Nucleoprotein of influenza A virus is a major target of immunodominant CD8 + T-cell responses

Immunology and Cell Biology

Volumn 91, Issue 2, 2013, Pages 184-194

  Grant, Emma ^a   Wu, Chao ^b,c   Chan, Kok Fei ^c   Eckle, Sidonia ^a   Bharadwaj, Mandvi ^a   Zou, Quan Ming ^b   Kedzierska, Katherine ^a   Chen, Weisan ^c,d  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b THIRD MILITARY MEDICAL UNIVERSITY   (China)

^c LUDWIG INSTITUTE FOR CANCER RESEARCH   (Australia)

^d LA TROBE UNIVERSITY   (Australia)

Author keywords

CD8 T cell; epitope; HLA; immunodominance; influenza A virus

Indexed keywords

EPITOPE; HLA A2 ANTIGEN; VIRUS NUCLEOPROTEIN;

ALLELE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CLUSTER ANALYSIS; INFLUENZA VIRUS A; NONHUMAN; PROTEIN TARGETING; VIRUS STRAIN;

ALGORITHMS; ALLELES; AMINO ACID SEQUENCE; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE; CONSERVED SEQUENCE; HLA-A2 ANTIGEN; HUMANS; IMMUNODOMINANT EPITOPES; INFLUENZA A VIRUS; MOLECULAR SEQUENCE DATA; PEPTIDES; PROTEIN BINDING; RNA-BINDING PROTEINS; VIRAL CORE PROTEINS;

EID: 84873683924     PISSN: 08189641     EISSN: 14401711     Source Type: Journal    
DOI: 10.1038/icb.2012.78     Document Type: Article

References (33)

