A mechanism for TCR sharing between T cell subsets and individuals revealed by pyrosequencing

Journal of Immunology

Volumn 186, Issue 7, 2011, Pages 4285-4294

  Venturi, Vanessa ^a   Quigley, Máire F ^b   Greenaway, Hui Yee ^a   Ng, Pauline C ^c,d   Ende, Zachary S ^b   McIntosh, Tina ^d   Asher, Tedi E ^b   Almeida, Jorge R ^b   Levy, Samuel ^e   Price, David A ^b,f   Davenport, Miles P ^a   Douek, Daniel C ^b  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

^b NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^c GENOME INSTITUTE OF SINGAPORE   (Singapore)

^d J CRAIG VENTER INSTITUTE   (United States)

^e SCRIPPS RESEARCH INSTITUTE   (United States)

^f CARDIFF UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

T LYMPHOCYTE RECEPTOR;

ADULT; ARTICLE; CD8+ T LYMPHOCYTE; CELL COMPARTMENTALIZATION; CONTROLLED STUDY; GENE; GENETIC RECOMBINATION; HUMAN; HUMAN CELL; MALE; MEMORY T LYMPHOCYTE; MOLECULAR CLONING; PHENOTYPE; PREDICTION; PRIORITY JOURNAL; PROTEIN SYNTHESIS; PYROSEQUENCING; T LYMPHOCYTE SUBPOPULATION; TRBJ GENE; TRBV GENE;

ADULT; CLONE CELLS; G0 PHASE; GENE REARRANGEMENT, BETA-CHAIN T-CELL ANTIGEN RECEPTOR; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; IMMUNOGLOBULIN VARIABLE REGION; IMMUNOLOGIC MEMORY; MALE; MIDDLE AGED; RECEPTORS, ANTIGEN, T-CELL, ALPHA-BETA; RECOMBINATION, GENETIC; T-LYMPHOCYTE SUBSETS; YOUNG ADULT;

EID: 79955022207     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1003898     Document Type: Article

References (43)

