Broad cross-reactive TCR repertoires recognizing dissimilar Epstein-Barr and influenza a virus epitopes

Journal of Immunology

Volumn 185, Issue 11, 2010, Pages 6753-6764

  Clute, Shalyn C ^a   Naumov, Yuri N ^a   Watkin, Levi B ^a   Aslan, Nuray ^a   Sullivan, John L ^a   Thorley Lawson, David A ^b   Luzuriaga, Katherine ^a   Welsh, Raymond M ^a   Puzone, Roberto ^c   Celada, Franco ^d   Selin, Liisa K ^a  

^a UNIVERSITY OF MASSACHUSETTS   (United States)

^b TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c National Institute for Cancer Research   (United States)

^d NYU HOSPITAL FOR JOINT DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; EPSTEIN BARR VIRUS ANTIGEN; HLA A2 ANTIGEN; T LYMPHOCYTE RECEPTOR; VIRUS ANTIGEN;

ADULT; ANTIGEN RECOGNITION; ARTICLE; CELLULAR IMMUNITY; COMPUTER SIMULATION; CONTROLLED STUDY; CROSS REACTION; EPSTEIN BARR VIRUS; HUMAN; HUMAN CELL; INFECTION RESISTANCE; INFLUENZA VIRUS A; MEMORY T LYMPHOCYTE; MOLECULAR CLONING; PRIORITY JOURNAL; STRUCTURAL HOMOLOGY;

ADOLESCENT; ADULT; CD8-POSITIVE T-LYMPHOCYTES; CLONE CELLS; CROSS REACTIONS; EPITOPES, T-LYMPHOCYTE; HERPESVIRUS 4, HUMAN; HLA-A2 ANTIGEN; HUMANS; IMMUNODOMINANT EPITOPES; INFLUENZA A VIRUS; MIDDLE AGED; OLIGOPEPTIDES; PEPTIDE FRAGMENTS; RECEPTORS, ANTIGEN, T-CELL; VIRAL MATRIX PROTEINS; YOUNG ADULT;

EID: 78650647253     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1000812     Document Type: Article

References (50)

