Cross-allele cytotoxic T lymphocyte responses against 2009 pandemic H1N1 influenza a virus among HLA-A24 and HLA-A3 supertype-positive individuals

Journal of Virology

Volumn 86, Issue 24, 2012, Pages 13281-13294

  Liu, Jun ^a   Zhang, Shihong ^a,b   Tan, Shuguang ^a,b   Yi, Yong ^c   Wu, Bin ^d   Cao, Bin ^e   Zhu, Fengcai ^d   Wang, Chen ^e   Wang, Hua ^d   Qi, Jianxun ^a   Gao, George F ^a,b,f  

^a INSTITUTE OF MICROBIOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c 306 HOSPITAL OF PLA   (China)

^d JIANGSU PROVINCIAL CENTER FOR DISEASE CONTROL AND PREVENTION   (China)

^e CAPITAL MEDICAL UNIVERSITY   (China)

^f INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; HLA A11 ANTIGEN; HLA A24 ANTIGEN; HLA A3 ANTIGEN; HLA A30 ANTIGEN; HLA A31 ANTIGEN; HLA A33 ANTIGEN; UNCLASSIFIED DRUG;

2009 H1N1 INFLUENZA; ADULT; AGED; ALLELE; ANTIGEN RECOGNITION; ANTIGEN SPECIFICITY; ARTICLE; BINDING AFFINITY; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; CRYSTAL STRUCTURE; EPITOPE MAPPING; FEMALE; FLOW CYTOMETRY; HETEROZYGOSITY; HOMOZYGOSITY; HUMAN; INFLUENZA VIRUS A H1N1; MAJOR CLINICAL STUDY; MALE; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN FOLDING; PROTEIN MOTIF; T LYMPHOCYTE; X RAY CRYSTALLOGRAPHY;

ADULT; AGED; ALLELES; AMINO ACID SEQUENCE; COHORT STUDIES; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; HLA-A24 ANTIGEN; HLA-A3 ANTIGEN; HUMANS; INFLUENZA A VIRUS, H1N1 SUBTYPE; MALE; MIDDLE AGED; MODELS, MOLECULAR; T-LYMPHOCYTES, CYTOTOXIC;

INFLUENZA A VIRUS; ORTHOMYXOVIRIDAE;

EID: 84870696513     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01841-12     Document Type: Article

References (89)

