Changes to peptide structure, not concentration, contribute to expansion of the lowest avidity cytotoxic T lymphocytes

Journal of Leukocyte Biology

Volumn 76, Issue 4, 2004, Pages 787-795

  Leggatt, Graham R ^a,b   Narayan, Sharmal ^a   Fernando, Germain J P ^a   Frazer, Ian H ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b PRINCESS ALEXANDRA HOSPITAL   (Australia)

Author keywords

Adoptive immunotherapy; CTL; T cell growth; T cell receptors; Variant peptides

Indexed keywords

ANTIGEN; AUTOANTIGEN; CD8 ANTIGEN; EPITOPE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; PEPTIDE; T LYMPHOCYTE RECEPTOR;

ADOPTIVE IMMUNOTHERAPY; AMINO ACID SUBSTITUTION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL ADHESION; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; CYTOTOXICITY; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME LINKED IMMUNOSPOT ASSAY; EX VIVO STUDY; IMMUNOLOGICAL TOLERANCE; IMMUNOTHERAPY; IN VITRO STUDY; MOUSE; NONHUMAN; OUTCOMES RESEARCH; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN STRUCTURE; REGULATORY MECHANISM; T LYMPHOCYTE SUBPOPULATION;

ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; CELL SURVIVAL; COMPLEMENTARITY DETERMINING REGIONS; CYTOTOXICITY, IMMUNOLOGIC; ENZYME-LINKED IMMUNOSORBENT ASSAY; GENES, T-CELL RECEPTOR BETA; HUMANS; IMMUNIZATION; INTERFERON TYPE II; MICE; MICE, INBRED C57BL; ONCOGENE PROTEINS, VIRAL; PEPTIDE FRAGMENTS; T-LYMPHOCYTES, CYTOTOXIC;

ANIMALIA;

EID: 4744353167     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0104026     Document Type: Article

References (31)

