CD8+ T cell immunodominance shifts during the early stages of acute LCMV infection independently from functional avidity maturation

Virology

Volumn 390, Issue 2, 2009, Pages 197-204

  Raué, Hans Peter ^a   Slifka, Mark K ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

CD8; Functional avidity; Immunodominance; LCMV; T cells

Indexed keywords

ANIMAL CELL; ARTICLE; BINDING AFFINITY; C57BL 6 MOUSE; CD8+ T LYMPHOCYTE; CELL MATURATION; CONTROLLED STUDY; EX VIVO STUDY; IMMUNE RESPONSE; LYMPHOCYTE COUNT; LYMPHOCYTE SUBPOPULATION; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MOUSE; NONHUMAN; PRIORITY JOURNAL; RNA VIRUS INFECTION; SPLEEN;

ANIMALS; ARENAVIRIDAE INFECTIONS; CD8-POSITIVE T-LYMPHOCYTES; EPITOPES, T-LYMPHOCYTE; INTERFERON-GAMMA; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MICE; MICE, INBRED C57BL; SPLEEN;

LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MUS;

EID: 67649861899     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2009.05.021     Document Type: Article

References (66)

1. Alexander-Miller M.A. High-avidity CD8+ T cells: optimal soldiers in the war against viruses and tumors. Immunol. Res. 31 1 (2005) 13-24
2. Alexander-Miller M.A., Leggatt G.R., Sarin A., and Berzofsky J.A. Role of antigen, CD8, and cytotoxic T lymphocyte (CTL) avidity in high dose antigen induction of apoptosis of effector CTL. J. Exp. Med. 184 2 (1996) 485-492
3. Arnold L.D., Calderwood D.J., Dixon R.W., Johnston D.N., Kamens J.S., Munschauer R., Rafferty P., and Ratnofsky S.E. Pyrrolo[2,3-d]pyrimidines containing an extended 5-substituent as potent and selective inhibitors of lck I. Bioorg. Med. Chem. Lett. 10 19 (2000) 2167-2170
4. Bachmann M.F., Gallimore A., Linkert S., Cerundolo V., Lanzavecchia A., Kopf M., and Viola A. Developmental regulation of Lck targeting to the CD8 coreceptor controls signaling in naive and memory T cells. J. Exp. Med. 189 10 (1999) 1521-1530
5. Barber E.K., Dasgupta J.D., Schlossman S.F., Trevillyan J.M., and Rudd C.E. The CD4 and CD8 antigens are coupled to a protein-tyrosine kinase (p56lck) that phosphorylates the CD3 complex. Proc. Natl. Acad. Sci. U.S.A. 86 9 (1989) 3277-3281
6. Belz G.T., Xie W.D., Altman J.D., and Doherty P.C. A previously unrecognized H-2D(b)-restricted peptide prominent in the primary influenza A virus-specific CD8(+) T-cell response is much less apparent following secondary challenge. J. Virol. 74 8 (2000) 3486-3493
7. Belz G.T., Xie W., and Doherty P.C. Diversity of epitope and cytokine profiles for primary and secondary influenza a virus-specific cd8(+) t cell responses. J. Immunol. 166 7 (2001) 4627-4633
8. Bergmann C.C., Altman J.D., Hinton D., and Stohlman S.A. Inverted immunodominance and impaired cytolytic function of CD8+ T cells during viral persistence in the central nervous system. J. Immunol. 163 6 (1999) 3379-3387
9. Brehm M.A., Pinto A.K., Daniels K.A., Schneck J.P., Welsh R.M., and Selin L.K. T cell immunodominance and maintenance of memory regulated by unexpectedly cross-reactive pathogens. Nat. Immunol. 3 7 (2002) 627-634
10. Buchmeier M.J., and Zajac A.J. Lymphocytic Choriomeningitis Virus. In: Ahmed R., and Chen I. (Eds). Persistent Viral Infections (1999), John Wiley & Sons Ltd. 575-605
11. Burchat A.F., Calderwood D.J., Hirst G.C., Holman N.J., Johnston D.N., Munschauer R., Rafferty P., and Tometzki G.B. Pyrrolo[2,3-d]pyrimidines containing an extended 5-substituent as potent and selective inhibitors of lck II. Bioorg. Med. Chem. Lett. 10 19 (2000) 2171-2174
12. Busch D.H., and Pamer E.G. T cell affinity maturation by selective expansion during infection. J. Exp. Med. 189 4 (1999) 701-710
13. Butz E.A., and Bevan M.J. Massive expansion of antigen-specific CD8+ T cells during an acute virus infection. Immunity 8 (1998) 167-175
14. Calderwood D.J., Johnston D.N., Munschauer R., and Rafferty P. Pyrrolo[2,3-d]pyrimidines containing diverse N-7 substituents as potent inhibitors of Lck. Bioorg. Med. Chem. Lett. 12 12 (2002) 1683-1686
