Development and function of innate polyclonal TCRαβ+ CD8+ thymocytes

Journal of Immunology

Volumn 187, Issue 6, 2011, Pages 3133-3144

  Rafei, Moutih ^a   Hardy, Marie Pierre ^a   Williams, Patrick ^b   Vanegas, Juan Ruiz ^a   Forner, Kathy Ann ^b   Dulude, Gaël ^a   Labrecque, Nathalie ^c   Galipeau, Jacques ^a,d   Perreault, Claude ^a  

^a INSTITUTE FOR RESEARCH IN IMMUNOLOGY AND CANCER   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c UNIVERSITY OF MONTREAL   (Canada)

^d EMORY UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD2 ANTIGEN; CD38 ANTIGEN; CD5 ANTIGEN; GAMMA INTERFERON; INTERLEUKIN 2; INTERLEUKIN 2 RECEPTOR BETA; INTERLEUKIN 4; INTERLEUKIN 4 RECEPTOR ALPHA; PROGRAMMED DEATH 1 LIGAND 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CD4 CD8 RATIO; CD8+ T LYMPHOCYTE; CELL COUNT; CELL EXPANSION; CELL FUNCTION; CELL MATURATION; CELL PROLIFERATION; CELL SELECTION; CELL STIMULATION; CELL SURFACE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DOWN REGULATION; EOMES GENE; GENE; ID3 GENE; IMMUNOREACTIVITY; INNATE IMMUNITY; KLF2 GENE; MOUSE; NONHUMAN; POLYCLONAL ACTIVATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; T BET GENE; THYMOCYTE;

ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; CYTOKINES; ENZYME-LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION PROFILING; IMMUNITY, INNATE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PHENOTYPE; RECEPTORS, ANTIGEN, T-CELL, ALPHA-BETA; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; T-LYMPHOCYTE SUBSETS;

EID: 80053083320     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1101097     Document Type: Article

References (69)