1. Valkenburg SA, Rutigliano J, Ellebedy AH, Doherty PC, Thomas PG, Kedzierska K. Immunity to seasonal and pandemic influenza A viruses. Microb Infect 2011; 13: 489-501.
2. Valkenburg SA, Venturi V, Dang TH, Bird NL, Doherty PC, Turner SJ et al. Early priming minimizes the age-related immune compromise of CD8 T cell diversity and function. Plos Pathog 2012; 8: e1002544.
3. Doherty PC, Topham DJ, Tripp RA. Establishment and persistence of virus-specific CD4\+ and CD8\+ T cell memory. Immunol Rev 1996; 150: 23-44.
4. Doherty PC, Turner SJ, Webby RG, Thomas PG. Influenza and the challenge for immunology. Nat Immunol 2006; 7: 449-455.
5. McMichael AJ, Gotch FM, Noble GR, Beare PA. Cytotoxic T-cell immunity to influenza. N Engl J Med 1983; 309: 13-17.
6. Epstein SL. Prior H1N1 influenza infection and susceptibility of Cleveland Family Study participants during the H2N2 pandemic of 1957: an experiment of nature. J Infect Dis 2006; 193: 49-53.
7. Kreijtz JH, de Mutsert G, van Baalen CA, Fouchier RA, Osterhaus AD, Rimmelzwaan GF. Cross-recognition of avian H5N1 influenza virus by human cytotoxic T lymphocyte populations directed to human influenza A virus. J Virol 2008; 82: 5161-5166.
8. Lee LY, Ha do LA, Simmons C, de Jong MD, Chau NV, 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 2008; 118: 3478-3490.
9. Goulder PJ, Watkins DI. Impact of MHC class I diversity on immune control of immunodeficiency virus replication. Nat Rev Immunol 2008; 8: 619-630.
10. Leslie AJ, Pfafferott KJ, Chetty P, Draenert R, Addo MM, Feeney M et al. HIV evolution: CTL escape mutation and reversion after transmission. Nat Med 2004; 10: 282-289.
11. Boon AC, de Mutsert G, van Baarle D, Smith DJ, Lapedes AS, Fouchier RA et al. Recognition of homo-and heterosubtypic variants of influenza A viruses by human CD8\+ T lymphocytes. J Immunol 2004; 172: 2453-2460.
12. Voeten JT, Bestebroer TM, Nieuwkoop NJ, Fouchier RA, Osterhaus AD, Rimmelzwaan GF. Antigenic drift in the influenza A virus (H3N2) nucleoprotein and escape from recognition by cytotoxic T lymphocytes. J Virol 2000; 74: 6800-6807.
13. Wu C, Zanker D, Valkenburg S, Tan B, Kedzierska K, Zou QM et al. Systematic identification of immunodominant CD8\+ T-cell responses to influenza A virus in HLAA2 individuals. Proc Natl Acad Sci USA 2011; 108: 9178-9183.
14. Jackson HM, Dimopoulos N, Chen Q, Luke T, Yee Tai T, Maraskovsky E et al. A robust human T-cell culture method suitable for monitoring CD8\+ and CD4\+ T-cell responses from cancer clinical trial samples. J Immunol Methods 2004; 291: 51-62.
15. Gschoesser C, Almanzar G, Hainz U, Ortin J, Schonitzer D, Schild H et al. CD4\+ and CD8\+ mediated cellular immune response to recombinant influenza nucleoprotein. Vaccine 2002; 20: 3731-3738.
16. Voeten JT, Rimmelzwaan GF, Nieuwkoop NJ, Fouchier RA, Osterhaus AD. Antigen processing for MHC class I restricted presentation of exogenous influenza A virus nucleoprotein by B-lymphoblastoid cells. Clin Exp Immunol 2001; 125: 423-431.
17. Wang M, Lamberth K, Harndahl M, Roder G, Stryhn A, Larsen MV et al. CTL epitopes for influenza A including the H5N1 bird flu; genome-, pathogen-, and HLA-wide screening. Vaccine 2007; 25: 2823-2831.
18. Alexander J, Bilsel P, del Guercio MF, Marinkovic-Petrovic A, Southwood S, Stewart S et al. Identification of broad binding class I HLA supertype epitopes to provide universal coverage of influenza A virus. Hum Immunol 2010; 71: 468-474.
19. Silver ML, Guo HC, Strominger JL, Wiley DC. Atomic structure of a human MHC molecule presenting an influenza virus peptide. Nature 1992; 360: 367-369.
20. McMichael AJ, Gotch FM, Rothbard J. HLA B37 determines an influenza A virus nucleoprotein epitope recognized by cytotoxic T lymphocytes. J Exp Med 1986; 164: 1397-1406.
21. DiBrino M, Parker KC, Margulies DH, Shiloach J, Turner RV, Biddison WE et al. Identification of the peptide binding motif for HLA-B44, one of the most common HLA-B alleles in the Caucasian population. Biochemistry 1995; 34: 10130-10138.
22. Boon AC, de Mutsert G, Graus YM, Fouchier RA, Sintnicolaas K, Osterhaus AD et al. Sequence variation in a newly identified HLA-B35-restricted epitope in the influenza A virus nucleoprotein associated with escape from cytotoxic T lymphocytes. J Virol 2002; 76: 2567-2572.
23. Valkenburg SA, Gras S, Guillonneau C, La Gruta NL, Thomas PG, Purcell AW et al. Protective efficacy of cross-reactive CD8\+ T cells recognising mutant viral epitopes depends on peptide-MHC-I structural interactions and T cell activation threshold. PLoS Pathog 2010; 6: e1001039.
24. Gras S, Kedzierski L, Valkenburg SA, Laurie K, Liu YC, Denholm JT et al. Cross-reactive CD8\+ T-cell immunity between the pandemic H1N1-2009 and H1N1-1918 influenza A viruses. Proc Natl Acad Sci USA 2010; 107: 12599-12604.
25. Erup Larsen M, Kloverpris H, Stryhn A, Koofhethile CK, Sims S, Ndung'u T et al. HLArestrictor-a tool for patient-specific predictions of HLA restriction elements and optimal epitopes within peptides. Immunogenetics 2011; 63: 43-55.
26. Assarsson E, Bui HH, 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 2008; 82: 12241-12251.
27. Belz GT, Stevenson PG, Doherty PC. Contemporary analysis of MHC-related immunodominance hierarchies in the CD8\+ T cell response to influenza A viruses. J Immunol 2000; 165: 2404-2409.
28. Kedzierska K, Valkenburg SA, Guillonneau C, Hubert FX, Cukalac T, Curtis JM et al. Diversity and clonotypic composition of influenza-specific CD8\+ TCR repertoires remain unaltered in the absence of Aire. Eur J Immunol 2010; 40: 849-858.
29. Chen W, Anton LC, Bennink JR, Yewdell JW. Dissecting the multifactorial causes of immunodominance in class I-restricted T cell responses to viruses. Immunity 2000; 12: 83-93.
30. Chen W, Pang K, Masterman KA, Kennedy G, Basta S, Dimopoulos N et al. Reversal in the immunodominance hierarchy in secondary CD8\+ T cell responses to influenza A virus: roles for cross-presentation and lysis-independent immunodomination. J Immunol 2004; 173: 5021-5027.
31. Shaw ML, Stone KL, Colangelo CM, Gulcicek EE, Palese P. Cellular proteins in influenza virus particles. PLoS Pathog 2008; 4: e1000085.
32. Chaves FA, Lee AH, Nayak JL, Richards KA, Sant AJ. The utility and limitations of current Web-available algorithms to predict peptides recognized by CD4 T cells in response to pathogen infection. J Immunol 2012; 188: 4235-4248.
33. Rehermann B, Chang KM, McHutchinson J, Kokka R, Houghton M, Rice CM et al. Differential cytotoxic T-lymphocyte responsiveness to the hepatitis B and C viruses in chronically infected patients. J Virol 1996; 70: 7092-7102.