15. Chen W., Anton L.C., Bennink J.R., and Yewdell J.W. Dissecting the multifactorial causes of immunodominance in class I-restricted T cell responses to viruses. Immunity 12 1 (2000) 83-93
16. Chen W., and McCluskey J. Immunodominance and immunodomination: critical factors in developing effective CD8+ T-cell-based cancer vaccines. Adv. Cancer Res. 95 (2006) 203-247
17. Choi E.Y., Christianson G.J., Yoshimura Y., Sproule T.J., Jung N., Joyce S., and Roopenian D.C. Immunodominance of H60 is caused by an abnormally high precursor T cell pool directed against its unique minor histocompatibility antigen peptide. Immunity 17 5 (2002) 593-603
18. Crowe S.R., Turner S.J., Miller S.C., Roberts A.D., Rappolo R.A., Doherty P.C., Ely K.H., and Woodland D.L. Differential antigen presentation regulates the changing patterns of CD8+ T cell immunodominance in primary and secondary influenza virus infections. J. Exp. Med. 198 3 (2003) 399-410
19. Daly K., Nguyen P., Woodland D.L., and Blackman M.A. Immunodominance of major histocompatibility complex class I-restricted influenza virus epitopes can be influenced by the T-cell receptor repertoire. J. Virol. 69 12 (1995) 7416-7422
20. Edwards B.H., Bansal A., Sabbaj S., Bakari J., Mulligan M.J., and Goepfert P.A. Magnitude of functional CD8+ T-cell responses to the gag protein of human immunodeficiency virus type 1 correlates inversely with viral load in plasma. J. Virol. 76 5 (2002) 2298-2305
21. Fuller M.J., and Zajac A.J. Ablation of CD8 and CD4 T cell responses by high viral loads. J. Immunol. 170 1 (2003) 477-486
22. Fuller-Pace F.V., and Southern P.J. Temporal analysis of transcription and replication during acute infection with lymphocytic choriomeningitis virus. Virology 162 1 (1988) 260-263
23. Grayson J.M., Harrington L.E., Lanier J.G., Wherry E.J., and Ahmed R. Differential sensitivity of naive and memory CD8(+) T cells to apoptosis in vivo. J. Immunol. 169 7 (2002) 3760-3770
24. Hanke J.H., Gardner J.P., Dow R.L., Changelian P.S., Brissette W.H., Weringer E.J., Pollok B.A., and Connelly P.A. Discovery of a novel, potent, and Src family-selective tyrosine kinase inhibitor. Study of Lck- and FynT-dependent T cell activation. J. Biol. Chem. 271 2 (1996) 695-701
25. Homann D., Teyton L., and Oldstone M.B. Differential regulation of antiviral T-cell immunity results in stable CD8+ but declining CD4+ T-cell memory. Nat. Med. 7 8 (2001) 913-919
26. Karni R., Mizrachi S., Reiss-Sklan E., Gazit A., Livnah O., and Levitzki A. The pp60c-Src inhibitor PP1 is non-competitive against ATP. FEBS Lett. 537 1-3 (2003) 47-52
27. Kotturi M.F., Peters B., Buendia-Laysa Jr. F., Sidney J., Oseroff C., Botten J., Grey H., Buchmeier M.J., and Sette A. The CD8+ T-cell response to lymphocytic choriomeningitis virus involves the L antigen: uncovering new tricks for an old virus. J. Virol. 81 10 (2007) 4928-4940
28. Kroger C.J., and Alexander-Miller M.A. Cutting edge: CD8+ T cell clones possess the potential to differentiate into both high- and low-avidity effector cells. J. Immunol. 179 2 (2007) 748-751
29. Kroger C.J., and Alexander-Miller M.A. Dose-dependent modulation of CD8 and functional avidity as a result of peptide encounter. Immunology 122 2 (2007) 167-178
30. La Gruta N.L., Doherty P.C., and Turner S.J. A correlation between function and selected measures of T cell avidity in influenza virus-specific CD8+ T cell responses. Eur. J. Immunol. 36 11 (2006) 2951-2959
31. La Gruta N.L., Kedzierska K., Pang K., Webby R., Davenport M., Chen W., Turner S.J., and Doherty P.C. A virus-specific CD8+ T cell immunodominance hierarchy determined by antigen dose and precursor frequencies. Proc. Natl. Acad. Sci. U.S.A. 103 4 (2006) 994-999
32. Latour S., and Veillette A. Proximal protein tyrosine kinases in immunoreceptor signaling. Curr. Opin. Immunol. 13 3 (2001) 299-306
