Specificity, promiscuity, and precursor frequency in immunoreceptors

Current Opinion in Immunology

Volumn 25, Issue 5, 2013, Pages 639-645

  Venturi, Vanessa ^a   Rudd, Brian D ^b   Davenport, Miles P ^a  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

^b Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

B LYMPHOCYTE RECEPTOR; T LYMPHOCYTE RECEPTOR; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 4; ANTIGEN; HISTOCOMPATIBILITY ANTIGEN; LYMPHOCYTE ANTIGEN RECEPTOR;

CELL SPECIFICITY; HUMAN; IMMUNOCOMPETENT CELL; INCIDENCE; MUCOSAL-ASSOCIATED INVARIANT T CELL; NATURAL KILLER T CELL; NONHUMAN; PREVALENCE; PROTEIN EXPRESSION; REVIEW; ANIMAL; GERM CELL; IMMUNOLOGY; INNATE IMMUNITY;

ANIMALS; ANTIGENS; GERM CELLS; HISTOCOMPATIBILITY ANTIGENS; HUMANS; IMMUNITY, INNATE; NATURAL KILLER T-CELLS; RECEPTORS, ANTIGEN, T-CELL;

EID: 84898018750     PISSN: 09527915     EISSN: 18790372     Source Type: Journal    
DOI: 10.1016/j.coi.2013.07.001     Document Type: Review

References (55)