1. Nikolich-Zugich, J., M. K. Slifka, and I. Messaoudi. 2004. The many important facets of T-cell repertoire diversity. Nat. Rev. Immunol. 4: 123-132. (Pubitemid 38209206)
2. Davenport, M. P., D. A. Price, and A. J. McMichael. 2007. The T cell repertoire in infection and vaccination: Implications for control of persistent viruses. Curr. Opin. Immunol. 19: 294-300. (Pubitemid 46687007)
3. Price, D. A., T. E. Asher, N. A. Wilson, M. C. Nason, J. M. Brenchley, I. S. Metzler, V. Venturi, E. Gostick, P. K. Chattopadhyay, M. Roederer, et al. 2009. Public clonotype usage identifies protective Gag-specific CD8+ T cell responses in SIV infection. J. Exp. Med. 206: 923-936.
4. Arstila, T. P., A. Casrouge, V. Baron, J. Even, J. Kanellopoulos, and P. Kourilsky. 1999. A direct estimate of the human alphabeta T cell receptor diversity. Science 286: 958-961.
5. Arstila, T. P., A. Casrouge, V. Baron, J. Even, J. Kanellopoulos, and P. Kourilsky. 2000. Diversity of human alpha beta T cell receptors. Science 288: 1135.
6. Mason, D. 1998. A very high level of crossreactivity is an essential feature of the T-cell receptor. Immunol. Today 19: 395-404. (Pubitemid 28392279)
7. Snyder, C. M., K. S. Cho, E. L. Bonnett, S. van Dommelen, G. R. Shellam, and A. B. Hill. 2008. Memory inflation during chronic viral infection is maintained by continuous production of short-lived, functional T cells. Immunity 29: 650-659.
8. Vezys, V., D. Masopust, C. C. Kemball, D. L. Barber, L. A. O'Mara, C. P. Larsen, T. C. Pearson, R. Ahmed, and A. E. Lukacher. 2006. Continuous recruitment of naive T cells contributes to heterogeneity of antiviral CD8 T cells during persistent infection. J. Exp. Med. 203: 2263-2269. (Pubitemid 44498361)
9. van Heijst, J. W., C. Gerlach, E. Swart, D. Sie, C. Nunes-Alves, R. M. Kerkhoven, R. Arens, M. Correia-Neves, K. Schepers, and T. N. Schumacher. 2009. Recruitment of antigen-specific CD8+ T cells in response to infection is markedly efficient. Science 325: 1265-1269.
10. Price, D. A., J. M. Brenchley, L. E. Ruff, M. R. Betts, B. J. Hill, M. Roederer, R. A. Koup, S. A. Migueles, E. Gostick, L. Wooldridge, et al. 2005. Avidity for antigen shapes clonal dominance in CD8+ T cell populations specific for persistent DNA viruses. J. Exp. Med. 202: 1349-1361. (Pubitemid 41668738)
11. Zehn, D., S. Y. Lee, and M. J. Bevan. 2009. Complete but curtailed T-cell response to very low-affinity antigen. Nature 458: 211-214.
12. Correia-Neves, M., C. Waltzinger, D. Mathis, and C. Benoist. 2001. The shaping of the T cell repertoire. Immunity 14: 21-32. (Pubitemid 32144684)
13. Furmanski, A. L., C. Ferreira, I. Bartok, S. Dimakou, J. Rice, F. K. Stevenson, M. M. Millrain, E. Simpson, and J. Dyson. 2008. Public T cell receptor betachains are not advantaged during positive selection. J. Immunol. 180: 1029-1039.
14. Bouneaud, C., Z. Garcia, P. Kourilsky, and C. Pannetier. 2005. Lineage relationships, homeostasis, and recall capacities of central- and effector-memory CD8 T cells in vivo. J. Exp. Med. 201: 579-590. (Pubitemid 40289548)
15. Baron, V., C. Bouneaud, A. Cumano, A. Lim, T. P. Arstila, P. Kourilsky, L. Ferradini, and C. Pannetier. 2003. The repertoires of circulating human CD8 (+) central and effector memory T cell subsets are largely distinct. Immunity 18: 193-204. (Pubitemid 36262995)
16. Bousso, P., A. Casrouge, J. D. Altman, M. Haury, J. Kanellopoulos, J. P. Abastado, and P. Kourilsky. 1998. Individual variations in the murine T cell response to a specific peptide reflect variability in naive repertoires. Immunity 9: 169-178. (Pubitemid 28400030)
17. Turner, S. J., P. C. Doherty, J. McCluskey, and J. Rossjohn. 2006. Structural determinants of T-cell receptor bias in immunity. Nat. Rev. Immunol. 6: 883-894. (Pubitemid 44851731)
18. Venturi, V., D. A. Price, D. C. Douek, and M. P. Davenport. 2008. The molecular basis for public T-cell responses? Nat. Rev. Immunol. 8: 231-238. (Pubitemid 351323289)
19. Venturi, V., K. Kedzierska, D. A. Price, P. C. Doherty, D. C. Douek, S. J. Turner, and M. P. Davenport. 2006. Sharing of T cell receptors in antigen-specific responses is driven by convergent recombination. Proc. Natl. Acad. Sci. USA 103: 18691-18696. (Pubitemid 44913472)
20. Venturi, V., H. Y. Chin, D. A. Price, D. C. Douek, and M. P. Davenport. 2008. The role of production frequency in the sharing of simian immunodeficiency virus-specific CD8+ TCRs between macaques. J. Immunol. 181: 2597-2609.
21. Venturi, V., H. Y. Chin, T. E. Asher, K. Ladell, P. Scheinberg, E. Bornstein, D. van Bockel, A. D. Kelleher, D. C. Douek, D. A. Price, and M. P. Davenport. 2008. TCR beta-chain sharing in human CD8+ T cell responses to cytomegalovirus and EBV. J. Immunol. 181: 7853-7862.
22. Freeman, J. D., R. L. Warren, J. R. Webb, B. H. Nelson, and R. A. Holt. 2009. Profiling the T-cell receptor beta-chain repertoire by massively parallel sequencing. Genome Res. 19: 1817-1824.
23. Robins, H. S., P. V. Campregher, S. K. Srivastava, A. Wacher, C. J. Turtle, O. Kahsai, S. R. Riddell, E. H. Warren, and C. S. Carlson. 2009. Comprehensive assessment of T-cell receptor beta-chain diversity in alphabeta T cells. Blood 114: 4099-4107.
