Peripheral regulatory T lymphocytes recirculating to the thymus suppress the development of their precursors

Nature Immunology

Volumn 16, Issue 6, 2015, Pages 628-634

  Thiault, Nicolas ^a,b,c   Darrigues, Julie ^a,b,c   Adoue, Véronique ^a,b,c   Gros, Marine ^a,b,c,d   Binet, Bénédicte ^a,b,c   Perals, Corine ^a,b,c   Leobon, Bertrand ^e   Fazilleau, Nicolas ^a,b,c   Joffre, Olivier P ^a,b,c   Robey, Ellen A ^f   Van Meerwijk, Joost P M ^a,b,c   Romagnoli, Paola ^a,b,c  

^a INSERM   (France)

^b CNRS   (France)

^c UNIVERSITÉ PAUL SABATIER   (France)

^d UNIVERSITÉ DE LYON   (France)

^e TOULOUSE UNIVERSITY HOSPITAL   (France)

^f UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 2; TRANSCRIPTION FACTOR FOXP3; TRANSCRIPTION FACTOR T BET; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, MOUSE;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CD4+ T LYMPHOCYTE; CELL MATURATION; CONTROLLED STUDY; GENE EXPRESSION; GROWTH INHIBITION; HUMAN; HUMAN CELL; INVOLUTION; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE FUNCTION; LYMPHOID PROGENITOR CELL; MOUSE; NEGATIVE FEEDBACK; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; THYMUS; AGING; ANIMAL; C57BL MOUSE; CELL CULTURE; CELL DIFFERENTIATION; CHILD; CIRCULATION; FEEDBACK SYSTEM; GENETICS; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; METABOLISM; PHYSIOLOGY; PRE T LYMPHOCYTE; T LYMPHOCYTE SUBPOPULATION; TRANSGENIC MOUSE;

AGING; ANIMALS; BLOOD CIRCULATION; CELL DIFFERENTIATION; CELLS, CULTURED; CHILD; FEEDBACK, PHYSIOLOGICAL; FORKHEAD TRANSCRIPTION FACTORS; HUMANS; IMMUNE TOLERANCE; INTERLEUKIN-2; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PRECURSOR CELLS, T-LYMPHOID; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES, REGULATORY; THYMUS GLAND;

EID: 84929944502     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/ni.3150     Document Type: Article

References (45)

