Asynchronous differentiation of CD8 T cells that recognize dominant and cryptic antigens

Journal of Immunology

Volumn 177, Issue 12, 2006, Pages 8466-8475

  Baron, Chantal ^a,b   Meunier, Marie Christine ^a,b   Caron, Étienne ^a,b   Côté, Caroline ^a,b   Cameron, Mark J ^c   Kelvin, David J ^c   LeBlanc, Richard ^d   Rineau, Vincent ^a,b   Perreault, Claude ^a,b  

^a INSTITUTE FOR RESEARCH IN IMMUNOLOGY AND CANCER   (Canada)

^b MAISONNEUVE ROSEMONT HOSPITAL   (Canada)

^c UNIVERSITY HEALTH NETWORK   (Canada)

^d CENTRE HOSPITALIER UNIVERSITAIRE DE SHERBROOKE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; CD8 ANTIGEN; CELL MARKER; CYTOKINE; H7 ANTIGEN; HY ANTIGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIGEN PRESENTING CELL; ANTIGEN RECOGNITION; ANTIGEN SPECIFICITY; ARTICLE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; EFFECTOR CELL; FEMALE; GENETIC TRANSCRIPTION; IMMUNE RESPONSE; LYMPHOCYTE DIFFERENTIATION; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; T LYMPHOCYTE SUBPOPULATION;

EID: 33845454691     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.177.12.8466     Document Type: Article

References (81)