24. Robins, H. S., S. K. Srivastava, P. V. Campregher, C. J. Turtle, J. Andriesen, S. R. Riddell, C. S. Carlson, and E. H. Warren. 2010. Overlap and effective size of the human CD8+ T cell receptor repertoire. Sci. Transl. Med. 2: 47ra64.
25. Chattopadhyay, P. K., D. A. Price, T. F. Harper, M. R. Betts, J. Yu, E. Gostick, S. P. Perfetto, P. Goepfert, R. A. Koup, S. C. De Rosa, et al. 2006. Quantum dot semiconductor nanocrystals for immunophenotyping by polychromatic flow cytometry. Nat. Med. 12: 972-977. (Pubitemid 44175152)
26. Lefranc, M. P., V. Giudicelli, C. Ginestoux, J. Bodmer, W. Müller, R. Bontrop, M. Lemaitre, A. Malik, V. Barbié, and D. Chaume. 1999. IMGT, the international ImMunoGeneTics database. Nucleic Acids Res. 27: 209-212. (Pubitemid 29209441)
27. Margulies, M., M. Egholm, W. E. Altman, S. Attiya, J. S. Bader, L. A. Bemben, J. Berka, M. S. Braverman, Y. J. Chen, Z. Chen, et al. 2005. Genome sequencing in microfabricated high-density picolitre reactors. [Published erratum appears in 2006 Nature: 441: 326-327.] Nature 437: 376-380. (Pubitemid 41613494)
28. Douek, D. C., M. R. Betts, J. M. Brenchley, B. J. Hill, D. R. Ambrozak, K. L. Ngai, N. J. Karandikar, J. P. Casazza, and R. A. Koup. 2002. A novel approach to the analysis of specificity, clonality, and frequency of HIV-specific T cell responses reveals a potential mechanism for control of viral escape. J. Immunol. 168: 3099-3104. (Pubitemid 34211693)
29. Altschul, S. F., W. Gish, W. Miller, E. W. Myers, and D. J. Lipman. 1990. Basic local alignment search tool. J. Mol. Biol. 215: 403-410.
30. Weekes, M. P., M. R. Wills, K. Mynard, A. J. Carmichael, and J. G. Sissons. 1999. The memory cytotoxic T-lymphocyte (CTL) response to human cytomegalovirus infection contains individual peptide-specific CTL clones that have undergone extensive expansion in vivo. J. Virol. 73: 2099-2108. (Pubitemid 29098114)
31. Khan, N., M. Cobbold, R. Keenan, and P. A. Moss. 2002. Comparative analysis of CD8+ T cell responses against human cytomegalovirus proteins pp65 and immediate early 1 shows similarities in precursor frequency, oligoclonality, and phenotype. J. Infect. Dis. 185: 1025-1034. (Pubitemid 34297759)
32. Khan, N., N. Shariff, M. Cobbold, R. Bruton, J. A. Ainsworth, A. J. Sinclair, L. Nayak, and P. A. Moss. 2002. Cytomegalovirus seropositivity drives the CD8 T cell repertoire toward greater clonality in healthy elderly individuals. J. Immunol. 169: 1984-1992. (Pubitemid 34857662)
33. Trautmann, L., M. Rimbert, K. Echasserieau, X. Saulquin, B. Neveu, J. Dechanet, V. Cerundolo, and M. Bonneville. 2005. Selection of T cell clones expressing high-affinity public TCRs within Human cytomegalovirus-specific CD8 T cell responses. J. Immunol. 175: 6123-6132. (Pubitemid 41508100)
34. Day, E. K., A. J. Carmichael, I. J. ten Berge, E. C. Waller, J. G. Sissons, and M. R. Wills. 2007. Rapid CD8+ T cell repertoire focusing and selection of highaffinity clones into memory following primary infection with a persistent human virus: Human cytomegalovirus. J. Immunol. 179: 3203-3213.
35. Fazilleau, N., J. P. Cabaniols, F. Lemaître, I. Motta, P. Kourilsky, and J. M. Kanellopoulos. 2005. Valpha and Vbeta public repertoires are highly conserved in terminal deoxynucleotidyl transferase-deficient mice. J. Immunol. 174: 345-355. (Pubitemid 40007422)
36. Price, D. A., S. M. West, M. R. Betts, L. E. Ruff, J. M. Brenchley, D. R. Ambrozak, Y. Edghill-Smith, M. J. Kuroda, D. Bogdan, K. Kunstman, et al. 2004. T cell receptor recognition motifs govern immune escape patterns in acute SIV infection. Immunity 21: 793-803. (Pubitemid 39626670)
37. Cornberg, M., A. T. Chen, L. A. Wilkinson, M. A. Brehm, S. K. Kim, C. Calcagno, D. Ghersi, R. Puzone, F. Celada, R. M. Welsh, and L. K. Selin. 2006. Narrowed TCR repertoire and viral escape as a consequence of heterologous immunity. J. Clin. Invest. 116: 1443-1456.
38. Meyer-Olson, D., N. H. Shoukry, K. W. Brady, H. Kim, D. P. Olson, K. Hartman, A. K. Shintani, C. M. Walker, and S. A. Kalams. 2004. Limited T cell receptor diversity of HCV-specific T cell responses is associated with CTL escape. J. Exp. Med. 200: 307-319. (Pubitemid 39031250)
39. Cicin-Sain, L., S. Smyk-Pearson, N. Currier, L. Byrd, C. Koudelka, T. Robinson, G. Swarbrick, S. Tackitt, A. Legasse, M. Fischer, et al. 2010. Loss of naive T cells and repertoire constriction predict poor response to vaccination in old primates. [Published erratum in 2010 J. Immunol. 185: 4509.] J. Immunol. 184: 6739-6745.
40. Nikolich-Zugich, J. 2008. Ageing and life-long maintenance of T-cell subsets in the face of latent persistent infections. Nat. Rev. Immunol. 8: 512-522. (Pubitemid 351913675)
41. Malherbe, L., C. Hausl, L. Teyton, and M. G. McHeyzer-Williams. 2004. Clonal selection of helper T cells is determined by an affinity threshold with no further skewing of TCR binding properties. Immunity 21: 669-679. (Pubitemid 39487890)
42. Chang, J. T., V. R. Palanivel, I. Kinjyo, F. Schambach, A. M. Intlekofer, A. Banerjee, S. A. Longworth, K. E. Vinup, P. Mrass, J. Oliaro, et al. 2007. Asymmetric T lymphocyte division in the initiation of adaptive immune responses. Science 315: 1687-1691. (Pubitemid 46515618)
43. Douek, D. C., P. D. Kwong, and G. J. Nabel. 2006. The rational design of an AIDS vaccine. Cell 124: 677-681. (Pubitemid 43261441)