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. Alexander J, et al. 2010. Identification of broad binding class I HLA supertype epitopes to provide universal coverage of influenza A virus. Hum. Immunol. 71:468-474.
3. Assarsson E, et al. 2008. Immunomic analysis of the repertoire of T-cell specificities for influenza A virus in humans. J. Virol. 82:12241-12251.
4. Bednarek MA, et al. 1991. The minimum peptide epitope from the influenza virus matrix protein. Extra and intracellular loading of HLA-A2. J. Immunol. 147:4047-4053.
5. Berthoud TK, 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.
6. Boon AC, et al. 2004. Preferential HLA usage in the influenza virusspecific CTL response. J. Immunol. 172:4435-4443.
7. Boon AC, et al. 2002. 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. 76:582-590.
8. Bouvier M, Wiley DC. 1994. Importance of peptide amino and carboxyl termini to the stability of MHC class I molecules. Science 265:398-402.
9. Brooks JM, Colbert RA, Mear JP, Leese AM, Rickinson AB. 1998. HLA-B27 subtype polymorphism and CTL epitope choice: studies with EBV peptides link immunogenicity with stability of the B27:peptide complex. J. Immunol. 161:5252-5259.
10. Brunger AT, et al. 1998. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 54:905-921.
11. 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.
12. Burrows SR, et al. 2003. Promiscuous CTL recognition of viral epitopes on multiple human leukocyte antigens: biological validation of the proposed HLA A24 supertype. J. Immunol. 171:1407-1412.
13. Cao B, et al. 2009. Clinical features of the initial cases of 2009 pandemic influenza A (H1N1) virus infection in China. N. Engl. J. Med. 361:2507-2517.
14. 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.
15. Cheuk E, et al. 2002. Human MHC class I transgenic mice deficient for H2 class I expression facilitate identification and characterization of new HLA class I-restricted viral T cell epitopes. J. Immunol. 169:5571-5580.
16. 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.
17. Emsley P, Lohkamp B, Scott WG, Cowtan K. 2004. Features and development of coot. Acta Crystallogr. D Biol. Crystallogr. 66:486-501.
18. Epstein SL, et al. 2005. Protection against multiple influenza A subtypes by vaccination with highly conserved nucleoprotein. Vaccine 23:5404-5410.
19. Fisman DN, et al. 2009. Older age and a reduced likelihood of 2009 H1N1 virus infection. N. Engl. J. Med. 361:2000-2001.
20. Frahm N, et al. 2007. Extensive HLA class I allele promiscuity among viral CTL epitopes. Eur. J. Immunol. 37:2419-2433.
21. Gallimore A, et al. 1998. A protective cytotoxic T cell response to a subdominant epitope is influenced by the stability of theMHCclass I/peptide complex and the overall spectrum of viral peptides generated within infected cells. Eur. J. Immunol. 28:3301-3311.
22. Gao GF, Sun Y. 2010. It is not just AIV: from avian to swine-origin influenza virus. Sci. China Life Sci. 53:151-153.
23. Garten RJ, et al. 2009. Antigenic and genetic characteristics of swineorigin 2009 A(H1N1) influenza viruses circulating in humans. Science 325:197-201.
24. 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.
25. Gras S, et al. 2010. Cross-reactive CD8+ T-cell immunity between the pandemic H1N1-2009 and H1N1-1918 influenza A viruses. Proc. Natl. Acad. Sci. U. S. A. 107:12599-12604.
26. Guan Y, et al. 2010. The emergence of pandemic influenza viruses. Protein Cell 1:9-13.
27. Guan Z, et al. 2010. Interaction of Hsp40 with influenza virus M2 protein:implications for PKR signaling pathway. Protein Cell 1:944-955.
28. Guo H, Santiago F, Lambert K, Takimoto T, Topham DJ. 2011. T cell-mediated protection against lethal 2009 pandemic H1N1 influenza virus infection in a mouse model. J. Virol. 85:448-455.
29. Guo HC, et al. 1992. Different length peptides bind to HLA-Aw68 similarly at their ends but bulge out in the middle. Nature 360:364-366.
30. 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.
31. Hildebrand WH, et al. 2002. HLA class I polymorphism has a dual impact on ligand binding and chaperone interaction. Hum. Immunol. 63:248-255.
32. Hillaire ML, et al. 2011. Characterization of the human CD8 T cell response following infection with 2009 pandemic influenza H1N1 virus. J. Virol. 85:12057-12061.
33. Hillaire ML, et al. 2011. Cross-protective immunity against influenza pH1N1 2009 viruses induced by seasonal influenza A (H3N2) virus is mediated by virus-specific T-cells. J. Gen. Virol. 92:2339-2349.
34. Hong W, et al. 2007. HLA class I polymorphism in Mongolian and Hui ethnic groups from Northern China. Hum. Immunol. 68:439-448.