1. Berger, M., P. J. Wettstein, and R. Korngold. 1994. T cell subsets involved in lethal graft-versus-host disease directed to immunodominant minor histocompatibility antigens. Transplantation 57: 1095-1102.
2. Yewdell, J. W., and J. R. Bennink. 1999. Immunodominance in major histocompatibility complex class I-restricted T lymphocyte responses. Annu. Rev. Immunol. 17: 51-88.
3. Perreault, C., D. C. Roy, and C. Fortin. 1998. Immunodominant minor histocompatibility antigens: the major ones. Immunol. Today 19: 69-74.
4. Choi, E. Y., G. J. Christianson, Y. Yoshimura, N. Jung, T. J. Sproule, S. Malarkannan, S. Joyce, and D. C. Roopenian. 2002. Real-time T-cell profiling identifies H60 as a major minor histocompatibility antigen in murine graft-versus-host disease. Blood 100: 4259-4264.
5. Kjer-Nielsen, L., C. S. Clements, A. W. Purcell, A. G. Brooks, J. C. Whisstock, S. R. Burrows, J. McCluskey, and J. Rossjohn. 2003. A structural basis for the selection of dominant αβ T cell receptors in antiviral immunity. Immunity 18: 53-64.
6. b-restricted HBsAg epitopes. J. Immunol. 168: 6253-6262.
7. + responses to viruses; cell biology, cellular immunology, and mathematical models. Immunity 21: 149-153.
8. Korngold, R., C. Leighton, L. E. Mobraaten, and M. A. Berger. 1997. Inter-strain graft-vs.-host disease T-cell responses to immunodominant minor histocompatibility antigens. Biol. Blood Marrow Transplant. 3: 57-64.
9. Nikolich-Žugich, J., M. K. Slifka, and I. Messaoudi. 2004. The many important facets of T-cell repertoire diversity. Nat. Rev. Immunol. 4: 123-132.
10. Barouch, D. H., J. Kunstman, M. J. Kuroda, J. E. Schmitz, S. Santra, F. W. Peyerl, G. R. Krivulka, K. Beaudry, M. A. Lifton, D. A. Gorgone, et al. 2002. Eventual AIDS vaccine failure in a rhesus monkey by viral escape from cytotoxic T lymphocytes. Nature 415: 335-339.
11. Erickson, A. L., Y. Kimura, S. Igarashi, J. Eichelberger, M. Houghton, J. Sidney, D. McKinney, A. Sette, A. L. Hughes, and C. M. Walker. 2001. The outcome of hepatitis C virus infection is predicted by escape mutations in epitopes targeted by cytotoxic T lymphocytes. Immunity 15: 883-895.
12. Berkhoff, E. G., A. C. Boon, N. J. Nieuwkoop, R. A. Fouchier, K. Sintnicolaas, A. D. Osterhaus, and G. F. Rimmelzwaan. 2004. A mutation in the HLA-B*2705-restricted NP383-391 epitope affects the human influenza A virus-specific cytotoxic T-lymphocyte response in vitro. J. Virol. 78: 5216-5222.
13. Deng, Y., J. W. Yewdell, L. C. Eisenlohr, and J. R. Bennink. 1997. MHC affinity, peptide liberation, T cell repertoire, and immunodominance all contribute to the paucity of MHC class I-restricted peptides recognized by antiviral CTL. J. Immunol. 158: 1507-1515.
14. Chen, W., L. C. Anton, J. R. Bennink, and J. W. Yewdell. 2000. Dissecting the multifactorial causes of immunodominance in class I-restricted T cell responses to viruses. Immunity 12: 83-93.
15. Kedl, R. M., J. W. Kappler, and P. Marrack. 2003. Epitope dominance, competition and T cell affinity maturation. Curr. Opin. Immunol. 15: 120-127.
16. Pion, S., P. Fontaine, M. Desaulniers, J. Jutras, J. G. Filep, and C. Perreault. 1997. On the mechanisms of immunodominance in cytotoxic T lymphocyte responses to minor histocompatibility antigens. Eur. J. Immunol. 27: 421-430.
17. Kedl, R. M., W. A. Rees, D. A. Hildeman, B. Schaefer, T. Mitchell, J. Kappler, and P. Marrack. 2000. T cells compete for access to antigen-bearing antigen-presenting cells. J. Exp. Med. 192: 1105-1114.
18. Grufman, P., E. Z. Wolpert, J. K. Sandberg, and K. Karre. 1999. T cell competition for the antigen-presenting cell as a model for immunodominance in the cytotoxic T lymphocyte response against minor histocompatibility antigens. Eur. J. Immunol. 29: 2197-2204.
