An essential role for medullary thymic epithelial cells during the intrathymic development of invariant NKT cells

Journal of Immunology

Volumn 192, Issue 6, 2014, Pages 2659-2666

  White, Andrea J ^a   Jenkinson, William E ^a   Cowan, Jennifer E ^a   Parnell, Sonia M ^a   Bacon, Andrea ^a   Jones, Nick D ^a   Jenkinson, Eric J ^a   Anderson, Graham ^a  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOIMMUNE REGULATOR PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 15; INTERLEUKIN 15 RECEPTOR ALPHA; RECEPTOR ACTIVATOR OF NUCLEAR FACTOR KAPPA B; RETINOID RELATED ORPHAN RECEPTOR GAMMA; TRANSCRIPTION FACTOR RELB;

ADAPTIVE IMMUNITY; ADULT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL COMPARTMENTALIZATION; CELL INTERACTION; CELL LINEAGE; CELL MATURATION; CELL TRANSFORMATION; COMPARATIVE STUDY; EMBRYO; EPITHELIUM CELL; FETUS; IMMUNOLOGICAL TOLERANCE; INNATE IMMUNITY; INTRACELLULAR MEMBRANE; MOLECULAR INTERACTION; MOUSE; NATURAL KILLER T CELL; NONHUMAN; PRIORITY JOURNAL; THYMOCYTE; THYMUS TRANSPLANTATION;

ANIMALS; ANTIGENS, CD1D; CELL DIFFERENTIATION; CELLULAR MICROENVIRONMENT; EPITHELIAL CELLS; FLOW CYTOMETRY; INTERLEUKIN-15; MICE, INBRED C57BL; MICE, KNOCKOUT; NATURAL KILLER T-CELLS; NUCLEAR RECEPTOR SUBFAMILY 1, GROUP F, MEMBER 3; RANK LIGAND; RECEPTOR ACTIVATOR OF NUCLEAR FACTOR-KAPPA B; RECEPTORS, INTERLEUKIN-15; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; THYMOCYTES; THYMUS GLAND; TRANSCRIPTION FACTOR RELB;

EID: 84897512352     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1303057     Document Type: Article

References (42)