1. Dutton, R. W., L. M. Bradley, and S. L. Swain. 1998. T cell memory. Annu. Rev. Immunol. 16:201-223.
2. Sprent, J., and C. D. Surh. 2002. T cell memory. Annu. Rev. Immunol. 20:551-579.
3. Welsh, R. M., L. K. Selin, and E. Szomolanyi-Tsuda. 2004. Immunological memory to viral infections. Annu. Rev. Immunol. 22:711-743.
4. Chen, H. D., A. E. Fraire, I. Joris, M. A. Brehm, R. M. Welsh, and L. K. Selin. 2001. Memory CD8+ T cells in heterologous antiviral immunity and immunopathology in the lung. Nat. Immunol. 2:1067-1076.
5. Selin, L. K., and R. M. Welsh. 2004. Plasticity of T cell memory responses to viruses. Immunity 20:5-16.
6. Cornberg, M., A. T. Chen, L. A. Wilkinson, M. A. Brehm, S. K. Kim, C. Calcagno, D. Ghersi, R. Puzone, F. Celada, R. M. Welsh, and L. K. Selin. 2006. Narrowed TCR repertoire and viral escape as a consequence of heterologous immunity. J. Clin. Invest. 116:1443-1456.
7. Brehm, M. A., A. K. Pinto, K. A. Daniels, J. P. Schneck, R. M. Welsh, and L. K. Selin. 2002. T cell immunodominance and maintenance of memory regulated by unexpectedly cross-reactive pathogens. Nat. Immunol. 3:627-634.
8. Haanen, J. B., M. C. Wolkers, A. M. Kruisbeek, and T. N. Schumacher. 1999. Selective expansion of cross-reactive CD8 (+) memory T cells by viral variants. J. Exp. Med. 190:1319-1328.
9. Urbani, S., B. Amadei, P. Fisicaro, M. Pilli, G. Missale, A. Bertoletti, and C. Ferrari. 2005. Heterologous T cell immunity in severe hepatitis C virus infection. J. Exp. Med. 201:675-680.
10. Borrow, P., H. Lewicki, X. Wei, M. S. Horwitz, N. Peffer, H. Meyers, J. A. Nelson, J. E. Gairin, B. H. Hahn, M. B. Oldstone, and G. M. Shaw. 1997. Antiviral pressure exerted by HIV-1-specific cytotoxic T lymphocytes (CTLs) during primary infection demonstrated by rapid selection of CTL escape virus. Nat. Med. 3:205-211.
11. Khan, N., M. Cobbold, R. Keenan, and P. A. Moss. 2002. Comparative analysis of CD8+ T cell responses against human cytomegalovirus proteins pp65 and immediate early 1 shows similarities in precursor frequency, oligoclonality, and phenotype. J. Infect. Dis. 185:1025-1034.
12. Meyer-Olson, D., N. H. Shoukry, K. W. Brady, H. Kim, D. P. Olson, K. Hartman, A. K. Shintani, C. M. Walker, and S. A. Kalams. 2004. Limited T cell receptor diversity of HCV-specific T cell responses is associated with CTL escape. J. Exp. Med. 200:307-319.
13. Peggs, K., S. Verfuerth, A. Pizzey, J. Ainsworth, P. Moss, and S. Mackinnon. 2002. Characterization of human cytomegalovirus peptide-specific CD8 (+) T-cell repertoire diversity following in vitro restimulation by antigen-pulsed dendritic cells. Blood 99:213-223.
14. Clute, S. C, L. B. Watkin, M. Cornberg, Y. N. Naumov, J. L. Sullivan, K. Luzuriaga, R. M. Welsh, and L. K. Selin. 2005. Cross-reactive influenza virus-specific CD8+ T cells contribute to lymphoproliferation in Epstein-Barr virus-associated infectious mononucleosis. J. Clin. Invest. 115:3602-3612.
15. Lawson, T. M., S. Man, S. Williams, A. C. Boon, M. Zambon, and L. K. Borysiewicz. 2001. Influenza A antigen exposure selects dominant Vbeta17+ TCR in human CD8+ cytotoxic T cell responses. Int. Immunol. 13:1373-1381.
16. Lehner, P. J., E. C. Wang, P. A. Moss, S. Williams, K. Platt, S. M. Friedman, J. I. Bell, and L. K. Borysiewicz. 1995. Human HLA-A0201-restricted cytotoxic T lymphocyte recognition of influenza A is dominated by T cells bearing the V beta 17 gene segment. J. Exp. Med. 181:79-91.
17. Moss, P. A., R. J. Moots, W. M. Rosenberg, S. J. Rowland-Jones, H. C. Bodmer, A. J. McMichael, and J. I. Bell. 1991. Extensive conservation of alpha and beta chains of the human T-cell antigen receptor recognizing HLA-A2 and influenza A matrix peptide. Proc. Natl. Acad. Sci. USA 88:8987-8990.