33. Liu F., Whitton J.L., and Slifka M.K. The rapidity with which virus-specific CD8+ T cells initiate IFN-gamma synthesis increases markedly over the course of infection and correlates with immunodominance. J. Immunol. 173 1 (2004) 456-462
34. McHeyzer-Williams L.J., Panus J.F., Mikszta J.A., and McHeyzer-Williams M.G. Evolution of antigen-specific T cell receptors in vivo: preimmune and antigen-driven selection of preferred complementarity-determining region 3 (CDR3) motifs. J. Exp. Med. 189 11 (1999) 1823-1838
35. Munks M.W., Cho K.S., Pinto A.K., Sierro S., Klenerman P., and Hill A.B. Four distinct patterns of memory CD8 T cell responses to chronic murine cytomegalovirus infection. J. Immunol. 177 1 (2006) 450-458
36. Murali-Krishna K., Altman J.D., Suresh M., Sourdive D.J.D., Zajac A.J., Miller J.D., Slansky J., and Ahmed R. Counting antigen-specific CD8 T cells: a reevaluation of bystander activation during viral infection. Immunity 8 (1998) 177-187
37. Obar J.J., Khanna K.M., and Lefrancois L. Endogenous naive CD8+ T cell precursor frequency regulates primary and memory responses to infection. Immunity 28 6 (2008) 859-869
38. In: Oldstone M.B.A. (Ed). Arenaviruses II. The molecular pathogenesis of Arenavirus infections. Current Topics in Microbiology and Immunology Vol. 263 (2002), Springer, Berlin
39. Ou R., Zhou S., Huang L., and Moskophidis D. Critical role for alpha/beta and gamma interferons in persistence of lymphocytic choriomeningitis virus by clonal exhaustion of cytotoxic T cells. J. Virol. 75 18 (2001) 8407-8423
40. Palacios E.H., and Weiss A. Function of the Src-family kinases, Lck and Fyn, in T-cell development and activation. Oncogene 23 48 (2004) 7990-8000
41. Phillips R.E., Rowland-Jones S., Nixon D.F., Gotch F.M., Edwards J.P., Ogunlesi A.O., Elvin J.G., Rothbard J.A., Bangham C.R., Rizza C.R., et al. Human immunodeficiency virus genetic variation that can escape cytotoxic T cell recognition. Nature 354 6353 (1991) 453-459
42. Pircher H., Moskophidis D., Rohrer U., Burki K., Hengartner H., and Zinkernagel R.M. Viral escape by selection of cytotoxic T cell-resistant virus variants in vivo. Nature 346 6285 (1990) 629-633
43. Probst H.C., Tschannen K., Gallimore A., Martinic M., Basler M., Dumrese T., Jones E., and van den Broek M.F. Immunodominance of an antiviral cytotoxic T cell response is shaped by the kinetics of viral protein expression. J. Immunol. 171 10 (2003) 5415-5422
44. Purbhoo M.A., Boulter J.M., Price D.A., Vuidepot A.L., Hourigan C.S., Dunbar P.R., Olson K., Dawson S.J., Phillips R.E., Jakobsen B.K., Bell J.I., and Sewell A.K. The human CD8 coreceptor effects cytotoxic T cell activation and antigen sensitivity primarily by mediating complete phosphorylation of the T cell receptor zeta chain. J. Biol. Chem. 276 35 (2001) 32786-32792
45. Raue H.P., and Slifka M.K. Pivotal Advance: CTLA-4+ T cells exhibit normal antiviral functions during acute viral infection. J. Leukoc. Biol. 81 5 (2007) 1165-1175
46. Rodriguez F., Harkins S., Slifka M.K., and Whitton J.L. Immunodominance in virus-induced CD8(+) T-cell responses is dramatically modified by DNA immunization and is regulated by gamma interferon. J. Virol. 76 9 (2002) 4251-4259
47. Rudd C.E., Trevillyan J.M., Dasgupta J.D., Wong L.L., and Schlossman S.F. The CD4 receptor is complexed in detergent lysates to a protein-tyrosine kinase (pp58) from human T lymphocytes. Proc. Natl. Acad. Sci. U.S.A. 85 14 (1988) 5190-5194
48. Rudd C.E., Barber E.K., Burgess K.E., Hahn J.Y., Odysseos A.D., Sy M.S., and Schlossman S.F. Molecular analysis of the interaction of p56lck with the CD4 and CD8 antigens. Adv. Exp. Med. Biol. 292 (1991) 85-96
49. Salmond R.J., Filby A., Qureshi I., Caserta S., and Zamoyska R. T-cell receptor proximal signaling via the Src-family kinases, Lck and Fyn, influences T-cell activation, differentiation, and tolerance. Immunol. Rev. 228 1 (2009) 9-22
