The many important facets of T-cell repertoire diversity

Nature Reviews Immunology

Volumn 4, Issue 2, 2004, Pages 123-132

  Nikolich Žugich, Janko ^a   Slifka, Mark K ^a   Messaoudi, Ilhem ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

T LYMPHOCYTE RECEPTOR; T LYMPHOCYTE RECEPTOR ALPHA CHAIN; T LYMPHOCYTE RECEPTOR BETA CHAIN;

BONE MARROW TRANSPLANTATION; CROSS REACTION; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNE RESPONSE; MAJOR HISTOCOMPATIBILITY COMPLEX; PRIORITY JOURNAL; REVIEW; T LYMPHOCYTE;

EID: 1142274484     PISSN: 14741733     EISSN: None     Source Type: Journal    
DOI: 10.1038/nri1292     Document Type: Review

References (98)

1. Burnet, F. M. The cellular basis of Immunology. Jpn. J. Microbiol. 5, 1-10(1961).
2. Weill, J. C. et al. Ig gene hypermutation: a mechanism is due. Adv. Immunol. 80, 183-202 (2002).
3. + T cells against malaria liver stages. J. Exp. Med. 194, 173-180(2001).
4. + T cell responses. J. Immunol. 166, 4627-4633(2001).
5. Iezzi, G., Scheidegger, D. & Lanzavecchia, A. Migration and function of antigen-primed nonpolarized T lymphocytes in vivo. J. Exp. Med. 193, 987-993 (2001).
6. Echchakir, H. et al. Cytotoxic T lymphocytes directed against a tumor-specific mutated antigen display similar HLA tetramer binding but distinct functional avidity and tissue distribution. Proc. Natl Acad. Sci. USA 31, 9358-9363 (2002).
7. Garcia, K. C., Teyton, L. & Wilson, I. A. Structural basis of T cell recognition. Annu. Rev. Immunol. 17, 369-397 (1999).
8. Rudolph, M. G. & Wilson, I. A. The specificity of TCR/pMHC interaction. Curr. Opin. Immunol. 14, 52-65 (2002).
9. Malissen, B. Glimpses at TCR trans-species crossreactivity. Immunity 19, 463-464 (2003).
10. Reiser, J. B. et al. CDR3 loop flexibility contributes to the degeneracy of TCR recognition. Nature Immunol. 4, 241-247 (2003).
11. Buslepp, J., Wang, H., Biddison, W. E., Appella, E. & Collins, E. J. A correlation between TCR Vα docking on MHC and CD8 dependence: implications for T cell selection. Immunity. 19, 595-606 (2003).
12. Tonegawa, S. et al. Somatic reorganization of immunoglobulin genes during lymphocyte differentiation. Cold Spring Harb. Symp. Quant. Biol. 45, 839-858 (1981).
13. Davis, M. M. & Bjorkman, P. J. T-cell antigen receptor genes and T-cell recognition. Nature 334, 395 (1988).
14. Padovan, E. et al. Expression of two TCR α-chains: dual receptor T cells. Science 262, 422 (1993).
15. Heath, W. R. & Miller, J. F. Expression of two α-chains on the surface of T cells in TCR transgenic mice. J. Exp. Med. 178, 1807 (1993).
16. Petrie, H. T. et al. Multiple rearrangements in T cell receptor α-chain genes maximize the production of useful thymocytes. J. Exp. Med. 178, 615-622 (1993).
17. Ignatowicz, L., Kappler, J. & Marrack, P. The repertoire of T cells shaped by a single MHC/peptide ligand. Cell 64, 521-529 (1996).
18. Tourne, S., Naoko, N., Viville, S., Benoist, C. & Mathis, D. The influence of invariant chain on the positive selection of single T cell receptor specificities. Eur. J. Immunol. 25, 1851-1856 (1995).
19. Zerrahn, J., Held, W. & Raulet, D. H. The MHC reactivity of the T cell repertoire prior to positive and negative selection. Cell 88, 627-636 (1997).