1. Zinkernagel, R. M. 2002. Uncertainties - discrepancies in immunology. Immunol. Rev. 185: 103-125. (Pubitemid 34994935)
2. Flajnik, M. F., and L. Du Pasquier. 2008. Evolution of the immune system. In Fundamental Immunology, 6th Ed. W. E. Paul, ed. Lippincott Williams & Wilkins, Philadelphia, p. 56-124.
3. Parham, P. 2009. Principles of adaptive immunity. In The Immune System, 3rd Ed. P. Parham, ed. Garland Science, New York, p. 71-92.
4. Berg, L. J. 2007. Signalling through TEC kinases regulates conventional versus innate CD8(+) T-cell development. Nat. Rev. Immunol. 7: 479-485. (Pubitemid 46834846)
5. Hayday, A. C. 2009. Gammadelta T cells and the lymphoid stress-surveillance response. Immunity 31: 184-196.
6. Godfrey, D. I., S. Stankovic, and A. G. Baxter. 2010. Raising the NKT cell family. Nat. Immunol. 11: 197-206.
7. Surh, C. D., and J. Sprent. 2008. Homeostasis of naive and memory T cells. Immunity 29: 848-862.
8. Lee, Y. J., S. C. Jameson, and K. A. Hogquist. 2011. Alternative memory in the CD8 T cell lineage. Trends Immunol. 32: 50-56.
9. Blais, M. E., I. Louis, and C. Perreault. 2006. T-cell development: an extrathymic perspective. Immunol. Rev. 209: 103-114.
10. Blais, M. E., S. Brochu, M. Giroux, M. P. Bélanger, G. Dulude, R. P. Sékaly, and C. Perreault. 2008. Why T cells of thymic versus extrathymic origin are functionally different. J. Immunol. 180: 2299-2312.
11. Weinreich, M. A., O. A. Odumade, S. C. Jameson, and K. A. Hogquist. 2010. T cells expressing the transcription factor PLZF regulate the development of memory-like CD8+ T cells. Nat. Immunol. 11: 709-716.
12. Fukuyama, T., L. H. Kasper, F. Boussouar, T. Jeevan, J. Van Deursen, and P. K. Brindle. 2009. Histone acetyltransferase CBP is vital to demarcate conventional and innate CD8+ T-cell development. Mol. Cell. Biol. 29: 3894-3904.
13. Verykokakis, M., M. D. Boos, A. Bendelac, and B. L. Kee. 2010. SAP protein-dependent natural killer T-like cells regulate the development of CD8(+) T cells with innate lymphocyte characteristics. Immunity 33: 203-215.
14. Kovalovsky, D., E. S. Alonzo, O. U. Uche, M. Eidson, K. E. Nichols, and D. B. Sant'Angelo. 2010. PLZF induces the spontaneous acquisition of memory/ effector functions in T cells independently of NKT cell-related signals. J. Immunol. 184: 6746-6755.
15. Hale, J. S., T. E. Boursalian, G. L. Turk, and P. J. Fink. 2006. Thymic output in aged mice. Proc. Natl. Acad. Sci. USA 103: 8447-8452. (Pubitemid 43838475)
16. Yu, W., H. Nagaoka, M. Jankovic, Z. Misulovin, H. Suh, A. Rolink, F. Melchers, E. Meffre, and M. C. Nussenzweig. 1999. Continued RAG expression in late stages of B cell development and no apparent re-induction after immunization. Nature 400: 682-687.
17. Meunier, M. C., J. S. Delisle, J. Bergeron, V. Rineau, C. Baron, and C. Perreault. 2005. T cells targeted against a single minor histocompatibility antigen can cure solid tumors. Nat. Med. 11: 1222-1229. (Pubitemid 43093670)
18. Giroux, M., J.-S. Delisle, S.-D. Gauthier, K. M. Heinonen, J. Hinsinger, B. Houde, L. Gaboury, S. Brochu, J. Wu, M. J. Hébert, and C. Perreault. 2011. SMAD3 prevents graft-versus-host disease by restraining Th1 differentiation and granulocyte-mediated tissue damage. Blood 117: 1734-1744.
19. Louis, I., K. M. Heinonen, J. Chagraoui, S. Vainio, G. Sauvageau, and C. Perreault. 2008. The signaling protein Wnt4 enhances thymopoiesis and expands multipotent hematopoietic progenitors through β-catenin-independent signaling. Immunity 29: 57-67.
20. Poulin, J. F., M. Sylvestre, P. Champagne, M. L. Dion, N. Kettaf, A. Dumont, M. Lainesse, P. Fontaine, D. C. Roy, C. Perreault, et al. 2003. Evidence for adequate thymic function but impaired naive T-cell survival following allogeneic hematopoietic stem cell transplantation in the absence of chronic graft-versushost disease. Blood 102: 4600-4607. (Pubitemid 37494130)
21. Yang Yu, Zizheng Wang, and Tongxin Du. 2008. Mouse thymus targeted peptide isolated by in vivo phage display can inhibit bioactivity of thymus output in vivo. J. Biomol. Screen. 13: 968-974.
22. Hale, J. S., and P. J. Fink. 2009. Back to the thymus: peripheral T cells come home. Immunol. Cell Biol. 87: 58-64.
23. Dion, M. L., R. P. Sékaly, and R. Cheynier. 2007. Estimating thymic function through quantification of T-cell receptor excision circles. Methods Mol. Biol. 380: 197-213. (Pubitemid 350183330)
24. Azzam, H. S., A. Grinberg, K. Lui, H. Shen, E. W. Shores, and P. E. Love. 1998. CD5 expression is developmentally regulated by T cell receptor (TCR) signals and TCR avidity. J. Exp. Med. 188: 2301-2311. (Pubitemid 29028502)
