564.
75. Sui J, et al. 2009. Structural and functional bases for broad-spectrum neutralization of avian and human influenza A viruses. Nat. Struct. Mol. Biol. 16:265-273.
76. Swain SL, et al. 2006. CD4+ T-cell memory: generation and multifaceted roles for CD4+ T cells in protective immunity to influenza. Immunol. Rev. 211:8-22.
77. Swain SL, Dutton RW, Woodland DL. 2004. T cell responses to influenza virus infection: effector and memory cells. Viral Immunol. 17:197-209.
78. 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.
79. Throsby M, et al. 2008. Heterosubtypic neutralizing monoclonal antibodies cross-protective against H5N1 and H1N1 recovered from human IgM+ memory B cells. PLoS One 3:e3942. doi:10.1371/journal.pone.0003942.
80. Wang P, et al. 2008. A systematic assessment of MHC class II peptide binding predictions and evaluation of a consensus approach. PLoS Comput. Biol. 4:e1000048. doi:10.1371/journal.pcbi.1000048.
81. Wilkinson TM, et al. 2012. Preexisting influenza-specific CD4+ T cells correlate with disease protection against influenza challenge in humans. Nat. Med. 18:274-280.
82. Wrammert J, et al. 2011. Broadly cross-reactive antibodies dominate the human B cell response against 2009 pandemic H1N1 influenza virus infection. J. Exp. Med. 208:181-193.
83. Xing Z, Cardona CJ. 2009. Preexisting immunity to pandemic (H1N1). Emerg. Infect. Dis. 15:1847-1849. (Letter.)
84. Yang J, et al. 2009. H5N1 strain-specific Hemagglutinin CD4+ T cell epitopes restricted by HLA DR4. Vaccine 27:3862-3869.
85. Zeliszewski D, et al. 1994. Molecular basis for degenerate T-cell recognition of one peptide in the context of several DR molecules. Hum. Immunol. 41:28-33.
86. Zhu F, et al. 2011. Analysis of the complete cDNA sequences of HLADRB1 alleles with group-specific amplification primers in the Chinese Han population. Tissue Antigens 77:329-332.