20. Bouneaud, C., Kourilsky, P., & Bousso, P. Impact of negative selection of the T cell repertoire reactive to a self-peptide: a large fraction of T cell clones escapes clonal deletion. Immunity 13, 829-840 (2000).
21. + T-cell response to readily eliminated and persistent viruses. Phil. Trans. R. Soc. Lond. B Biol. Sci. 355, 1093-1101 (2000).
22. Arstila, T. P. et al. A direct estimate of the human αβ T cell receptor diversity. Science 286, 958-961 (1999). This paper presents the first reliable experiments that estimate peripheral T-cell receptor (TCR) diversity in humans.
23. Even, J. et al. T cell repertoires in healthy and diseased human tissues analyzed by T cell receptor β-chain CDR3 size determination: evidence for oligoclonal expansions in tumours and inflammatory diseases. Res. Immunol. 146, 65-80 (1995).
24. Pannetier, C., Even, J. & Kourilsky, P. T-cell repertoire diversity and clonal expansions in normal and clinical samples. Immunol. Today 16, 176-181 (1995).
25. Casrouge, A. et al. Size estimates of the αβ TCR repertoire of naive mouse splenocytes. J. Immunol. 164, 5782-5787 (2001). This paper presents the first experimentally sound estimate of peripheral TCR diversity in mice.
26. Bousso, P. et al. Individual variations in the murine T cell response to a specific peptide reflect variability in naive repertoires. Immunity 9, 169-178 (1998). Together with reference 27, this study documents marked variability of the T-cell repertoire in individual animals, and provides rationale to reconcile the numerical figures between theoretical and measured repertoire diversity.
27. Maryanski, J. L. et al. Individuality of Ag-selected and preimmune TCR repertoires. Immunol. Res. 23, 75-84 (2001).
28. Lin, M. Y. & Welsh, R. M. Stability and diversity of T cell receptor repertoire usage during lymphocytic choriomeningitis virus infection of mice. J. Exp. Med. 188, 1993-2005 (1998).
29. Nossal, G. J. V. Negative selection of lymphocytes. Cell 76, 229-240 (1994).
30. Fink, P. J. & Bevan, M. J. Positive selection of thymocytes. Adv. Immunol. 59, 99-133 (1995).
31. Nikolich-Zugich, J. & Bevan, M. J. Role of self-peptides in positively selecting the T-cell repertoire. Nature 344, 65-67 (1990).
32. Messaoudi, I., Guevara Patino, J. A., Dyall, R., LeMaoult, J. & Nikolich-Zugich, J. Direct link between MHC polymorphism, T-cell avidity and diversity in immune defense. Science 298, 1797-1801 (2002). This study provides a rare direct glimpse into the relationship between TCR diversity and pathogen resistance.
33. Dyall, R., Messaoudi, I., Janetzki, S. & Nikolich-Zugich, J. MHC polymorphism can enrich the cell repertoire of the species by shifts in intrathymic selection. J. Immunol. 164, 1695-1698 (2000).
34. Kappler, J. W., Roehm, N. & Marrack, P. T cell tolerance by clonal elimination in the thymus. Cell 49, 273-281 (1987).
35. + T cells during negative selection results in an altered antiviral T cell hierarchy. J. Immunol. 170, 1231-1239 (2003). This work delineates the relationship between immunodominance and tolerance with regard to TCR diversity.
36. Holler, P. D., Chlewicki, L. K. & Kranz, D. M. TCRs with high affinity for foreign pMHC show self-reactivity. Nature Immunol. 4, 55-62 (2003).
37. Sourdive, D. J. D. et al. Conserved T cell receptor repertoire in primary and memory CD8 T cell responses to an acute viral infection. J. Exp. Med. 188, 71-82 (1998).
38. Sim, B. C. Zerva, L., Greene, M. I. & Gascoigne, N. R. Control of MHC restriction by TCR Vα CDR1 and CDR2. Science 273, 963-966 (1996).