25. Phee, H., I. Dzhagalov, M. Mollenauer, Y. Wang, D. J. Irvine, E. Robey, and A. Weiss. 2010. Regulation of thymocyte positive selection and motility by GIT2. Nat. Immunol. 11: 503-511.
26. + T cell responses develop independent of thymic epithelial MHC. Proc. Natl. Acad. Sci. USA 103: 14435-14440.
27. Nitta, T., S. Murata, K. Sasaki, H. Fujii, A. M. Ripen, N. Ishimaru, S. Koyasu, K. Tanaka, and Y. Takahama. 2010. Thymoproteasome shapes immunocompetent repertoire of CD8+ T cells. Immunity 32: 29-40.
28. Terra, R., N. Labrecque, and C. Perreault. 2002. Thymic and extrathymic T cell development pathways follow different rules. J. Immunol. 169: 684-692. (Pubitemid 34753423)
29. Madsen, L., N. Labrecque, J. Engberg, A. Dierich, A. Svejgaard, C. Benoist, D. Mathis, and L. Fugger. 1999. Mice lacking all conventional MHC class II genes. Proc. Natl. Acad. Sci. USA 96: 10338-10343. (Pubitemid 29422559)
30. Hogquist, K. A., S. C. Jameson, W. R. Heath, J. L. Howard, M. J. Bevan, and F. R. Carbone. 1994. T cell receptor antagonist peptides induce positive selection. Cell 76: 17-27. (Pubitemid 24035278)
31. Murali-Krishna, K., and R. Ahmed. 2000. Cutting edge: naive T cells masquerading as memory cells. J. Immunol. 165: 1733-1737. (Pubitemid 30643121)
32. Chen, L. 2004. Co-inhibitory molecules of the B7-CD28 family in the control of T-cell immunity. Nat. Rev. Immunol. 4: 336-347. (Pubitemid 38649276)
33. Francisco, L. M., P. T. Sage, and A. H. Sharpe. 2010. The PD-1 pathway in tolerance and autoimmunity. Immunol. Rev. 236: 219-242.
34. Butte, M. J., M. E. Keir, T. B. Phamduy, A. H. Sharpe, and G. J. Freeman. 2007. Programmed death-1 ligand 1 interacts specifically with the B7-1 costimulatory molecule to inhibit T cell responses. Immunity 27: 111-122. (Pubitemid 47089023)
35. Keir, M. E., S. C. Liang, I. Guleria, Y. E. Latchman, A. Qipo, L. A. Albacker, M. Koulmanda, G. J. Freeman, M. H. Sayegh, and A. H. Sharpe. 2006. Tissue expression of PD-L1 mediates peripheral T cell tolerance. J. Exp. Med. 203: 883-895.
36. Park, J. H., Q. Yu, B. Erman, J. S. Appelbaum, D. Montoya-Durango, H. L. Grimes, and A. Singer. 2004. Suppression of IL7Ralpha transcription by IL-7 and other prosurvival cytokines: a novel mechanism for maximizing IL-7- dependent T cell survival. Immunity 21: 289-302. (Pubitemid 39094057)
37. Ohara, J., and W. E. Paul. 1988. Up-regulation of interleukin 4/B-cell stimulatory factor 1 receptor expression. Proc. Natl. Acad. Sci. USA 85: 8221-8225.
38. Mummert, M. E., D. Mummert, D. Edelbaum, F. Hui, H. Matsue, and A. Takashima. 2002. Synthesis and surface expression of hyaluronan by dendritic cells and its potential role in antigen presentation. J. Immunol. 169: 4322-4331. (Pubitemid 35178205)
39. Baaten, B. J. B., C. R. Li, M. F. Deiro, M. M. Lin, P. J. Linton, and L. M. Bradley. 2010. CD44 regulates survival and memory development in Th1 cells. Immunity 32: 104-115.
40. Weinreich, M. A., K. Takada, C. Skon, S. L. Reiner, S. C. Jameson, and K. A. Hogquist. 2009. KLF2 transcription-factor deficiency in T cells results in unrestrained cytokine production and upregulation of bystander chemokine receptors. Immunity 31: 122-130.
41. Urdahl, K. B., J. C. Sun, and M. J. Bevan. 2002. Positive selection of MHC class Ib-restricted CD8(+) T cells on hematopoietic cells. Nat. Immunol. 3: 772-779.
42. Prince, A. L., C. C. Yin, M. E. Enos, M. Felices, and L. J. Berg. 2009. The Tec kinases Itk and Rlk regulate conventional versus innate T-cell development. Immunol. Rev. 228: 115-131.
43. Singer, A., S. Adoro, and J. H. Park. 2008. Lineage fate and intense debate: myths, models and mechanisms of CD4- versus CD8-lineage choice. Nat. Rev. Immunol. 8: 788-801.
44. Berg, L. J. 2009. Strength of T cell receptor signaling strikes again. Immunity 31: 529-531.
45. Carpenter, A. C., and R. Bosselut. 2010. Decision checkpoints in the thymus. Nat. Immunol. 11: 666-673.
46. Labrecque, N., T. Baldwin, and S. Lesage. 2011. Molecular and genetic parameters defining T-cell clonal selection. Immunol. Cell Biol. 89: 16-26.
47. Berg, L. J., L. D. Finkelstein, J. A. Lucas, and P. L. Schwartzberg. 2005. Tec family kinases in T lymphocyte development and function. Annu. Rev. Immunol. 23: 549-600. (Pubitemid 40563180)
48. Keir, M. E., M. J. Butte, G. J. Freeman, and A. H. Sharpe. 2008. PD-1 and its ligands in tolerance and immunity. Annu. Rev. Immunol. 26: 677-704. (Pubitemid 351600389)