1. Bromley, S. K., Burack, W. R., Johnson, K. G., Somersalo, K., Sims, T. N., Sumen, C., Davis, M. M., Shaw, A. S., Allen, P. M., Dustin, M. L. (2001) The immunological synapse. Annu. Rev. Immunol. 19, 375-396.
2. Lanzavecchia, A., Sallusto, F. (2001) Antigen decoding by T lymphocytes: from synapses to fate determination. Nat. Immunol. 2, 487-492.
3. Grakoui, A., Bromley, S. K., Sumen, C., Davis, M. M., Shaw, A. S., Allen, P. M., Dustin, M. L. (1999) The immunological synapse: a molecular machine controlling T cell activation. Science 285, 221-227.
4. Alexander-Miller, M. A., Leggatt, G. R., Berzofsky, J. A. (1996) Selective expansion of high- or low-avidity cytotoxic T lymphocytes and efficacy for adoptive immunotherapy. Proc. Natl. Acad. Sci. USA 93, 4102-4107.
5. Dutoit, V., Rubio-Godoy, V., Doucey, M. A., Batard, P., Lienard, D., Rimoldi, D., Speiser, D., Guillaume, P., Cerottini, J. C., Romero, P., Valmori, D. (2002) Functional avidity of tumor antigen-specific CTL recognition directly correlates with die stability of MHC/peptide multimer binding to TCR. J. Immunol. 168, 1167-1171.
6. Zeh III, H. J., Perry-Lalley, D., Dudley, M. E., Rosenberg, S. A., Yang, J. C. (1999) High avidity CTLs for two self-antigens demonstrate superior in vitro and in vivo antitumor efficacy. J. Immunol. 162, 989-994.
7. Gallimore, A., Dumrese, T., Hengartner, H., Zinkernagel, R. M., Rammensee, H. G. (1998) Protective immunity does not correlate with the hierarchy of virus-specific cytoloxic T cell responses to naturally processed peptides. J. Exp. Med. 187, 1647-1657.
8. Alexander-Miller, M. A., Leggatt, G. R., Sarin, A., Berzofsky, J. A. (1996) Role of antigen, CD8, and cytotoxic T lymphocyte (CTL) avidity in high dose antigen induction of apoptosis of effector CTL. J. Exp. Med. 184, 485-492.
9. Derby, M., Alexander-Miller, M., Tse, R., Berzofsky, J. (2001) High-avidity CTL exploit two complementary mechanisms to provide better protection against viral infection than low-avidity CTL. J. Immunol. 166, 1690-1697.
10. Morgan, D. J., Kreuwel, H. T., Fleck, S., Levitsky, H. I., Pardoll, D. M., Sherman, L. A. (1998) Activation of low avidity CTL specific for a self epilope results in tumor rejection but not autoimmunity. J. Immunol. 160, 643-651.
11. Sedlik, C., Dadaglio, G., Saron, M. F., Deriaud. E., Hojas, M., Casal, S. I., Leclerc, C. (2000) In vivo induction of a high-avidity, high-frequency cytotoxic T-lymphocyte response is associated with antiviral protective immunity. J. Virol 74, 5769-5775.
12. Yee, C., Savage, P. A., Lee, P. P., Davis, M. M., Greenberg, P. D. (1999) Isolation of high avidity melanoma-reactive CTL from heterogeneous populations using peptide-MHC tetramers. J. Immunol. 162, 2227-2234.
13. Busch, D. H., Pamer, E. C. (1999) T cell affinity maturation by selective expansion during infection. J. Exp. Med. 189, 701-710.
14. Slifka, M. K., Whitton, J. L. (2001) Functional avidity maturation of CD8(+) T cells without selection of higher affinity TCR. Nat. Immunol. 2, 711-717.
15. Amrani, A., Verdaguer, J., Serra, P., Tafuro, S., Tan, R., Santamaria, P. (2000) Progression of autoimmune diabetes driven by avidity maturation of a T-cell population. Nature 406, 739-742.
16. Alexander-Miller, M. A. (2000) Differential expansion and survival of high and low avidity cytotoxic T cell populations during the immune response to a viral infection. Cell. Immunol. 201, 58-62.
17. Fernando, G. J., Tindle, R. W., Frazer, I. H. (1995) T-helper epitopes of the E7 transforming protein of cervical cancer associated human papillomavirus type 18 (HPV18). Virus Res. 36, 1-13.
18. Fox, C. J., Danska, J. S. (2003) Molecular analysis of mouse T cell receptor expression using PCr. In Current Protocols in Immunology (Colligan, J. E., Druisbeek, A. M., Margulies, D. H., Shevach. E. M., Strober, W., eds) John Wiley & Sons, New York. 10.27.1-10.27.5.
19. Leggatt, G. R., Hosmalin, A., Pendleton, C. D., Kumar, A., Hoffman, S., Berzofsky, J. A. (1998) The importance of pairwise interactions between peptide residues in the delineation of TCR specificity. J. Immunol. 161, 4728-4735.
20. Gao, F. G., Khammanivong, V., Liu, W. J., Leggatt, G. R., Frazer, I. H., Fernando, G. J. (2002) Antigen-specific CD4+ T-cell help is required to activate a memory CD8+ T cell to a fully functional tumor killer cell. Cancer Res. 62, 6438-6441.
21. Alexander, M. A., Damico, C. A., Wieties, K. M., Hansen, T. H., Connolly, J. M. (1991) Correlation between CD8 dependency and determinant density using peptide-induced, Ld-restricted cytotoxic T lymphocytes. J. Exp. Med. 173, 849-858.
22. Lawson, T. M., Man, S., Williams, S., Boon, A. C., Zambon, M., Borysiewicz, L. K. (2001) Influenza A antigen exposure selects dominant Vβ17+ TCR in human CD8+ cytotoxic T cell responses. Int. Immunol. 13, 1373-1381.
23. Kalams, S. A., Johnson, R. P., Trocha, A. K., Dynan, M. J., Ngo, H. S., D'Aquila, R. T., Kurnick, J. T., Walker, B. D. (1994) Longitudinal analysis of T cell receptor (TCH) gene usage by human immunodeficiency virus I envelope-specific cytotoxic T lymphocyte clones reveals a limited TCR repertoire. J. Exp. Med. 179, 1261-1271.
24. Vierboom, M. P., Feltkamp, M. C., Neisig, A., Drijfhout, J. W., ter Sehegget, J., Neefjes, J. J., Melief, C. J., Kast, W. M. (1998) Peptide vaccination with an anchor-replaced CTL epitope protects against human papillomavirus type 16-induced tumors expressing the wild- type epitope. J. Immunother. 21, 399-408.
25. Critchfield, J. M., Racke, M. K., Zuniga-Pflucker, J. C., Canuella, B., Raine, C. S., Goverman, J., Lenardo, M. J. (1994) T cell deletion in high antigen dose therapy of autoimmune encephalomyelitis. Science 263, 1139-1143.
26. Gray, P. M., Parks, G. D., Alexander-Miller, M. A. (2001) A novel CD8-independent high-avidity cytotoxic T-lymphocyte response directed against an epitope in the phosphoprotein of the paramyxovirus simian virus 5. J. Virol. 75, 10065-10072.
27. Abe, R., Vacehio, M. S., Fox, R., Modes, R. J. (1988) Preferential expression of the T-cell receptor V β 3 gene by Mlsc reactive T cells. Nature 335, 827-830.
28. Marrack, P., Kushnir, E., Kappler, J. (1991) A maternally inherited superantigen encoded by a mammary tumour virus. Nature 349, 524-526.
29. de Visser, K. E., Cordaro, T. A., Kessels, H. W., Tirion, F. H., Schimiacher, T. N., Kruisbeek, A. M. (2001) Low-avidity self-specific T cells display a pronounced expansion defect that can be overcome by altered peptide ligands. J. Immunol. 167, 3818-3828.
30. Anderton, S. M., Radu, C. G., Lowrey, P. A., Ward, E. S., Wraith, D. C. (2001) Negative selection during the peripheral immune response to antigen. J. Exp. Med. 193, 1-11.
31. Sharma, A. K., Kuhns, J. J., Van, S., Friedline, R. H., Long, B., Tisch, R., Collins, E. J. (2001) Class I major histocompatibility complex anchor substitutions alter the conformation of T cell receptor contacts. J. Biol. Chem. 276, 21443-21449.