18. Naumov, Y. N., K. T Hogan, E. N. Naumova, J. T Pagel, and J. Gorski. 1998. A class I MHC-restricted recall response to a viral peptide is highly polyclonal despite stringent CDR3 selection: implications for establishing memory T cell repertoires in "real-world" conditions. J. Immunol. 160:2842-2852.
19. Naumov, Y. N., E. N. Naumova, K. T Hogan, L. K. Selin, and J. Gorski. 2003. A fractal clonotype distribution in the CD8+ memory T cell repertoire could optimize potential for immune responses. J. Immunol. 170:3994-4001.
20. Annels, N. E., M. F Callan, L. Tan, and A. B. Rickinson. 2000. Changing patterns of dominant TCR usage with maturation of an EBV-specific cytotoxic T cell response. J. Immunol. 165:4831-4841.
21. Cohen, G. B., S. A. Islam, M. S. Noble, C. Lau, C. Brander, M. A. Altfeld, E. S. Rosenberg, J. E. Schmitz, T. O. Cameron, and S. A. Kalams. 2002. Clonotype tracking of TCR repertoires during chronic virus infections. Virology 304:474-484.
22. Lim, A., L. Trautmann, M. A. Peyrat, C. Couedel, F. Davodeau, F. Romagne, P. Kourilsky, and M. Bonneville. 2000. Frequent contribution of T cell clonotypes with public TCR features to the chronic response against a dominant EBV-derived epitope: application to direct detection of their molecular imprint on the human peripheral T cell repertoire. J. Immunol. 165:2001-2011.
23. Catalina, M. D., J. L. Sullivan, K. R. Bak, and K. Luzuriaga. 2001. Differential evolution and stability of epitope-specific CD8 (+) T cell responses in EBV infection. J. Immunol. 167:4450-4457.
24. Arden, B., S. P. Clark, D. Kabelitz, and T. W. Mak. 1995. Human T-cell receptor variable gene segment families. Immunogenetics 42:455-500. (Pubitemid 26025063)
25. Han, M., L. Harrison, P. Kehn, K. Stevenson, J. Currier, and M. A. Robinson. 1999. Invariant or highly conserved TCR alpha are expressed on double-negative (CD3+CD4-CD8-) and CD8+ T cells. J. Immunol. 163:301-311.
26. Maslanka, K., T. Piatek, J. Gorski, M. Yassai, and J. Gorski. 1995. Molecular analysis of T cell repertoires. Spectratypes generated by multiplex polymerase chain reaction and evaluated by radioactivity or fluorescence. Hum. Immunol. 44:28-34.
27. Bahl, K., S. K. Kim, C. Calcagno, D. Ghersi, R. Puzone, F. Celada, L. K. Selin, and R. M. Welsh. 2006. IFN-induced attrition of CD8 T cells in the presence or absence of cognate antigen during the early stages of viral infections. J. Immunol. 176:4284-4295.
28. Cheng, Y, D. Ghersi, C. Calcagno, L. K. Selin, R. Puzone, and F. Celada. 2009. A discrete computer model of the immune system reveals competitive interactions between the humoral and cellular branch and between cross-reacting memory and naïve responses. Vaccine 27:833-845.
29. Kohler, B., R. Puzone, P. E. Seiden, and F. Celada. 2000. A systematic approach to vaccine complexity using an automaton model of the cellular and humoral immune system. I. Viral characteristics and polarized responses. Vaccine 19:862-876.
30. Selin, L. K., M. Cornberg, M. A. Brehm, S. K. Kim, C. Calcagno, D. Ghersi, R. Puzone, F. Celada, and R. M. Welsh. 2004. CD8 memory T cells: crossreactivity and heterologous immunity. Semin. Immunol. 16:335-347.
31. Callan, M. F., C. Fazou, H. Yang, T. Rostron, K. Poon, C. Hatton, and A. J. McMichael. 2000. CD8 (+) T-cell selection, function, and death in the primary immune response in vivo. J. Clin. Invest. 106:1251-1261.
32. Bousso, P., A. Casrouge, J. D. Altman, M. Haury, J. Kanellopoulos, J. P. Abastado, and P. Kourilsky. 1998. Individual variations in the murine T cell response to a specific peptide reflect variability in naive repertoires. Immunity 9:169-178.