1. 1 Kim, S., Poursine-Laurent, J., Truscott, S.M., Lybarger, L., Song, Y.J., Yang, L., French, A.R., Sunwoo, J.B., Lemieux, S., Hansen, T.H., et al. Licensing of natural killer cells by host major histocompatibility complex class I molecules. Nature 436 (2005), 709–713.
2. 2 Sun, J.C., Beilke, J.N., Lanier, L.L., Adaptive immune features of natural killer cells. Nature 457 (2009), 557–561.
3. 3• Sun, J.C., Madera, S., Bezman, N.A., Beilke, J.N., Kaplan, M.H., Lanier, L.L., Proinflammatory cytokine signaling required for the generation of natural killer cell memory. J Exp Med 209 (2012), 947–954 Demonstration of the direct in vivo role of IL-12 signaling in the expansion of NK cells during murine cytomegalovirus infection and generation of memory NK cells.
4. 4 Schlub, T.E., Sun, J.C., Walton, S.M., Robbins, S.H., Pinto, A.K., Munks, M.W., Hill, A.B., Brossay, L., Oxenius, A., Davenport, M.P., Comparing the kinetics of NK cells, CD4, and CD8 T cells in murine cytomegalovirus infection. J Immunol 187 (2011), 1385–1392.
5. 5 Kjer-Nielsen, L., Borg, N.A., Pellicci, D.G., Beddoe, T., Kostenko, L., Clements, C.S., Williamson, N.A., Smyth, M.J., Besra, G.S., Reid, H.H., et al. A structural basis for selection and cross-species reactivity of the semi-invariant NKT cell receptor in CD1d/glycolipid recognition. J Exp Med 203 (2006), 661–673.
6. 6 Borg, N.A., Wun, K.S., Kjer-Nielsen, L., Wilce, M.C., Pellicci, D.G., Koh, R., Besra, G.S., Bharadwaj, M., Godfrey, D.I., McCluskey, J., et al. CD1d-lipid-antigen recognition by the semi-invariant NKT T-cell receptor. Nature 448 (2007), 44–49.
7. 7 Pellicci, D.G., Patel, O., Kjer-Nielsen, L., Pang, S.S., Sullivan, L.C., Kyparissoudis, K., Brooks, A.G., Reid, H.H., Gras, S., Lucet, I.S., et al. Differential recognition of CD1d-alpha-galactosyl ceramide by the V beta 8.2 and V beta 7 semi-invariant NKT T cell receptors. Immunity 31 (2009), 47–59.
8. 8 Scott-Browne, J.P., Matsuda, J.L., Mallevaey, T., White, J., Borg, N.A., McCluskey, J., Rossjohn, J., Kappler, J., Marrack, P., Gapin, L., Germline-encoded recognition of diverse glycolipids by natural killer T cells. Nat Immunol 8 (2007), 1105–1113.
9. 9 Wun, K.S., Borg, N.A., Kjer-Nielsen, L., Beddoe, T., Koh, R., Richardson, S.K., Thakur, M., Howell, A.R., Scott-Browne, J.P., Gapin, L., et al. A minimal binding footprint on CD1d-glycolipid is a basis for selection of the unique human NKT TCR. J Exp Med 205 (2008), 939–949.
10. 10• Greenaway, H.Y., Ng, B., Price, D.A., Douek, D.C., Davenport, M.P., Venturi, V., NKT and MAIT invariant TCRalpha sequences can be produced efficiently by VJ gene recombination. Immunobiology 218 (2013), 213–224 Efficient production is an important determinant of the prevalence of the universal and evolutionarily conserved NKT and MAIT TCR alpha-chains.
11. 11 Le Bourhis, L., Martin, E., Peguillet, I., Guihot, A., Froux, N., Core, M., Levy, E., Dusseaux, M., Meyssonnier, V., Premel, V., et al. Antimicrobial activity of mucosal-associated invariant T cells. Nat Immunol 11 (2010), 701–708.
12. 12 Reantragoon, R., Kjer-Nielsen, L., Patel, O., Chen, Z., Illing, P.T., Bhati, M., Kostenko, L., Bharadwaj, M., Meehan, B., Hansen, T.H., et al. Structural insight into MR1-mediated recognition of the mucosal associated invariant T cell receptor. J Exp Med 209 (2012), 761–774.
13. 13 Cairo, C., Sagnia, B., Cappelli, G., Colizzi, V., Leke, R.G., Leke, R.J., Pauza, C.D., Human cord blood gammadelta T cells expressing public Vgamma2 chains dominate the response to bisphosphonate plus interleukin-15. Immunology 138 (2013), 346–360.
14. 14 Cairo, C., Armstrong, C.L., Cummings, J.S., Deetz, C.O., Tan, M., Lu, C., Davis, C.E., Pauza, C.D., Impact of age, gender, and race on circulating gammadelta T cells. Hum Immunol 71 (2010), 968–975.
15. 15 Quigley, M.F., Greenaway, H.Y., Venturi, V., Lindsay, R., Quinn, K.M., Seder, R.A., Douek, D.C., Davenport, M.P., Price, D.A., Convergent recombination shapes the clonotypic landscape of the naive T-cell repertoire. Proc Natl Acad Sci U S A 107 (2010), 19414–19419.
16. 16 Robins, H.S., Srivastava, S.K., Campregher, P.V., Turtle, C.J., Andriesen, J., Riddell, S.R., Carlson, C.S., Warren, E.H., Overlap and effective size of the human CD8+ T cell receptor repertoire. Sci Transl Med, 2, 2010, 47ra64.
17. 17 Venturi, V., Quigley, M.F., Greenaway, H.Y., Ng, P.C., Ende, Z.S., McIntosh, T., Asher, T.E., Almeida, J.R., Levy, S., Price, D.A., et al. A mechanism for TCR sharing between T cell subsets and individuals revealed by pyrosequencing. J Immunol 186 (2011), 4285–4294.
18. 18 Li, H., Ye, C., Ji, G., Wu, X., Xiang, Z., Li, Y., Cao, Y., Liu, X., Douek, D.C., Price, D.A., et al. Recombinatorial biases and convergent recombination determine interindividual TCRbeta sharing in murine thymocytes. J Immunol 189 (2012), 2404–2413.