1. Sakaguchi, S. , Miyara, M. , Costantino, C. M. & Hafler, D. A. FOXP3+ regulatory T cells in the human immune system. Nat. Rev. Immunol. 10, 490-500 (2010).
2. Josefowicz, S. Z. , Lu, L. F. & Rudensky, A. Y. Regulatory T cells: mechanisms of differentiation and function. Annu. Rev. Immunol. 30, 531-564 (2012).
3. Romagnoli, P. , Hudrisier, D. & van Meerwijk, J. P. M. Preferential recognition of self-antigens despite normal thymic deletion of CD4+CD25+ regulatory T cells. J. Immunol. 168, 1644-1648 (2002).
4. Hsieh, C. S. et al. Recognition of the peripheral self by naturally arising CD25+ CD4+ T cell receptors. Immunity 21, 267-277 (2004).
5. Chidgey, A. , Dudakov, J. , Seach, N. & Boyd, R. Impact of niche aging on thymic regeneration and immune reconstitution. Semin. Immunol. 19, 331-340 (2007).
6. Nikolich-Žugich, J. Ageing and life-long maintenance of T-cell subsets in the face of latent persistent infections. Nat. Rev. Immunol. 8, 512-522 (2008).
7. Yu, W. et al. Continued RAG expression in late stages of B cell development and no apparent re-induction after immunization. Nature 400, 682-687 (1999).
8. Borgulya, P. , Kishi, H. , Uematsu, Y. & von Boehmer, H. Exclusion and inclusion of alpha and beta T cell receptor alleles. Cell 69, 529-537 (1992).
9. McCaughtry, T. M. , Wilken, M. S. & Hogquist, K. A. Thymic emigration revisited. J. Exp. Med. 204, 2513-2520 (2007).
10. Liston, A. et al. Differentiation of regulatory Foxp3+ T cells in the thymic cortex. Proc. Natl. Acad. Sci. USA 105, 11903-11908 (2008).
11. Almeida, A. R. et al. Quorum-sensing in CD4+ T cell homeostasis: a hypothesis and a model. Front Immunol. 3, 125 (2012).
12. Liston, A. & Gray, D. H. Homeostatic control of regulatory T cell diversity. Nat. Rev. Immunol. 14, 154-165 (2014).
13. Cuss, S. M. & Green, E. A. Abrogation of CD40-CD154 signaling impedes the homeostasis of thymic resident regulatory T cells by altering the levels of IL-2, but does not affect regulatory T cell development. J. Immunol. 189, 1717-1725 (2012).
14. Yang, E. , Zou, T. , Leichner, T. M. , Zhang, S. L. & Kambayashi, T. Both retention and recirculation contribute to long-lived regulatory T-cell accumulation in the thymus. Eur. J. Immunol. 44, 2712-2720 (2014).
15. Attridge, K. & Walker, L. S. Homeostasis and function of regulatory T cells (Tregs) in vivo: lessons from TCR-transgenic Tregs. Immunol. Rev. 259, 23-39 (2014).
16. Fink, P. J. , Swan, K. , Turk, G. , Moore, M. W. & Carbone, F. R. Both intrathymic and peripheral selection modulate the differential expression of V5 among CD4+ and CD8+ T cells. J. Exp. Med. 176, 1733-1738 (1992).
17. McMahan, C. J. & Fink, P. J. RAG reexpression and DNA recombination at T cell receptor loci in peripheral CD4+ T cells. Immunity 9, 637-647 (1998).
18. Papiernik, M. , de Moraes, M. L. , Pontoux, C. , Vasseur, F. & Penit, C. Regulatory CD4 T cells: Expression of IL-2R chain, resistance to clonal deletion and IL-2 dependency. Int. Immunol. 10, 371-378 (1998).
19. Zhan, Y. , Corbett, A. J. , Brady, J. L. , Sutherland, R. M. & Lew, A. M. Delayed rejection of fetal pig pancreas in CD4 cell deficient mice was correlated with residual helper activity. Xenotransplantation 7, 267-274 (2000).
20. Agus, D. B. , Surh, C. D. & Sprent, J. Re-entry of T cells to the adult thymus is restricted to activated T cells. J. Exp. Med. 173, 1039-1046 (1991).
21. Leng, Q. , Nie, Y. , Zou, Y. & Chen, J. Elevated CXCL12 expression in the bone marrow of NOD mice is associated with altered T cell and stem cell trafficking and diabetes development. BMC Immunol. 9, 51 (2008).
22. Bajoghli, B. et al. Evolution of genetic networks underlying the emergence of thymopoiesis in vertebrates. Cell 138, 186-197 (2009).
