Incomplete CD8+ T lymphocyte differentiation as a mechanism for subdominant cytotoxic T lymphocyte responses to a viral antigen

Journal of Experimental Medicine

Volumn 191, Issue 10, 2000, Pages 1687-1698

  Spencer, Juliet V ^a,b   Braciale, Thomas J ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

^b Box 801386 ^*  (United States)

Author keywords

Anergy; CD8+ T cell; Immunodominance; MHC class I tetramer; Self peptide

Indexed keywords

MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; VIRUS ANTIGEN;

ANTIGEN RECOGNITION; ANTIGEN SPECIFICITY; ARTICLE; CELL CULTURE; CELLULAR IMMUNITY; CYTOTOXIC LYMPHOCYTE; FEMALE; IMMUNE RESPONSE; IMMUNOSTIMULATION; INFLUENZA VIRUS; LYMPHOCYTE DIFFERENTIATION; MASTOCYTOMA; MOUSE; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; ANTIGENS, VIRAL; CD8-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; CELL LINE; CLONAL ANERGY; CYTOTOXICITY, IMMUNOLOGIC; EPITOPES; FEMALE; H-2 ANTIGENS; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; IMMUNODOMINANT EPITOPES; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED BALB C; PROTEIN STRUCTURE, QUATERNARY; T-LYMPHOCYTES, CYTOTOXIC;

EID: 0034657243     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.191.10.1687     Document Type: Article

References (46)