49. Saini, M., C. Sinclair, D. Marshall, M. Tolaini, S. Sakaguchi, and B. Seddon. 2010. Regulation of Zap70 expression during thymocyte development enables temporal separation of CD4 and CD8 repertoire selection at different signaling thresholds. Sci. Signal. 3: ra23.
50. Tarakhovsky, A., S. B. Kanner, J. Hombach, J. A. Ledbetter, W. Müller, N. Killeen, and K. Rajewsky. 1995. A role for CD5 in TCR-mediated signal transduction and thymocyte selection. Science 269: 535-537.
51. Dalloul, A. 2009. CD5: a safeguard against autoimmunity and a shield for cancer cells. Autoimmun. Rev. 8: 349-353.
52. Shubinsky, G., and M. Schlesinger. 1997. The CD38 lymphocyte differentiation marker: new insight into its ectoenzymatic activity and its role as a signal transducer. Immunity 7: 315-324. (Pubitemid 27446006)
53. Muñoz, P., M. Mittelbrunn, H. De la Fuente, M. Pérez- Martínez, A. García-Pérez, A. Ariza-Veguillas, F. Malavasi, M. Zubiaur, F. Sánchez-Madrid, and J. Sancho. 2008. Antigen-induced clustering of surface CD38 and recruitment of intracellular CD38 to the immunologic synapse. Blood 111: 3653-3664.
54. Ferber, I., G. Schönrich, J. Schenkel, A. L. Mellor, G. J. Hämmerling, and B. Arnold. 1994. Levels of peripheral T cell tolerance induced by different doses of tolerogen. Science 263: 674-676. (Pubitemid 24076292)
55. Cai, Z., H. Kishimoto, A. Brunmark, M. R. Jackson, P. A. Peterson, and J. Sprent. 1997. Requirements for peptide-induced T cell receptor downregulation on naive CD8+ T cells. J. Exp. Med. 185: 641-651. (Pubitemid 27098149)
56. Sato, K., K. Ohtsuka, K. Hasegawa, S. Yamagiwa, H.Watanabe, H. Asakura, and T. Abo. 1995. Evidence for extrathymic generation of intermediate T cell receptor cells in the liver revealed in thymectomized, irradiated mice subjected to bone marrow transplantation. J. Exp. Med. 182: 759-767.
57. Park, J. H., S. Adoro, T. Guinter, B. Erman, A. S. Alag, M. Catalfamo, M. Y. Kimura, Y. Cui, P. J. Lucas, R. E. Gress, et al. 2010. Signaling by intrathymic cytokines, not T cell antigen receptors, specifies CD8 lineage choice and promotes the differentiation of cytotoxic-lineage T cells. Nat. Immunol. 11: 257-264.
58. Wills-Karp, M., and F. D. Finkelman. 2008. Untangling the complex web of IL-4- and IL-13-mediated signaling pathways. Sci. Signal. 1: pe55.
59. + T cell development by thymus-specific proteasomes. Science 316: 1349-1353.
60. Macagno, A., M. Gilliet, F. Sallusto, A. Lanzavecchia, F. O. Nestle, and M. Groettrup. 1999. Dendritic cells up-regulate immunoproteasomes and the proteasome regulator PA28 during maturation. Eur. J. Immunol. 29: 4037-4042.
61. Pelletier, S., K. G. Schuurman, C. R. Berkers, H. Ovaa, A. J. Heck, and R. Raijmakers. 2010. Quantifying cross-tissue diversity in proteasome complexes by mass spectrometry. Mol. Biosyst. 6: 1450-1453.
62. De Verteuil, D., T. L. Muratore-Schroeder, D. P. Granados, M. H. Fortier, M. P. Hardy, A. Bramoullé, E. Caron, K. Vincent, S. Mader, S. Lemieux, et al. 2010. Deletion of immunoproteasome subunits imprints on the transcriptome and has a broad impact on peptides presented by major histocompatibility complex I molecules. Mol. Cell. Proteomics 9: 2034-2047.
63. Florea, B. I., M. Verdoes, N. Li, W. A. Van der Linden, P. P. Geurink, H. Van den Elst, T. Hofmann, A. De Ru, P. A. Van Veelen, K. Tanaka, et al. 2010. Activitybased profiling reveals reactivity of the murine thymoproteasome- specific subunit beta5t. Chem. Biol. 17: 795-801.
64. Anderson, G., and E. J. Jenkinson. 2001. Lymphostromal interactions in thymic development and function. Nat. Rev. Immunol. 1: 31-40. (Pubitemid 33741973)
65. Petrie, H. T., and J. C. Zúñiga-Pflücker. 2007. Zoned out: functional mapping of stromal signaling microenvironments in the thymus. Annu. Rev. Immunol. 25: 649-679. (Pubitemid 46697920)
66. Heinonen, K. M., and C. Perreault. 2008. Development and functional properties of thymic and extrathymic T lymphocytes. Crit. Rev. Immunol. 28: 441-466.
67. Blais, M. E., G. Gérard, M. M. Martinic, G. Roy-Proulx, R. M. Zinkernagel, and C. Perreault. 2004. Do thymically and strictly extrathymically developing T cells generate similar immune responses? Blood 103: 3102-3110. (Pubitemid 38451687)
68. + T cells provide innate immune protection against Listeria monocytogenes in the absence of cognate antigen. J. Exp. Med. 198: 1583-1593.
69. Vivier, E., D. H. Raulet, A. Moretta, M. A. Caligiuri, L. Zitvogel, L. L. Lanier, W. M. Yokoyama, and S. Ugolini. 2011. Innate or adaptive immunity? The example of natural killer cells. Science 331: 44-49.