1. Gallegos, A. M., and M. J. Bevan. 2006. Central tolerance: good but imperfect. Immunol. Rev. 209: 290-296.
2. Boehm, T. 2008. Thymus development and function. Curr. Opin. Immunol. 20: 178-184.
3. Takahama, Y., T. Nitta, A. Mat Ripen, S. Nitta, S. Murata, and K. Tanaka. 2010. Role of thymic cortex-specific self-peptides in positive selection of T cells. Semin. Immunol. 22: 287-293.
4. Ueno, T., F. Saito, D. H. Gray, S. Kuse, K. Hieshima, H. Nakano, T. Kakiuchi, M. Lipp, R. L. Boyd, and Y. Takahama. 2004. CCR7 signals are essential for cortex-medulla migration of developing thymocytes. J. Exp. Med. 200: 493-505.
5. Guerau-de-Arellano, M., M. Martinic, C. Benoist, and D. Mathis. 2009. Neonatal tolerance revisited: a perinatal window for Aire control of autoimmunity. J. Exp. Med. 206: 1245-1252.
6. Anderson, M. S., E. S. Venanzi, L. Klein, Z. Chen, S. P. Berzins, S. J. Turley, H. von Boehmer, R. Bronson, A. Dierich, C. Benoist, and D. Mathis. 2002. Projection of an immunological self shadow within the thymus by the Aire protein. Science 298: 1395-1401.
7. Kyewski, B., and L. Klein. 2006. A central role for central tolerance. Annu. Rev. Immunol. 24: 571-606.
8. Gray, D. H., F. Kupresanin, S. P. Berzins, M. J. Herold, L. A. O'Reilly, P. Bouillet, and A. Strasser. 2012. The BH3-only proteins Bim and Puma cooperate to impose deletional tolerance of organ-specific antigens. Immunity 37: 451-462.
9. Anderson, G., and Y. Takahama. 2012. Thymic epithelial cells: working class heroes for T cell development and repertoire selection. Trends Immunol. 33: 256-263.
10. Godfrey, D. I., S. Stankovic, and A. G. Baxter. 2010. Raising the NKT cell family. Nat. Immunol. 11: 197-206.
11. Liu, Y., R. D. Goff, D. Zhou, J. Mattner, B. A. Sullivan, A. Khurana, C. Cantu, III, E. V. Ravkov, C. C. Ibegbu, J. D. Altman, et al. 2006. A modified a-galactosyl ceramide for staining and stimulating natural killer T cells. J. Immunol. Methods 312: 34-39.
12. Engel, I., and M. Kronenberg. 2012. Making memory at birth: understanding the differentiation of natural killer T cells. Curr. Opin. Immunol. 24: 184-190.
13. Brigl, M., and M. B. Brenner. 2004. CD1: antigen presentation and T cell function. Annu. Rev. Immunol. 22: 817-890.
14. Coles, M. C., and D. H. Raulet. 1994. Class I dependence of the development of CD4+ CD82 NK1.1+ thymocytes. J. Exp. Med. 180: 395-399.
15. Ohteki, T., and H. R. MacDonald. 1994. Major histocompatibility complex class I related molecules control the development of CD4+82 and CD4282 subsets of natural killer 1.1+ T cell receptor-α/β+ cells in the liver of mice. J. Exp. Med. 180: 699-704.
16. Bendelac, A. 1995. Positive selection of mouse NK1+ T cells by CD1-expressing cortical thymocytes. J. Exp. Med. 182: 2091-2096.
17. Gapin, L., J. L. Matsuda, C. D. Surh, and M. Kronenberg. 2001. NKT cells derive from double-positive thymocytes that are positively selected by CD1d. Nat. Immunol. 2: 971-978.
18. Berzins, S. P., F. W. McNab, C. M. Jones, M. J. Smyth, and D. I. Godfrey. 2006. Long-term retention of mature NK1.1+ NKT cells in the thymus. J. Immunol. 176: 4059-4065.
19. Drennan, M. B., A. S. Franki, P. Dewint, K. Van Beneden, S. Seeuws, S. A. van de Pavert, E. C. Reilly, G. Verbruggen, T. E. Lane, R. E. Mebius, et al. 2009. Cutting edge: the chemokine receptor CXCR3 retains invariant NK T cells in the thymus. J. Immunol. 183: 2213-2216.
20. Michel, M. L., D. Mendes-da-Cruz, A. C. Keller, M. Lochner, E. Schneider, M. Dy, G. Eberl, and M. C. Leite-de-Moraes. 2008. Critical role of ROR-gt in a new thymic pathway leading to IL-17-producing invariant NKT cell differentiation. Proc. Natl. Acad. Sci. USA 105: 19845-19850.
21. Weih, F., D. Carrasco, S. K. Durham, D. S. Barton, C. A. Rizzo, R. P. Ryseck, S. A. Lira, and R. Bravo. 1995. Multiorgan inflammation and hematopoietic abnormalities in mice with a targeted disruption of Rel B, a member of the NF-kB/Rel family. Cell 80: 331-340.
22. Mendiratta, S. K., W. D. Martin, S. Hong, A. Boesteanu, S. Joyce, and L. Van Kaer. 1997. CD1d1 mutant mice are deficient in natural T cells that promptly produce IL-4. Immunity 6: 469-477.
23. Mak, T. W., A. Shahinian, S. K. Yoshinaga, A. Wakeham, L. M. Boucher, M. Pintilie, G. Duncan, B. U. Gajewska, M. Gronski, U. Eriksson, et al. 2003. Costimulation through the inducible costimulator ligand is essential for both T helper and B cell functions in T cell-dependent B cell responses. Nat. Immunol. 4: 765-772.