19. 19• Ndifon, W., Gal, H., Shifrut, E., Aharoni, R., Yissachar, N., Waysbort, N., Reich-Zeliger, S., Arnon, R., Friedman, N., Chromatin conformation governs T-cell receptor Jbeta gene segment usage. Proc Natl Acad Sci U S A 109 (2012), 15865–15870 A mechanistic model of chromatin conformation explains observed biases in the pairing of Dβ and Jβ genes during somatic gene recombination.
20. 20 Murugan, A., Mora, T., Walczak, A.M., Callan, C.G. Jr., Statistical inference of the generation probability of T-cell receptors from sequence repertoires. Proc Natl Acad Sci U S A 109 (2012), 16161–16166.
21. 21 Venturi, V., Price, D.A., Douek, D.C., Davenport, M.P., The molecular basis for public T-cell responses?. Nat Rev Immunol 8 (2008), 231–238.
22. 22 Mallevaey, T., Clarke, A.J., Scott-Browne, J.P., Young, M.H., Roisman, L.C., Pellicci, D.G., Patel, O., Vivian, J.P., Matsuda, J.L., McCluskey, J., et al. A molecular basis for NKT cell recognition of CD1d-self-antigen. Immunity 34 (2011), 315–326.
23. 23 Allison, T.J., Winter, C.C., Fournie, J.J., Bonneville, M., Garboczi, D.N., Structure of a human gammadelta T-cell antigen receptor. Nature 411 (2001), 820–824.
24. 24 Adams, J.J., Narayanan, S., Liu, B., Birnbaum, M.E., Kruse, A.C., Bowerman, N.A., Chen, W., Levin, A.M., Connolly, J.M., Zhu, C., et al. T cell receptor signaling is limited by docking geometry to peptide-major histocompatibility complex. Immunity 35 (2011), 681–693.
25. 25 Liu, Y.C., Miles, J.J., Neller, M.A., Gostick, E., Price, D.A., Purcell, A.W., McCluskey, J., Burrows, S.R., Rossjohn, J., Gras, S., Highly divergent T-cell receptor binding modes underlie specific recognition of a bulged viral peptide bound to a HLA class I molecule. J Biol Chem 288 (2013), 15442–15454.
26. 26 Stadinski, B.D., Trenh, P., Smith, R.L., Bautista, B., Huseby, P.G., Li, G., Stern, L.J., Huseby, E.S., A role for differential variable gene pairing in creating T cell receptors specific for unique major histocompatibility ligands. Immunity 35 (2011), 694–704.
27. 27 Ekeruche-Makinde, J., Miles, J.J., van den Berg, H.A., Skowera, A., Cole, D.K., Dolton, G., Schauenburg, A.J., Tan, M.P., Pentier, J.M., Llewellyn-Lacey, S., et al. Peptide length determines the outcome of TCR/peptide-MHCI engagement. Blood 121 (2013), 1112–1123.
28. 28 Warren, R.L., Freeman, J.D., Zeng, T., Choe, G., Munro, S., Moore, R., Webb, J.R., Holt, R.A., Exhaustive T-cell repertoire sequencing of human peripheral blood samples reveals signatures of antigen selection and a directly measured repertoire size of at least 1 million clonotypes. Genome Res 21 (2011), 790–797.
29. 29 Scott-Browne, J.P., White, J., Kappler, J.W., Gapin, L., Marrack, P., Germline-encoded amino acids in the alphabeta T-cell receptor control thymic selection. Nature 458 (2009), 1043–1046.
30. 30• Scott-Browne, J.P., Crawford, F., Young, M.H., Kappler, J.W., Marrack, P., Gapin, L., Evolutionarily conserved features contribute to alphabeta T cell receptor specificity. Immunity 35 (2011), 526–535 Contrasting studies on the role of germline TCR gene-encoded residues in MHC binding.
31. 31• Holland, S.J., Bartok, I., Attaf, M., Genolet, R., Luescher, I.F., Kotsiou, E., Richard, A., Wang, E., White, M., Coe, D.J., et al. The T-cell receptor is not hardwired to engage MHC ligands. Proc Natl Acad Sci U S A 109 (2012), E3111–E3118 Contrasting studies on the role of germline TCR gene-encoded residues in MHC binding.
32. 32 Furmanski, A.L., Ferreira, C., Bartok, I., Dimakou, S., Rice, J., Stevenson, F.K., Millrain, M.M., Simpson, E., Dyson J: Public T, cell receptor beta-chains are not advantaged during positive selection. J Immunol 180 (2008), 1029–1039.
33. 33 Price, D.A., Asher, T.E., Wilson, N.A., Nason, M.C., Brenchley, J.M., Metzler, I.S., Venturi, V., Gostick, E., Chattopadhyay, P.K., Roederer, M., et al. Public clonotype usage identifies protective Gag-specific CD8+ T cell responses in SIV infection. J Exp Med 206 (2009), 923–936.
34. 34 Iglesias, M.C., Almeida, J.R., Fastenackels, S., van Bockel, D.J., Hashimoto, M., Venturi, V., Gostick, E., Urrutia, A., Wooldridge, L., Clement, M., et al. Escape from highly effective public CD8+ T-cell clonotypes by HIV. Blood 118 (2011), 2138–2149.
35. 35 Wang, G.C., Dash, P., McCullers, J.A., Doherty, P.C., Thomas, P.G., T Cell receptor alphabeta diversity inversely correlates with pathogen-specific antibody levels in human cytomegalovirus infection. Sci Transl Med, 4, 2012, 128ra142.
36. 36 Thomas, P.G., Handel, A., Doherty, P.C., La Gruta, N.L., Ecological analysis of antigen-specific CTL repertoires defines the relationship between naive and immune T-cell populations. Proc Natl Acad Sci U S A 110 (2013), 1839–1844.