39. Turner, S., Cose, S. C. & Carbone, F. R. TCR α-chain usage can determine antigen-selected TCR β-chain repertoire diversity. J. Immunol. 157, 4979-4985 (1996).
40. Wallace, M. E. et al. Junctional biases in the naive TCR repertoire control the CTL response to an immunodominant determinant of HSV-1. Immunity 12, 547-556 (2000).
41. Kjer-Nielsen, L. et al. A structural basis for the selection of dominant αβ-T cell receptors in antiviral immunity. Immunity 18, 53-64 (2003).
42. Blish, C. A. et al. Chronic modulation of the TCR repertoire in the lymphoid periphery. J. Immunol. 162, 3131-3140 (1999).
43. McGargill, M. A., Derbinski, J. M. & Hogquist, K. A. Receptor editing in developing T cells. Naure. Immunol. 1, 336-341 (2000).
44. Buch, T., Rieux-Laucat, F., Forster, I. & Rejewsky, K. Failure of HY-specific thymocytes to escape negative selection by receptor editing. Immunity 16, 707-718 (2002).
45. Schonrich, G. et al. Downregulation of T cell receptors on self-reactive T cells as a novel mechanism for extrathymic tolerance induction. Cell 65, 293-304 (1991).
46. Teh, H.-S., Kishi, H., Scott, B. & von Boehmer, H. Deletion of autospecific T cells in T cell receptor (TCR) transgenic mice spares cells with normal TCR levels and low levels of CD8 molecules. J. Exp. Med. 169, 795-806 (1989).
47. H2 immunity. Immunol. Today 19, 157-163 (1998).
48. Zinkernagal, R. M. Uncertainties - discrepencies in immunology. Immunol. Rev. 185, 103-125 (2002).
49. Mason, D. A very high level of crossreactivity is an essential feature of the T-cell receptor. Immunol. Today 19, 395-404 (1998).
50. Regner, M. Crossreactivity in T-cell antigen recognition. Immunol. Cell Biol. 79, 91-100 (2001).
51. Hiemstra, H. S., van Veelen, P. A. & Schloot, N. C. Definition of natural T cell antigens with mimicry epitopes obtained from dedicated synthetic peptide libraries. J. Immunol. 161, 4078-4082 (1998).
52. Selin, L. K., Nahill, S. R. & Welsh, R. M. Crossreactivities in memory cytotoxic T lymphocyte recognition of heterologous viruses. J. Exp. Med. 179, 1933 (1994).
53. + effector cell differentiation in vivo. Proc. Natl Acad. Sci. USA 96, 13932-13937 (1999).
54. Gudmundsdottir, H., Wells, A. D. & Turka, L. A. Dynamics and requirements of T cell clonal expansion in vivo at the single-cell level: effector function is linked to proliferative capacity. J. Immunol. 162, 5212-5223 (1999).
55. Henke, T. & Raulet D. Cumulative inhibition of NK cells and T cells resulting from engagement of multiple inhibitory Ly49 receptors. J. Immunol. 166, 3002-3007 (2001).
56. + T cells can be distinguished by their cytokine profiles and phenotypic markers. J. Immunol. 164, 208-216 (2000).
57. + T cells without selection of higher affinity TCR. Nature Immunol. 2, 711-717 (2001).
58. Manjunath, N. et al. Effector differentiation is not prerequisite for generation of memory cytotoxic T lymphocytes. J. Clin. Invest. 108, 871-878 (2001).
59. Bernaschi, M. & Castiglione, F. Selection of escape mutants from immune recognition during HIV infection. Immunol. Cell Biol. 80, 307-313 (2002).
60. Klenerman, P., Wu, Y. & Phillips, R. HIV: current opinion in escapology. Curr. Opin. Microbiol. 5, 408-413 (2002).
61. Carrington, M. et al. HLA and HIV-1: heterozygote advantage and B*35-Cw*04 disadvantage. Science 283, 1748-1752 (1999).
62. Evans, D. T. et al. Virus-specific cytotoxic T-lymphocyte responses select for amino-acid variation in simian immunodeficiency virus Env and Nef. Nature Med. 5, 1270-1276 (1999).