35. Ichihashi T, Yoshida R, Sugimoto C, Takada A, Kajino K. 2011. Crossprotective peptide vaccine against influenza A viruses developed in HLAA*2402 human immunity model. PLoS One 6:e24626. doi:10.1371/journal.pone.0024626.
36. Ikeda-Moore Y, et al. 1997. Identification and characterization of multiple HLA-A24-restricted HIV-1 CTL epitopes: strong epitopes are derived from V regions of HIV-1. J. Immunol. 159:6242-6252.
37. Iorio AM, et al. 2012. Influenza viruses and cross-reactivity in healthy adults: humoral and cellular immunity induced by seasonal 2007/2008 influenza vaccination against vaccine antigens and 2009 A(H1N1) pandemic influenza virus. Vaccine 30:1617-1623.
38. Lamberth K, et al. 2008. The peptide-binding specificity of HLA-A*3001 demonstrates membership of the HLA-A3 supertype. Immunogenetics 60:633-643.
39. Laskowski RA, Macarthur MW, Moss DS, and Thornton JM. 1993. Procheck - a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26:283-291.
40. 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.
41. Levitsky V, Zhang QJ, Levitskaya J, Masucci MG. 1996. The life span of major histocompatibility complex-peptide complexes influences the efficiency of presentation and immunogenicity of two class I-restricted cytotoxic T lymphocyte epitopes in the Epstein-Barr virus nuclear antigen 4. J. Exp. Med. 183:915-926.
42. Lewis DB. 2006. Avian flu to human influenza. Annu. Rev. Med. 57:139-154.
43. Li L, Bouvier M. 2004. Structures of HLA-A*1101 complexed with immunodominant nonamer and decamer HIV-1 epitopes clearly reveal the presence of a middle, secondary anchor residue. J. Immunol. 172:6175-6184.
44. Li X, et al. 2011. Two distinct conformations of a rinderpest virus epitope presented by bovine major histocompatibility complex class I N*01801: a host strategy to present featured peptides. J. Virol. 85:6038-6048.
45. Lichterfeld M, et al. 2006. T cell receptor cross-recognition of an HIV-1 CD8+ T cell epitope presented by closely related alleles from the HLA-A3 superfamily. Int. Immunol. 18:1179-1188.
46. Lillie PJ, et al. 2012. Preliminary assessment of the efficacy of a T-cellbased influenza vaccine, MVA-NP+M1, in humans. Clin. Infect. Dis. 55:19-25.
47. Liu J, et al. 2011. Diverse peptide presentation of rhesus macaque major histocompatibility complex class I mamu-a*02 revealed by two peptide complex structures and insights into immune escape of simian immunodeficiency virus. J. Virol. 85:7372-7383.
48. Liu J, et al. 2012. Crystal structure of cell adhesion molecule nectin-2/CD112 and Its binding to immune receptor DNAM-1/CD226. J. Immunol. 188:5511-5520.
49. Liu J, et al. 2010. The membrane protein of severe acute respiratory syndrome coronavirus acts as a dominant immunogen revealed by a clustering region of novel functionally and structurally defined cytotoxic Tlymphocyte epitopes. J. Infect. Dis. 202:1171-1180.
50. Liu J, et al. 2010. Novel immunodominant peptide presentation strategy:a featured HLA-A*2402-restricted cytotoxic T-lymphocyte epitope stabilized by intrachain hydrogen bonds from severe acute respiratory syndrome coronavirus nucleocapsid protein. J. Virol. 84:11849-11857.
51. Liu J, Zhang S, Tan S, Zheng B, Gao GF. 2011. Revival of the identification of cytotoxic T-lymphocyte epitopes for immunological diagnosis, therapy and vaccine development. Exp. Biol. Med. (Maywood) 236:253-267.
52. Lund O, et al. 2004. Definition of supertypes for HLA molecules using clustering of specificity matrices. Immunogenetics 55:797-810.
53. McMichael AJ, Gotch FM, Noble GR, Beare PA. 1983. Cytotoxic T-cell immunity to influenza. N. Engl. J. Med. 309:13-17.
54. Middleton D, Menchaca L, Rood H, Komerofsky R. 2003. New allele frequency database: http://www.allelefrequencies.net. Tissue Antigens 61:403-407.
55. Mohamed ER, et al. 2009. Capability of SART3(109-118) peptide to induce cytotoxic T lymphocytes from prostate cancer patients with HLA class I-A11, -A31 and -A33 alleles. Int. J. Oncol. 34:529-536.
56. Mongkolsapaya J, et al. 2006. T cell responses in dengue hemorrhagic fever: are cross-reactive T cells suboptimal? J. Immunol. 176:3821-3829.
57. Mullbacher A, Lobigs M, Alsharifi M, Regner M. 2006. Cytotoxic T-cell immunity as a target for influenza vaccines. Lancet Infect. Dis. 6:255-256.
58. Murshudov GN, Vagin AA, and Dodson EJ. 1997. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53:240-255.
59. Neumann G, Noda T, Kawaoka Y. 2009. Emergence and pandemic potential of swine-origin H1N1 influenza virus. Nature 459:931-939.
60. Otwinoski ZM, Minor W. 1997. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276:307.
61. Parker KC, Bednarek MA, Coligan JE. 1994. Scheme for ranking potential HLA-A2 binding peptides based on independent binding of individual peptide side-chains. J. Immunol. 152:163-175.