33. Cibotti, R., J. P. Cabaniols, C. Pannetier, C. Delarbre, I. Vergnon, J. M. Kanellopoulos, and P. Kourilsky. 1994. Public and private V beta T cell receptor repertoires against hen egg white lysozyme (HEL) in nontransgenic versus HEL transgenic mice. J. Exp. Med. 180:861-872.
34. Kim, S. K., M. Cornberg, X. Z. Wang, H. D. Chen, L. K. Selin, and R. M. Welsh. 2005. Private specificities of CD8 T cell responses control patterns of heterologous immunity. J. Exp. Med. 201:523-533.
35. Naumov, Y. N., E. N. Naumova, S. C. Clute, L. B. Watkin, K. Kota, J. Gorski, and L. K. Selin. 2006. Complex T cell memory repertoires participate in recall responses at extremes of antigenic load. J. Immunol. 177:2006-2014.
36. Yassai, M., E. N. Naumova, and J. Gorski. 1997. Generation of TCR spectratypes by multiplex PCR for T cell repertoire analysis. In The Antigen T Cell Receptor: Selected Protocols and Applications. J. R. Oksenberg, ed. Landes Company and Chapman & Hall, Austin, TX, p. 327-372.
37. Naumov, Y. N., E. N. Naumova, M. B. Yassai, K. Kota, R. M. Welsh, and L. K. Selin. 2008. Multiple glycines in TCR alpha-chains determine clonally diverse nature of human T cell memory to influenza A virus. J. Immunol. 181:7407-7419.
38. Abergel, C., and J. M. Claverie. 1991. A strong propensity toward loop formation characterizes the expressed reading frames of the D segments at the Ig H and T cell receptor loci. Eur. J. Immunol. 21:3021-3025.
39. Bentley, G. A., and R. A. Mariuzza. 1996. The structure of the T cell antigen receptor. Annu. Rev. Immunol. 14:563-590.
40. Cornberg, M., S. C. Clute, L. B. Watkin, F. M. Saccoccio, S. K. Kim, Y. N. Naumov, M. A. Brehm, N. Aslan, R. M. Welsh, and L. K. Selin. 2010. CD8 T cell cross-reactivity networks mediate heterologous immunity in human EBV and murine vaccinia virus infections. J. Immunol. 184:2825-2838.
41. Zehn, D., S. Y. Lee, and M. J. Bevan. 2009. Complete but curtailed T-cell response to very low-affinity antigen. Nature 458:211-214.
42. Xu, X., I. Beckman, M. Ahern, and J. Bradley. 1993. A comprehensive analysis of peripheral blood lymphocytes in healthy aged humans by flow cytometry. Immunol. Cell Biol. 71:549-557.
43. Provinciali, M., R. Moresi, A. Donnini, and R. M. Lisa. 2009. Reference values for CD4+ and CD8+ T lymphocytes with naïve or memory phenotype and their association with mortality in the elderly. Gerontology 55:314-321.
44. Stulnig, T., C. Maczek, G. Böck, O. Majdic, and G. Wick. 1995. Reference intervals for human peripheral blood lymphocyte subpopulations from'healthy' young and aged subjects. Int. Arch. Allergy Immunol. 108:205-210.
45. Utsuyama, M., K. Hirokawa, C. Kurashima, M. Fukayama, T. Inamatsu, K. Suzuki, W. Hashimoto, and K. Sato. 1992. Differential age-change in the numbers of CD4+CD45RA+ and CD4+CD29+ T cell subsets in human peripheral blood. Mech. Ageing Dev. 63:57-68.
46. Selin, L. K., M. Y. Lin, K. A. Kraemer, D. M. Pardoll, J. P. Schneck, S. M. Varga, P. A. Santolucito, A. K. Pinto, and R. M. Welsh. 1999. Attrition of T cell memory: selective loss of LCMV epitope-specific memory CD8 T cells following infections with heterologous viruses. Immunity 11:733-742.
47. Selin, L. K., K. Vergilis, R. M. Welsh, and S. R. Nahill. 1996. Reduction of otherwise remarkably stable virus-specific cytotoxic T lymphocyte memory by heterologous viral infections. J. Exp. Med. 183:2489-2499.
48. Welsh, R. M., and L. K. Selin. 2009. Attrition of memory CD8 T cells. Nature 459: E3-4; discussion E4.
49. Hammarlund, E., M. W. Lewis, S. G. Hansen, L. I. Strelow, J. A. Nelson, G. J. Sexton, J. M. Hanifin, and M. K. Slifka. 2003. Duration of antiviral immunity after smallpox vaccination. Nat. Med. 9:1131-1137.
50. Chothia, C., D. R. Boswell, and A. M. Lesk. 1988. The outline structure of the T-cell alpha beta receptor. EMBO J. 7:3745-3755.