37. 37•• Gerlach, C., Rohr, J.C., Perie, L., van Rooij, N., van Heijst, J.W., Velds, A., Urbanus, J., Naik, S.H., Jacobs, H., Beltman, J.B., et al. Heterogeneous differentiation patterns of individual CD8+ T cells. Science 340 (2013), 635–639 These two studies demonstrate that T cells bearing identical TCRs have heterogeneous clonal expansion and differentiation patterns in response to antigen.
38. 38•• Buchholz, V.R., Flossdorf, M., Hensel, I., Kretschmer, L., Weissbrich, B., Graf, P., Verschoor, A., Schiemann, M., Hofer, T., Busch, D.H., Disparate individual fates compose robust CD8+ T cell immunity. Science 340 (2013), 630–635 These two studies demonstrate that T cells bearing identical TCRs have heterogeneous clonal expansion and differentiation patterns in response to antigen.
39. 39 Rudd, B.D., Venturi, V., Davenport, M.P., Nikolich-Zugich, J., Evolution of the antigen-specific CD8 + TCR repertoire across the life span: evidence for clonal homogenization of the old TCR repertoire. J Immunol 186 (2011), 2056–2064.
40. 40 Ruckwardt, T.J., Malloy, A.M., Gostick, E., Price, D.A., Dash, P., McClaren, J.L., Thomas, P.G., Graham, B.S., Neonatal CD8 T-cell hierarchy is distinct from adults and is influenced by intrinsic t cell properties in respiratory syncytial virus infected mice. PLoS Pathog, 7, 2011, e1002377.
41. 41 Gilfillan, S., Bachmann, M., Trembleau, S., Adorini, L., Kalinke, U., Zinkernagel, R., Benoist, C., Mathis, D., Efficient immune responses in mice lacking N-region diversity. Eur J Immunol 25 (1995), 3115–3122.
42. 42 Cabaniols, J.P., Fazilleau, N., Casrouge, A., Kourilsky, P., Kanellopoulos, J.M., Most alpha/beta T cell receptor diversity is due to terminal deoxynucleotidyl transferase. J Exp Med 194 (2001), 1385–1390.
43. 43 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 (1995), 793–800.
44. 44 Mold, J.E., Venkatasubrahmanyam, S., Burt, T.D., Michaelsson, J., Rivera, J.M., Galkina, S.A., Weinberg, K., Stoddart, C.A., McCune, J.M., Fetal and adult hematopoietic stem cells give rise to distinct T cell lineages in humans. Science 330 (2010), 1695–1699.
45. 45 Montecino-Rodriguez, E., Dorshkind, K., New perspectives in B-1 B cell development and function. Trends Immunol 27 (2006), 428–433.
46. 46 Baumgarth, N., The double life of a B-1 cell: self-reactivity selects for protective effector functions. Nat Rev — Immunol 11 (2011), 34–46.
47. 47•• Van Rhijn, I., Kasmar, A., de Jong, A., Gras, S., Bhati, M., Doorenspleet, M.E., de Vries, N., Godfrey, D.I., Altman, J.D., de Jager, W., et al. A conserved human T cell population targets mycobacterial antigens presented by CD1b. Nat Immunol 14 (2013), 706–713 A new CD1-restricted T cell subset recognizing mycobacterial antigens bearing an invariant TCR alpha-chain.
48. 48 Venturi, V., Chin, H.Y., Asher, T.E., Ladell, K., Scheinberg, P., Bornstein, E., van Bockel, D., Kelleher, A.D., Douek, D.C., Price, D.A., et al. T cell receptor b-chain sharing in human CD8+ T cell responses to cytomegalovirus and Epstein–Barr virus. J Immunol 181 (2008), 7853–7862.
49. 49 Freeman, J.D., Warren, R.L., Webb, J.R., Nelson, B.H., Holt, R.A., Profiling the T-cell receptor beta-chain repertoire by massively parallel sequencing. Genome Res 19 (2009), 1817–1824.
50. 50 Robins, H.S., Campregher, P.V., Srivastava, S.K., Wacher, A., Turtle, C.J., Kahsai, O., Riddell, S.R., Warren, E.H., Carlson, C.S., Comprehensive assessment of T-cell receptor beta-chain diversity in alphabeta T cells. Blood 114 (2009), 4099–4107.
51. 51 Fazilleau, N., Cabaniols, J.P., Lemaitre, F., Motta, I., Kourilsky, P., Kanellopoulos, J.M., Valpha and Vbeta public repertoires are highly conserved in terminal deoxynucleotidyl transferase-deficient mice. J Immunol 174 (2005), 345–355.
52. 52 Agenes, F., Dangy, J.P., Kirberg, J., T cell receptor contact to restricting MHC molecules is a prerequisite for peripheral interclonal T cell competition. J Exp Med 205 (2008), 2735–2743.
53. 53 Cibotti, R., Cabaniols, J.P., Pannetier, C., Delarbre, C., Vergnon, I., Kanellopoulos, J.M., Kourilsky, P., Public and private V beta T cell receptor repertoires against hen egg white lysozyme (HEL) in nontransgenic versus HEL transgenic mice. J Exp Med 180 (1994), 861–872.
54. 54 Kedzierska, K., Turner, S.J., Doherty, P.C., Conserved T cell receptor usage in primary and recall responses to an immunodominant influenza virus nucleoprotein epitope. Proc Natl Acad Sci U S A 101 (2004), 4942–4947.
55. 55 Price, D.A., Brenchley, J.M., Ruff, L.E., Betts, M.R., Hill, B.J., Roederer, M., Koup, R.A., Migueles, S.A., Gostick, E., Wooldridge, L., et al. Avidity for antigen shapes clonal dominance in CD8+ T cell populations specific for persistent DNA viruses. J Exp Med 202 (2005), 1349–1361.