19. Roy-Proulx, G., M. C. Meunier, A. M. Lanteigne, S. Brochu, and C. Perreault. 2001. Immunodomination results from functional differences between competing CTL. Eur. J. Immunol. 31: 2284-2292.
20. + T-cell responses is dramatically modified by DNA immunization and is regulated by γ interferon. J. Virol. 76: 4251-4259.
21. Willis, R. A., J. W. Kappler, and P. C. Marrack. 2006. CD8 T cell competition for dendritic cells in vivo is an early event in activation. Proc. Natl. Acad. Sci. USA 103: 12063-12068.
22. Pion, S., G. J. Christianson, P. Fontaine, D. C. Roopenian, and C. Perreault. 1999. Shaping the repertoire of cytotoxic T-lymphocyte responses: explanation for the immunodominance effect whereby cytotoxic T lymphocytes specific for immunodominant antigens prevent recognition of nondominant antigens. Blood 93: 952-962.
23. Roy-Proulx, G., C. Baron, and C. Perreault. 2005. CD8 T-cell ability to exert immunodomination correlates with T-cell receptor:epitope association rate. Biol. Blood Marrow Transplant. 11: 260-271.
24. Choi, E. Y., Y. Yoshimura, G. J. Christianson, T. J. Sproule, S. Malarkannan, N. Shastri, S. Joyce, and D. C. Roopenian. 2001. Quantitative analysis of the immune response to mouse non-MHC transplantation antigens in vivo: the H60 histocompatibility antigen dominates over all others. J. Immunol. 166: 4370-4379.
25. Casanova, J. L., and L. Abel. 2004. The human model: a genetic dissection of immunity to infection in natural conditions. Nat. Rev. Immunol. 4: 55-66.
26. b epitope is encoded by a novel mouse Y chromosome gene. Nat. Genet. 14: 474-478.
27. dom1 minor histocompatibility antigen is encoded by a mouse homolog of the yeast STT3 gene. Immunogenetics 54: 562-569.
28. Kelleher, D. J., D. Karaoglu, E. C. Mandon, and R. Gilmore. 2003. Oligosaccharyltransferase isoforms that contain different catalytic STT3 subunits have distinct enzymatic properties. Mol. Cell. 12: 101-111.
29. Terra, R., I. Louis, R. LeBlanc, S. Ouellet, J. C. Zúñiga- Pflücker, and C. Perreault. 2005. T cell generation by lymph node resident progenitor cells. Blood 106: 193-200.
30. Benoist, C., R. N. Germain, and D. Mathis. 2006. A plaidoyer for "systems immunology". Immunol. Rev. 210: 229-234.
31. Scott, D., C. Addey, P. Ellis, E. James, M. J. Mitchell, N. Saut, S. Jurcevic, and E. Simpson. 2000. Dendritic cells permit identification of genes encoding MHC class II restricted epitopes of transplantation antigens. Immunity 12: 711-720.
32. Gett, A. V., F. Sallusto, A. Lanzavecchia, and J. Geginat. 2003. T cell fitness determined by signal strength. Nat. Immunol. 4: 355-360.
33. + T cell differentiation: initial antigen encounter triggers a developmental program in naive cells. Nat. Immunol. 2: 415-422.
34. Kaech, S. M., C. Hemby, E. Kersh, and R. Ahmed. 2002. Molecular and functional profiling of memory CD8 T cell differentiation. Cell 111: 837-851.
35. + T cells recovered from an influenza pneumonia differentiate to a state of focused gene expression. Proc. Natl. Acad. Sci. USA 102: 6074-6079.
36. Goldrath, A. W., C. J. Luckey, R. Park, C. Benoist, and D. Mathis. 2004. The molecular program induced in T cells undergoing homeostatic proliferation. Proc. Natl. Acad. Sci. USA 101: 16885-16890.
37. Kaech, S. M., J. T. Tan, E. J. Wherry, B. T. Konieczny, C. D. Surh, and R. Ahmed. 2003. Selective expression of the interleukin 7 receptor identifies effector CD8 T cells that give rise to long-lived memory cells. Nat. Immunol. 4: 1191-1198.
38. Li, J., G. Huston, and S. L. Swain. 2003. IL-7 promotes the transition of CD4 effectors to persistent memory cells. J. Exp. Med. 198: 1807-1815.