1. Doherty, P.C., W. Allan, M. Eichelberger, and S.R. Carding. 1992. Roles of alpha beta and gamma delta T cell subsets in viral immunity. Annu. Rev. Immunol. 10:123-151.
2. Askonas, B.A., P.M. Taylor, and F. Esquivel. 1988. Cytotoxic T cells in influenza infection. Ann. NY Acad. Sci. 532: 230-237.
3. Bender, B.S., T. Crighan, L. Zhang, and P.A. Small, Jr. 1992. Transgenic mice lacking class I major histocompatibility complex-restricted T cells have delayed clearance and increased mortality after influenza virus challenge. J. Exp. Med. 175:1143-1145.
4. Lukacher, A., V.L. Braciale, and T.J. Braciale. 1984. In vivo effector function of influenza virus-specific cytotoxic T lymphocyte clones is highly specific. J. Exp. Med. 160:814-826.
5. Jamieson, B.D., L.D. Butler, and R. Ahmed. 1987. Effective clearance of a persistent viral infection requires cooperation between virus-specific Lyt2+ T cells and nonspecific bone-marrow derived cells. J. Virol. 61:3930-3937.
6. Byrne, J.A., and M.B. Oldstone. 1984. Biology of cloned cytotoxic T lymphocytes specific for lymphocytic choriomeningitis virus: clearance of virus in vivo. J. Virol. 51:682-686.
7. Lehmann-Grube, F., D. Moskophidis, and J. Lohler. 1988. Recovery from acute virus infection. Role of cytotoxic T lymphocytes in the elimination of lymphocytic choriomeningitis virus from spleens of mice. Ann. NY Acad. Sci. 532:238-256.
8. Zinkernagel, R.M., and P.C. Doherty. 1974. Restriction of in vitro T cell-mediated cytotoxicity in lymphocytic choriomeningitis within a syngeneic or a semiallogeneic system. Nature. 248:701-702.
9. Townsend, A.R.M., A.J. McMichael, N.P. Carter, J.A. Huddlestone, and G.G. Brownlee. 1984. Cytotoxic T cell recognition of the influenza nucleoprotein and hemagglutinin expressed in transfected mouse L cells. Cell. 39:13-25.
10. Townsend, A., and H. Bodmer. 1989. Antigen recognition by class I-restricted cytotoxic T lymphocytes. Annu. Rev. Immunol. 7:601-624.
11. Sercacz, E.E., P.V. Lehman, A. Ametani, G. Benichou, A. Miller, and K. Moudgil. 1993. Dominance and crypticity of T cell antigenic determinants. Annu. Rev. Immunol. 11:729-766.
12. Yewdell, J.W., and J.R. Bennink. 1999. Immunodominance in major histocompatibility complex class 1-resticted T lymphocyte responses. Annu. Rev. Immunol. 17:51-88.
13. McMichael, A. 1994. Cytotoxic T lymphocytes specific for influenza virus. Curr. Top. Microbiol. Immunol. 189:75-91.
14. Braciale, T.J., M.T. Sweetser, L.A. Morrison, D.J. Kittleson, and V.L. Braciale. 1989. Class I major histocompatibility complex-restricted cytolytic T lymphocytes recognize a limited number of sites on the influenza hemagglutinin. Proc. Natl. Acad. Sci. USA. 86:277-281.
15. Sweetser, M.T., V.L. Braciale, and T.J. Braciale. 1989. Class I major histocompatibility complex-restricted T lymphocyte recognition of the influenza hemagglutinin. J. Exp. Med. 179: 1357-1368.
16. Braciale, T.J., V.L. Braciale, T.J. Henkel, J. Sambrook, and M.-J. Gething. 1984. Cytotoxic T lymphocyte recognition of the influenza hemagglutinin gene product expressed by DNA-mediated gene transfer. J. Exp. Med. 159:341-354.
17. Cao, W., B.A. Myers-Powell, and T.J. Braciale. 1996. The weak CD8+ T cell response to an influenza hemagglutinin epitope reflects limited T cell availability. J. Immunol. 157: 505-511.
18. Yang, B., and T.J. Braciale. 1995. Characteristics of ATP-dependent peptide transport in isolated microsomes. J. Immunol. 155:3889-3896.
19. + T cells by a self-derived peptide. Nature. 378:295-298.
20. Altman, J.D., P.A.H. Moss, P.J.R. Goulder, D.H. Barouch, M.G. McHeyzer-Williams, J.I. Bell, A.J. McMichael, and M.M. Davis. 1996. Phenotypic analysis of antigen-specific T lymphocytes. Science. 274:94-96.
21. Kuroda, M.J., J.E. Schmitz, D.H. Barouch, A. Craiu, T.M. Allen, A. Sette, D.I. Watkins, M.A. Forman, and N.L. Letvin. 1998. Analysis of Gag-specific cytotoxic T lymphocytes in simian immunodeficiency virus-infected rhesus monkeys by cell staining with a tetrameric major histocompatibility complex class I-peptide complex. J. Exp. Med. 187: 1373-1381.
22. + T cells during the primary immune response to Epstein-Barr virus in vivo. J. Exp. Med. 187:1395-1402.
23. Gallimore, A., A. Glithero, A. Godkin, A.C. Tissot, A. Pluckthun, T. Elliott, H. Hengartner, and R. Zinkernagel. 1998. Induction and exhaustion of lymphocytic choriomeningitis virus-specific cytotoxic T lymphocytes visualized using soluble tetrameric major histocompatibility complex class I-peptide complexes. J. Exp. Med. 187:1383-1393.