23. Joller, N. et al. Treg cells expressing the coinhibitory molecule TIGIT selectively inhibit proinflammatory Th1 and Th17 cell responses. Immunity 40, 569-581 (2014).
24. Lee, H. M. & Hsieh, C. S. Rare development of Foxp3+ thymocytes in the CD4+CD8+ subset. J. Immunol. 183, 2261-2266 (2009).
25. Pandiyan, P. , Zheng, L. , Ishihara, S. , Reed, J. & Lenardo, M. J. CD4+CD25+Foxp3+ regulatory T cells induce cytokine deprivation-mediated apoptosis of effector CD4+ T cells. Nat. Immunol. 8, 1353-1362 (2007).
26. Cheng, G. , Yu, A. & Malek, T. R. T-cell tolerance and the multi-functional role of IL-2R signaling in T-regulatory cells. Immunol. Rev. 241, 63-76 (2011).
27. Lio, C. W. & Hsieh, C. S. A two-step process for thymic regulatory T cell development. Immunity 28, 100-111 (2008).
28. Kimmig, S. et al. Two subsets of naive Thelper cells with distinct T cell receptor excision circle content in human adult peripheral blood. J. Exp. Med. 195, 789-794 (2002).
29. Miyara, M. et al. Functional delineation and differentiation dynamics of human CD4+ T cells expressing the FoxP3 transcription factor. Immunity 30, 899-911 (2009).
30. Dominguez-Villar, M. , Baecher-Allan, C. M. & Hafler, D. A. Identification of Thelper type 1-like, Foxp3+ regulatory T cells in human autoimmune disease. Nat. Med. 17, 673-675 (2011).
31. Duhen, T. , Duhen, R. , Lanzavecchia, A. , Sallusto, F. & Campbell, D. J. Functionally distinct subsets of human FOXP3+ Treg cells that phenotypically mirror effector Th cells. Blood 119, 4430-4440 (2012).
32. Bosco, N. , Agenes, F. , Rolink, A. G. & Ceredig, R. Peripheral T cell lymphopenia and concomitant enrichment in naturally arising regulatory T cells: the case of the pre-T gene-deleted mouse. J. Immunol. 177, 5014-5023 (2006).
33. Romagnoli, P. et al. The thymic niche does not limit development of the naturally diverse population of mouse regulatory T lymphocytes. J. Immunol. 189, 3831-3837 (2012).
34. Smigiel, K. S. et al. CCR7 provides localized access to IL-2 and defines homeostatically distinct regulatory T cell subsets. J. Exp. Med. 211, 121-136 (2014).
35. Tai, X. et al. Foxp3 transcription factor is proapoptotic and lethal to developing regulatory T cells unless counterbalanced by cytokine survival signals. Immunity 38, 1116-1128 (2013).
36. Yasunaga, J. et al. Impaired production of naive T lymphocytes in human T-cell leukemia virus type I-infected individuals: its implications in the immunodeficient state. Blood 97, 3177-3183 (2001).
37. Pilarski, L. M. , Mant, M. J. , Ruether, B. A. & Belch, A. Severe deficiency of B lymphocytes in peripheral blood from multiple myeloma patients. J. Clin. Invest. 74, 1301-1306 (1984).
38. Fisson, S. et al. Continuous activation of autoreactive CD4+ CD25+ regulatory T cells in the steady state. J. Exp. Med. 198, 737-746 (2003).
39. Boursalian, T. E. , Golob, J. , Soper, D. M. , Cooper, C. J. & Fink, P. J. Continued maturation of thymic emigrants in the periphery. Nat. Immunol. 5, 418-425 (2004).
40. Trapnell, C. et al. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat. Protoc. 7, 562-578 (2012).
41. Anders, S. & Huber, W. Differential expression analysis for sequence count data. Genome Biol. 11, R106 (2010).
42. Pavlidis, P. & Noble, W. S. Matrix2png: a utility for visualizing matrix data. Bioinformatics 19, 295-296 (2003).
43. Cabaniols, J. P. , Fazilleau, N. , Casrouge, A. , Kourilsky, P. & Kanellopoulos, J. M. Most T cell receptor diversity is due to terminal deoxynucleotidyl transferase. J. Exp. Med. 194, 1385-1390 (2001).
44. Fazilleau, N. et al. T cell repertoire diversity is required for relapses in myelin oligodendrocyte glycoprotein-induced experimental autoimmune encephalomyelitis. J. Immunol. 178, 4865-4875 (2007).
45. Arden, B. , Clark, S. P. , Kabelitz, D. & Mak, T. W. Mouse T-cell receptor variable gene segment families. Immunogenetics 42, 501-530 (1995).