39. Barry, M., and R. C. Bleackley. 2002. Cytotoxic T lymphocytes: all roads lead to death. Nat. Rev. Immunol. 2: 401-409.
40. Lieberman, J., and Z. Fan. 2003. Nuclear war: the granzyme A-bomb. Curr. Opin. Immunol. 15: 553-559.
41. Zeng, Q., T. T. Tran, H. X. Tan, and W. Hong. 2003. The cytoplasmic domain of Vamp4 and Vamp5 is responsible for their correct subcellular targeting: the N-terminal extenSion of VAMP4 contains a dominant autonomous targeting signal for the trans-Golgi network. J. Biol. Chem. 278: 23046-23054.
42. Das, V., B. Nal, A. Dujeancourt, M. I. Thoulouze, T. Galli, P. Roux, A. Dautry-Varsat, and A. Alcover. 2004. Activation-induced polarized recycling targets T cell antigen receptors to the immunological synapse; involvement of SNARE complexes. Immunity 20: 577-588.
43. Mikulits, W., T. Sauer, A. A. Infante, J. A. Garcia-Sanz, and E. W. Mullner. 1997. Structure and function of the iron-responsive element from human ferritin L chain mRNA. Biochem. Biophys. Res. Commun. 235: 212-216.
44. Jin, Y., E. Knudsen, L. Wang, Y. Bryceson, B. Damaj, S. Gessani, and A. A. Maghazachi. 2003. Sphingosine 1-phosphate is a novel inhibitor of T-cell proliferation. Blood 101: 4909-4915.
45. von Andrian, U. H., and C. R. Mackay. 2000. T-cell function and migration: two sides of the same coin. N. Engl. J. Med. 343: 1020-1034.
46. Voehringer, D., C. Blaser, P. Brawand, D. H. Raulet, T. Hanke, and H. Pircher. 2001. Viral infections induce abundant numbers of senescent CD8 T cells. J. Immunol. 167: 4838-4843.
47. Beyersdorf, N. B., X. Ding, K. Karp, and T. Hanke. 2001. Expression of inhibitory "killer cell lectin-like receptor G1′" identifies unique subpopulations of effector and memory CD8 T cells. Eur. J. Immunol. 31: 3443-3452.
48. Grundemann, C., M. Bauer, O. Schweier, N. von Oppen, U. Lassing, P. Saudan, K. F. Becker, K. Karp, T. Hanke, M. F. Bachmann, and H. Pircher. 2006. Cutting edge: identification of E-cadherin as a ligand for the murine killer cell lectin-like receptor G1. J. Immunol. 176: 1311-1315.
49. Ito, M., T. Maruyama, N. Saito, S. Koganei, K. Yamamoto, and N. Matsumoto. 2006. Killer cell lectin-like receptor G1 binds three members of the classical cadherin family to inhibit NK cell cytotoxicity. J. Exp. Med. 203: 289-295.
50. Nagai, S., S. Hashimoto, T. Yamashita, N. Toyoda, T. Satoh, T. Suzuki, and K. Matsushima. 2001. Comprehensive gene expression profile of human activated Th1- and Th2-polarized cells. Int. Immunol. 13: 367-376.
51. + T cells are programmed by prolonged antigen exposure and low levels of cellular activation. Eur. J. Immunol. 36: 842-854.
52. Ahn, A. C., M. Tewari, C. S. Poon, and R. S. Phillips. 2006. The limits of reductionism in medicine: could systems biology offer an alternative? PLoS. Med. 3: e208.
53. Harrington, L. E., M. Galvan, L. G. Baum, J. D. Altman, and R. Ahmed. 2000. Differentiating between memory and effector CD8 T cells by altered expression of cell surface O-glycans. J. Exp. Med. 191: 1241-1246.
54. Onami, T. M., L. E. Harrington, M. A. Williams, M. Galvan, C. P. Larsen, T. C. Pearson, N. Manjunath, L. G. Baum, B. D. Pearce, and R. Ahmed. 2002. Dynamic regulation of T cell immunity by CD43. J. Immunol. 168: 6022-6031.
55. Meunier, M. C., J. S. Delisle, J. Bergeron, V. Rineau, C. Baron, and C. Perreault. 2005. T cells targeted against a single minor histocompatibility antigen can cure solid tumors. Nat. Med. 11: 1222-1229.
56. Wolpert, E. Z., P. Grufman, J. K. Sandberg, A. Tegnesjö, and K. Kärre. 1998. Immunodominance in the CTL response against minor histocompatibility antigens: interference between responding T cells, rather than with presentation of epitopes. J. Immunol. 161: 4499-4505.