63. Vogel, T. U. et al. Escape in one of two cytotoxic T-lymphocyte epitopes bound by a high-frequency major histocompatibility complex class I molecule, Mamu-A*02: a paradigm for virus evolution and persistence? J. Virol. 76, 11623-11636 (2002).
64. McMichael, A. T cell responses and viral escape. Cell 93, 673-676 (1998).
65. Gilfillan, S., Dierich, A., Lemeur, M., Benoist, C. & Mathis, D. Mice lacking TdT: mature animals with an immature lymphocyte repertoire. Science 261, 1175-1178 (1993).
66. Cabaniols, J. P., Fazilleau, N., Casrouge, A., Kourilsky, P. & Kanellopoulos, J. Most α/β T cell receptor diversity is due to terminal deoxynucleotidyl transferase. J. Exp. Med. 194, 1385-1390 (2001).
67. Gavin, M. A. & Bevan, M. J. Increased peptide promiscuity provides a rationale for the lack of N regions in the neonatal T cell repertoire. Immunity 3, 793-800 (1995).
68. Kikly, K. & Dennert, G. Evidence for a role for T-cell receptors (TCR) in the effector phase of acute bone marrow graft rejection: TCR Vβ5 transgenic mice lack effector cells able to cause graft rejection. J. Immunol. 149, 3489-3494 (1992).
69. Bousso, P. et al. Diversity, functionality, and stability of the T cell repertoire derived in vivo from a single human T cell precursor. Proc. Natl Acad. Sci. USA 97, 274-278 (2000).
70. Woodland, D., Kotzin, B. L. & Palmer, E. Functional consequences of a T-cell receptor Dβ2 and Jβ2 gene segment deletion. J. Immunol. 144, 379-385 (1990).
71. Nanda, N. K., Apple, R. & Sercarz, E. Limitations in plasticity of the T-cell receptor repertoire. Proc. Natl Acad. Sci. USA 88, 9503-9507 (1991).
72. Cose, S. C., Kelly, J. M. & Carbone, F. R. Characterization of a diverse primary herpes simplex virus type 1 gB-specific cytotoxic T-cell response showing a preferential Vβ bias. J. Virol. 69, 5849-5852 (1995).
73. Wallace, M. E., Keating, R., Heath, W. R. & Carbone, F. R. The cytotoxic T-cell response to herpes simplex virus type 1 infection of C57BL/6 mice is almost entirely directed against a single immunodominant determinant. J. Virol. 73, 7619-7626 (1999).
74. + T cells. J. Virol. 77, 2445-2451 (2003).
75. Jones, C. M., Cose, S. C. & Carbone, F. R. Evidence for cooperation between TCR V region and junctional sequences in determining a dominant cytotoxic T lymphocyte response to herpes simplex virus glycoprotein B. Int. Immunol. 9, 1319-1328 (1997).
76. Turner, S. J. & Carbone, F. R. A dominant Vβ bias in the CTL response after HSV-1 infection is determined by peptide residues predicted to also interact with the TCR β-chain CDR3. Mol. Immunol. 35, 307-316 (1998).
77. + T-cell clones in old mice. Immunol. Rev. 160, 139-144 (1997).
78. + lymphocyte homeostasis during the natural course of HIV-1 infection. J. Clin. Invest. 101, 137-144 (1998).
79. Effros, R. B. & Pawelec, G. Replicative senescence of T cells: does the Hayflick limit lead to immune exhaustion? Immunol. Today 18, 450-454 (1997).
80. Gilfillan, S. et al. Efficient immune responses in mice lacking N-region diversity. Eur. J. Immunol. 25, 3115-3122 (1995).
81. Nanda, N. K., Apple, R. & Sercarz, E. Limitations in plasticity of the T-cell receptor repertoire. Proc. Natl Acad. Sci. USA 88, 9503-9507 (1991).