50. Savage P.A., Boniface J.J., and Davis M.M. A kinetic basis for T cell receptor repertoire selection during an immune response. Immunity 10 4 (1999) 485-492
51. Slifka M.K., and Whitton J.L. Functional avidity maturation of CD8+ T cells without selection of higher affinity TCR. Nat. Immunol. 2 8 (2001) 711-717
52. Tebo A.E., Fuller M.J., Gaddis D.E., Kojima K., Rehani K., and Zajac A.J. Rapid recruitment of virus-specific CD8 T cells restructures immunodominance during protective secondary responses. J. Virol. 79 20 (2005) 12703-12713
53. Tewari K., Walent J., Svaren J., Zamoyska R., and Suresh M. Differential requirement for Lck during primary and memory CD8+ T cell responses. Proc. Natl. Acad. Sci. U.S.A. 103 44 (2006) 16388-16393
54. van der Most R.G., Sette A., Oseroff C., Alexander J., Murali-Krishna K., Lau L.L., Southwood S., Sidney J., Chesnut R.W., Matloubian M., and Ahmed R. Analysis of cytotoxic T cell responses to dominant and subdominant epitopes during acute and chronic lymphocytic choriomeningitis virus infection. J. Immunol. 157 12 (1996) 5543-5554
55. van der Most R.G., Concepcion R.J., Oseroff C., Alexander J., Southwood S., Sidney J., Chesnut R.W., Ahmed R., and Sette A. Uncovering subdominant cytotoxic T-lymphocyte responses in lymphocytic choriomeningitis virus-infected BALB/c mice. J. Virol. 71 7 (1997) 5110-5114
56. van der Most R.G., Murali-Krishna K., Whitton J.L., Oseroff C., Alexander J., Southwood S., Sidney J., Chesnut R.W., Sette A., and Ahmed R. Identification of Db- and Kb-restricted subdominant cytotoxic T-cell responses in lymphocytic choriomeningitis virus-infected mice. Virology 240 1 (1998) 158-167
57. van der Most R.G., Murali-Krishna K., Lanier J.G., Wherry E.J., Puglielli M.T., Blattman J.N., Sette A., and Ahmed R. Changing immunodominance patterns in antiviral CD8 T-cell responses after loss of epitope presentation or chronic antigenic stimulation. Virology 315 1 (2003) 93-102
58. Veillette A., Bookman M.A., Horak E.M., and Bolen J.B. The CD4 and CD8 T cell surface antigens are associated with the internal membrane tyrosine-protein kinase p56lck. Cell 55 2 (1988) 301-308
59. Viola A., Salio M., Tuosto L., Linkert S., Acuto O., and Lanzavecchia A. Quantitative contribution of CD4 and CD8 to T cell antigen receptor serial triggering. J. Exp. Med. 186 10 (1997) 1775-1779
60. Weiss A. T cell antigen receptor signal transduction: a tale of tails and cytoplasmic protein-tyrosine kinases. Cell 73 2 (1993) 209-212
61. Wherry E.J., Blattman J.N., Murali-Krishna K., van der Most R., and Ahmed R. Viral persistence alters CD8 T-cell immunodominance and tissue distribution and results in distinct stages of functional impairment. J. Virol. 77 8 (2003) 4911-4927
62. Woodberry T., Suscovich T.J., Henry L.M., Davis J.K., Frahm N., Walker B.D., Scadden D.T., Wang F., and Brander C. Differential targeting and shifts in the immunodominance of Epstein-Barr virus-specific CD8 and CD4 T cell responses during acute and persistent infection. J. Infect. Dis. 192 9 (2005) 1513-1524
63. Yewdell J.W., and Bennink J.R. Immunodominance in major histocompatibility complex class I-restricted T lymphocyte responses. Annu. Rev. Immunol. 17 (1999) 51-88
64. Zajac A.J., Blattman J.N., Murali-Krishna K., Sourdive D.J., Suresh M., Altman J.D., and Ahmed R. Viral immune evasion due to persistence of activated T cells without effector function. J. Exp. Med. 188 12 (1998) 2205-2213
65. Zamoyska R., Derham P., Gorman S.D., von Hoegen P., Bolen J.B., Veillette A., and Parnes J.R. Inability of CD8 alpha' polypeptides to associate with p56lck correlates with impaired function in vitro and lack of expression in vivo. Nature 342 6247 (1989) 278-281
66. Zehn D., Lee S.Y., and Bevan M.J. Complete but curtailed T-cell response to very low-affinity antigen. Nature 458 7235 (2009) 211-214