57. + T cells after infection. Nat. Immunol. 3: 619-626.
58. Wong, P., and E. G. Pamer. 2003. CD8 T cell responses to infectious pathogens. Annu. Rev. Immunol. 21: 29-70.
59. + T cells initiate IFN-γ synthesis increases markedly over the course of infection and correlates with immunodominance. J. Immunol. 173: 456-441.
60. + T cell homeostasis by perform and interferon-α. Science 290: 1354-1357.
61. Brehm, M. A., K. A. Daniels, and R. M. Welsh. 2005. Rapid production of TNF-α following TCR engagement of naive CD8 T cells. J. Immunol. 175: 5043-5049.
62. + T-cell memory. Nat. Med. 7: 913-919.
63. D'Souza, W. N., and S. M. Hedrick. 2006. Cutting edge: latecomer CD8 T cells are imprinted with a unique differentiation program. J. Immunol. 177: 777-781.
64. Ehl, S., P. Klenerman, P. Aichele, H. Hengartner, and R. M. Zinkernagel. 1997. A functional and kinetic comparison of antiviral effector and memory cytotoxic T lymphocyte populations in vivo and in vitro. Eur. J. Immunol. 27: 3404-3413.
65. Blattman, J. N., J. M. Grayson, E. J. Wherry, S. M. Kaech, K. A. Smith, and R. Ahmed. 2003. Therapeutic use of IL-2 to enhance antiviral T-cell responses in vivo. Nat. Med. 9: 540-547.
66. + effector and memory T cell generation. Nat. Immunol. 4: 835-842.
67. + memory cell pool. J. Clin. Invest. 115: 1177-1187.
68. Blattman, J. N., D. J. Sourdive, K. Murali-Krishna, R. Ahmed, and J. D. Altman. 2000. Evolution of the T cell repertoire during primary, memory, and recall responses to viral infection. J. Immunol. 165: 6081-6090.
69. + T cell immunodominance in primary and secondary influenza virus infections. J. Exp. Med. 198: 399-410.
70. + T cell populations specific for persistent DNA viruses. J. Exp. Med. 202: 1349-1361.
71. Bihl, F., N. Frahm, L. Di Giammarino, J. Sidney, M. John, K. Yusim, T. Woodberry, K. Sango, H. S. Hewitt, L. Henry, et al. 2006. Impact of HLA-B alleles, epitope binding affinity, functional avidity, and viral coinfection on the immunodominance of virus-specific CTL responses. J. Immunol. 176: 4094-4101.
72. Alexander-Miller, M. A., G. R. Leggatt, and J. A. Berzofsky. 1996. Selective expansion of high- or low-avidity cytotoxic T lymphocytes and efficacy for adoptive immunotherapy. Proc. Natl. Acad. Sci. USA 93: 4102-4107.
73. + lymphocytes respond to different HIV epitopes in seronegative and infected subjects. J. Clin. Invest. 107: 1303-1310.
74. Frahm, N., P. Kiepiela, S. Adams, C. H. Linde, H. S. Hewitt, K. Sango, M. E. Feeney, M. M. Addo, M. Lichterfeld, M. P. Lahaie, et al. 2006. Control of human immunodeficiency virus replication by cytotoxic T lymphocytes targeting subdominant epitopes. Nat. Immunol. 7: 173-178.
75. Loyer, V., P. Fontaine, S. Pion, F. Hétu, D. C. Roy, and C. Perreault. 1999. The in vivo fate of APCs displaying minor H antigens and/or MHC differences is regulated by CTLs specific for immunodominant class I-associated epitopes. J. Immunol. 163: 6462-6467.
76. + T cell response. J. Exp. Med. 203: 2135-2143.
77. Langenkamp, A., M. Messi, A. Lanzavecchia, and F. Sallusto. 2000. Kinetics of dendritic cell activation: impact on priming of Th1, Th2 and nonpolarized T cells. Nat. Immunol. 1: 311-316.
78. Wong, P., and E. G. Pamer. 2003. Feedback regulation of pathogen-specific T cell priming. Immunity 18: 499-511.
79. + T cells can protect APC from CTL-mediated elimination. J. Immunol. 176: 7379-7384.
80. + T cells in vivo. Proc. Natl. Acad. Sci. USA 103: 147-152.
81. Hamilton, S. E., B. B. Porter, K. A. Nordyke Messingham, V. P. Badovinac, and J. T. Harty. 2004. MHC class Ia-restricted memory T cells inhibit expansion of a nonprotective MHC class Ib (H2-M3)-restricted memory response. Nat. Immunol. 5: 159-168.