82. Speiser, D. E., Kyburz, D., Stubi, U., Hengartner, H. & Zinkernagel, R. M. Discrepancy between in vitro measurable and in vivo virus neutralizing cytotoxic T cell reactivities. Low T cell receptor specificity and avidity sufficient for in vitro proliferation or cytotoxicity to peptide-coated target cells but not for in vivo protection. J. Immunol. 149, 972-980 (1992).
83. + T cell-mediated antiviral protection. J. Immunol. 162, 2867-2874 (1999).
84. Moskophidis, D., Lechner, F., Hengartner, H. & Zinkernagel, R. M. MHC class I and non-MHC-linked capacity for generating an anti-viral CTL response determines susceptibility to CTL exhaustion and establishment of virus persistence in mice. J. Immunol. 152, 4976-4983 (1994).
85. Riddell, S. R. et al. Restoration of viral immunity in immunosuppressed humans by the adoptive transfer of T-cell clones. Science 257, 238-241 (1992).
86. Cohn, M. & Langman, R. E. The protection: the unit of humoral immunity selected by evolution. Immunol. Rev. 115, 11-142 (1990).
87. Blattman, J. et al. Estmating the precursor frequency of naive antigen-specific CD8 T cells. J. Exp. Med. 195, 657-664 (2002). Together with references 22 and 88, this paper attempts to estimate the numbers and diversity of naive T cells specific for an epitope.
88. Pewe, L., Heard, S. B., Bergmann, C., Dailey, M. O. & Perlman, S. Selection of CTL escape mutants in mice infected with a neurotropic coronavirus: quantitative estimate of TCR diversity in the infected central nervous system. J. Immunol. 163, 6106-6113 (1999).
89. Berger, D. P., Homann, D. & Oldstone, M. B. A. Defining parameters for successful immunocytotherapy of persistent viral infection. Virol. 266, 257-263 (2000).
90. Dyall, R., Fremont, D. H., Jameson, S. C. & Nikolich-Zugich, J. T cell receptor (TCR) recognition of MHC class I variants: intermolecular second-site reversion of an MHC mutation by substituted peptides provides evidence for peptide/MHC conformational variation. J. Exp. Med. 164, 253-258 (1996).
91. Saito, Y., Peterson, P. A. & Matsumura, M. Quantitation of peptide anchor residue contributions to class I major histocompatibility complex molecule binding. J. Biol. Chem. 266, 21309-21317 (1993).
92. Fremont, D. H., Stura, E. A., Masazumi, M., Peterson, P. A. & Wilson, I. A. Crystal structure of an H-2Kb-ovalbumin peptide complex reveals the interplay of primary and secondary anchor positions in the major histocompatibility complex binding groove. Proc. Natl Acad. Sci. USA 92, 2479-2483 (1995).
93. Huard, R., Dyall, R., & Nikolich-Zugich, J. The role of a T cell receptor-contact residue of a major histocompatibility complex (MHC) encoded class I molecule-restricted peptide in MHC-peptide binding. Int. Immunol. 9, 1701-1708 (1997).
94. Molano, A., Erdjument-Bromage, H., Fremont, D. H., Messaoudi, I. & Nikolich-Zugich, J. Peptide selection by an MHC class I H-2Kb molecule devoid of the central anchor ('C') pocket. J. Immunol. 160, 2815-2823 (1998).
95. Falk, K. et al. Identification of naturally processed viral nonapeptides allows their quantification in infected cells and suggests an allele-specific T cell epitope forecast. J. Exp. Med. 174, 425-434 (1991).
96. Boehncke, W.-H. et al. The importance of dominant negative effects of amino acid side chain substitution in peptide-MHC molecule interactions and T cell recognition. J. Immunol. 150, 331-341 (1993).
97. Reinherz, E. L. et al. The crystal structure of a T cell receptor in complex with peptide and MHC class II. Science 286, 1913-1921 (1999).
98. Correia-Neves, M., Waltzinger, C., Mathis, D. & Benoist, C. The shaping of the T cell repertoire. Immunity 14, 21-32 (2001).