62. Parker KC, et al. 1992. Sequence motifs important for peptide binding to the human MHC class-I molecule, Hla-A2. J. Immunol. 149:3580-3587.
63. Purcell AW, McCluskey J, Rossjohn J. 2007. More than one reason to rethink the use of peptides in vaccine design. Nat. Rev. Drug Discov. 6:404-414.
64. Schanen BC, et al. 2011. Coupling sensitive in vitro and in silico techniques to assess cross-reactive CD4(+) T cells against the swine-origin H1N1 influenza virus. Vaccine 29:3299-3309.
65. Scheible K, et al. 2011. CD8+ T cell immunity to 2009 pandemic and seasonal H1N1 influenza viruses. Vaccine 29:2159-2168.
66. Sette A, Sidney J. 1999. Nine major HLA class I supertypes account for the vast preponderance of HLA-A and -B polymorphism. Immunogenetics 50:201-212.
67. Sidney J, et al. 1996. Definition of an HLA-A3-like supermotif demonstrates the overlapping peptide-binding repertoires of commonHLAmolecules. Hum. Immunol. 45:79-93.
68. Soboleski MR, et al. 2011. Cold-adapted influenza and recombinant adenovirus vaccines induce cross-protective immunity against pH1N1 challenge in mice. PLoS One 6:e21937. doi:10.1371/journal.pone.0021937.
69. Sun K, Ye J, Perez DR, Metzger DW. 2011. Seasonal FluMist vaccination induces cross-reactive T cell immunity against H1N1 (2009) influenza and secondary bacterial infections. J. Immunol. 186:987-993.
70. Sun Y, et al. 2010. Identification and structural definition of H5-specific CTL epitopes restricted by HLA-A*0201 derived from the H5N1 subtype of influenza A viruses. J. Gen. Virol. 91:919-930.
71. Sun Y, et al. 2010. In silico characterization of the functional and structural modules of the hemagglutinin protein from the swine-origin influenza virus A (H1N1)-2009. Sci. China Life Sci. 53:633-642.
72. Takedatsu H, et al. 2004. Identification of peptide vaccine candidates sharing among HLA-A3+, -A11+, -A31+, and -A33+ cancer patients. Clin. Cancer Res. 10:1112-1120.
73. Takiguchi M, Matsuda T, Tomiyama H. 2000. Polarity of the P1 anchor residue determines peptide binding specificity between HLA-A*3101 and HLA-A*3303. Tissue Antigens 56:501-506.
74. Terasaki Y, et al. 2009. An HLA-A3-binding prostate acid phosphatasederived peptide can induce CTLs restricted to HLA-A2 and -A24 alleles. Cancer Immunol. Immunother. 58:1877-1885.
75. Threlkeld SC, et al. 1997. Degenerate and promiscuous recognition by CTL of peptides presented by theMHCclass I A3-like superfamily: implications for vaccine development. J. Immunol. 159:1648-1657.
76. Townsend AR, Skehel JJ. 1982. Influenza A specific cytotoxic T-cell clones that do not recognize viral glycoproteins. Nature 300:655-657.
77. Townsend AR, Skehel JJ. 1984. The influenza A virus nucleoprotein gene controls the induction of both subtype specific and cross-reactive cytotoxic T cells. J. Exp. Med. 160:552-563.
78. Turnquist HR, et al. 2000. HLA-B polymorphism affects interactions with multiple endoplasmic reticulum proteins. Eur. J. Immunol. 30:3021-3028.
79. Ueno T, Tomiyama H, Takiguchi M. 2002. Single T cell receptormediated recognition of an identical HIV-derived peptide presented by multiple HLA class I molecules. J. Immunol. 169:4961-4969.
80. Valkenburg SA, et al. 2011. Immunity to seasonal and pandemic influenza A viruses. Microbes Infect. 13:489-501.
81. van der Burg SH, Visseren MJ, Brandt RM, Kast WM, Melief CJ. 1996. Immunogenicity of peptides bound toMHCclass I molecules depends on the MHC-peptide complex stability. J. Immunol. 156:3308-3314.
82. Wei CJ, et al. 2010. Cross-neutralization of 1918 and 2009 influenza viruses: role of glycans in viral evolution and vaccine design. Sci. Transl. Med. 2:24ra21.
83. Weinfurter JT, et al. 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.
84. 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.
85. Xuan C, et al. 2011. Structural vaccinology: structure-based design of influenza A virus hemagglutinin subtype-specific subunit vaccines. Protein Cell 2:997-1005.
86. Yap KL, Ada GL, McKenzie IF. 1978. Transfer of specific cytotoxic T lymphocytes protects mice inoculated with influenza virus. Nature 273:238-239.
87. Zernich D, et al. 2004. Natural HLA class I polymorphism controls the pathway of antigen presentation and susceptibility to viral evasion. J. Exp. Med. 200:13-24.
88. Zhang S, et al. 2011. Structural basis of cross-allele presentation by HLAA*0301 and HLA-A*1101 revealed by two HIV-derived peptide complexes. Mol. Immunol. 49:395-401.
89. Zhang W, et al. 2010. Crystal structure of the swine-origin A (H1N1)-2009 influenza A virus hemagglutinin (HA) reveals similar antigenicity to that of the 1918 pandemic virus. Protein Cell 1:459-467.