24. Flynn, K.J., G.T. Belz, J.D. Altman, R. Ahmed, D.L. Woodland, and P.C. Doherty. 1998. Virus-specific CD8+ T cells in primary and secondary influenza pneumonia. Immunity. 8:683-691.
25. Murali-Krishna, K., J.D. Altman, M. Suresh, D.J.D. Sourdive, A.J. Zajac, J.D. Miller, J. Slansky, and R. Ahmed. 1998. Counting antigen specific CD8 T cells: a reevaluation of bystander activation during viral infection. Immunity. 8:177-187.
26. Braciale, T.J. 1977. Immunological recognition of influenza virus-infected cells. II. Expression of influenza A matrix protein on the infected cell surface and its role in recognition by cross-reactive cytotoxic T cells. J. Exp. Med. 146:673-689.
27. Mackett, M., G.L. Smith, and B. Moss. 1984. General method for production and selection of infectious vaccinia virus recombinants expressing foreign genes. J. Virol. 49:857-864.
28. Morrison, L.A., A.E. Lukacher, V.L. Braciale, D.P. Fan, and T.J. Braciale. 1986. Differences in antigen presentation to MHC class I- and class II-restricted influenza virus-specific cytolytic T lymphocyte clones. J. Exp. Med. 163:903-921.
29. Busch, D.H., I.M. Pilip, S. Vijh, and E.G. Pamer. 1998. Coordinate regulation of complex T cell populations responding to bacterial infection. Immunity. 8:353-862.
30. Lyons, A.B., and C.R. Parish. 1994. Determination of lymphocyte division by flow cytometry. J. Immunol. Methods. 171:131-137.
31. Hahn, Y.S., B. Yang, and T.J. Braciale. 1996. Regulation of antigen processing and presentation to class I MHC restricted CD8+ T lymphocytes. Immunol. Rev. 151:31-49.
32. Weidt, G., O. Utermohlen, J. Heukeshoven, F. Lehmann-Grubbe, and W. Deppert. 1998. Relationship among immunodominance of single CD8+ T cell epitopes, virus load, and kinetics of primary antiviral CTL response. J. Immunol. 160: 2923-2931.
33. Wettstein, P.J. 1986. Immunodominance in the T-cell response to multiple non-H-2 histocompatibility antigens. II. Observation of a hierarchy among dominant antigens. Immunogenetics. 24:24-31.
34. Valitutti, S., S. Muller, M. Dessing, and A. Lanzavecchia. 1996. Different responses are elicited in cytotoxic T lymphocytes by different levels of T cell receptor occupancy. J. Exp. Med. 183:1917-1921.
35. Gervois, N., Y. Guilloux, E. Diez, and F. Jotereau. 1996. Suboptimal activation of melanoma infiltrating lymphocytes (TIL) due to low avidity of TCR/MHC-tumor peptide interactions. J. Exp. Med. 183:2403-2407.
36. Hollsberg, P., W.E.J. Weber, F. Dangond, V. Batra, A. Sette, and D. Hafler. 1995. Differential activation of proliferation and cytotoxicity in human T-cell lymphotropic virus type I Tax specific-CD8 T cells by an altered peptide ligand. Proc. Natl. Acad. Sci. USA. 92:4036-4040.
37. Arsov, I., and S. Vukmanovic. 1997. Altered effector responses of H-Y transgenic CD8+ cells. Int. Immunol. 9:1423-1430.
38. Cao, W., and T.J. Braciale. 1996. Partial activation of foreign antigen specific T lymphocytes by a self peptide: possible roles of altered peptide ligands in regulating T lymphocyte mediated immune responses. J. Mol. Med. 74:573-582.
39. Evavold, B.D., L.J. Sloan, and P.M. Allen. 1993. Tickling the TCR: selective T cell functions stimulated by altered peptide ligands. Immunol. Today. 14:602-609.
40. + T cells. J. Exp. Med. 185:641-652.
41. Itoh, Y., B. Hemmer, R. Martin, and R.N. Germain. 1999. Serial TCR engagement and down-modulation by peptide: MHC molecule ligands: relationship to the quality of individual TCR signaling events. J. Immunol. 162:2073-2080.
42. Busch, D.H., and E.G. Pamer. 1999. T cell affinity maturation by selective expansion during infection. J. Exp. Med. 189:701-710.
43. Viola, A., S. Schroeder, Y. Sakakibara, and A. Lanzavecchia. 1999. T lymphocyte costimulation mediated by reorganization of membrane microdomains. Science. 283:680-682.
44. Grakoui, A., S.K. Bromley, C. Sumen, M.M. Davis, A.S. Shaw, P.M. Allen, and M.L. Dustin. 1999. The immunological synapse: a molecular machine controlling T cell activation. Science. 285:221-227.
45. Lukacher, A.E., J.M. Moser, A. Hadley, and J.D. Altman. 1999. Visualization of polyomavirus-specific CD8+ T cells in vivo during infection and tumor rejection. J. Immunol. 163:3369-3378.
46. Busch, D.H., and E.G. Pamer. 1998. MHC class I/peptide stability: implications for immunodominance, in vitro proliferation, and diversity of responding CTL. J. Immunol. 160: 4441-4448.