24. Borriello, F., M. P. Sethna, S. D. Boyd, A. N. Schweitzer, E. A. Tivol, D. Jacoby, T. B. Strom, E. M. Simpson, G. J. Freeman, and A. H. Sharpe. 1997. B7-1 and B7-2 have overlapping, critical roles in immunoglobulin class switching and germinal center formation. Immunity 6: 303-313.
25. Desanti, G. E., J. E. Cowan, S. Baik, S. M. Parnell, A. J. White, J. M. Penninger, P. J. Lane, E. J. Jenkinson, W. E. Jenkinson, and G. Anderson. 2012. Developmentally regulated availability of RANKL and CD40 ligand reveals distinct mechanisms of fetal and adult cross-talk in the thymus medulla. J. Immunol. 189: 5519-5526.
26. Cowan, J. E., S. M. Parnell, K. Nakamura, J. H. Caamano, P. J. Lane, E. J. Jenkinson, W. E. Jenkinson, and G. Anderson. 2013. The thymic medulla is required for Foxp3+ regulatory but not conventional CD4+ thymocyte development. J. Exp. Med. 210: 675-681.
27. Roberts, N. A., A. J. White, W. E. Jenkinson, G. Turchinovich, K. Nakamura, D. R. Withers, F. M. McConnell, G. E. Desanti, C. Benezech, S. M. Parnell, et al. 2012. Rank signaling links the development of invariant γδ T cell progenitors and Aire+ medullary epithelium. Immunity 36: 427-437.
28. Stoklasek, T. A., K. S. Schluns, and L. Lefrançois. 2006. Combined IL-15/IL-15Ra immunotherapy maximizes IL-15 activity in vivo. J. Immunol. 177: 6072-6080.
29. Williams, J. A., J. M. Lumsden, X. Yu, L. Feigenbaum, J. J. Zhang, S. M. Steinberg, and R. J. Hodes. 2008. Regulation of thymic NKT cell development by the B7-CD28 costimulatory pathway. J. Immunol. 181: 907-917.
30. Chung, Y., R. Nurieva, E. Esashi, Y. H. Wang, D. Zhou, L. Gapin, and C. Dong. 2008. A critical role of costimulation during intrathymic development of invariant NK T cells. J. Immunol. 180: 2276-2283.
31. Rossi, S. W., M. Y. Kim, A. Leibbrandt, S. M. Parnell, W. E. Jenkinson, S. H. Glanville, F. M. McConnell, H. S. Scott, J. M. Penninger, E. J. Jenkinson, et al. 2007. RANK signals from CD4+32 inducer cells regulate development of Aire-expressing epithelial cells in the thymic medulla. J. Exp. Med. 204: 1267-1272.
32. Gäbler, J., J. Arnold, and B. Kyewski. 2007. Promiscuous gene expression and the developmental dynamics of medullary thymic epithelial cells. Eur. J. Immunol. 37: 3363-3372.
33. Matsuda, J. L., L. Gapin, S. Sidobre, W. C. Kieper, J. T. Tan, R. Ceredig, C. D. Surh, and M. Kronenberg. 2002. Homeostasis of Vα14i NKT cells. Nat. Immunol. 3: 966-974.
34. Castillo, E. F., L. F. Acero, S. W. Stonier, D. Zhou, and K. S. Schluns. 2010. Thymic and peripheral microenvironments differentially mediate development and maturation of iNKT cells by IL-15 transpresentation. Blood 116: 2494-2503.
35. Chang, C. L., Y. G. Lai, M. S. Hou, P. L. Huang, and N. S. Liao. 2011. IL-15Ra of radiation-resistant cells is necessary and sufficient for thymic invariant NKT cell survival and functional maturation. J. Immunol. 187: 1235-1242.
36. Akiyama, T., Y. Shimo, H. Yanai, J. Qin, D. Ohshima, Y. Maruyama, Y. Asaumi, J. Kitazawa, H. Takayanagi, J. M. Penninger, et al. 2008. The tumor necrosis factor family receptors RANK and CD40 cooperatively establish the thymic medullary microenvironment and self-tolerance. Immunity 29: 423-437.
37. Hikosaka, Y., T. Nitta, I. Ohigashi, K. Yano, N. Ishimaru, Y. Hayashi, M. Matsumoto, K. Matsuo, J. M. Penninger, H. Takayanagi, et al. 2008. The cytokine RANKL produced by positively selected thymocytes fosters medullary thymic epithelial cells that express autoimmune regulator. Immunity 29: 438-450.
38. Elewaut, D., R. B. Shaikh, K. J. Hammond, H. DeWinter, A. J. Leishman, S. Sidobre, O. Turovskaya, T. I. Prigozy, L. Ma, T. A. Banks, et al. 2003. NIK-dependent RelB activation defines a unique signaling pathway for the development of Va14i NKT cells. J. Exp. Med. 197: 1623-1633.
39. Sivakumar, V., K. J. Hammond, N. Howells, K. Pfeffer, and F. Weih. 2003. Differential requirement for Rel/nuclear factor kB family members in natural killer T cell development. J. Exp. Med. 197: 1613-1621.
40. Lkhagvasuren, E., M. Sakata, I. Ohigashi, and Y. Takahama. 2013. Lymphotoxin β receptor regulates the development of CCL21-expressing subset of postnatal medullary thymic epithelial cells. J. Immunol. 190: 5110-5117.
41. Yano, M., N. Kuroda, H. Han, M. Meguro-Horike, Y. Nishikawa, H. Kiyonari, K. Maemura, Y. Yanagawa, K. Obata, S. Takahashi, et al. 2008. Aire controls the differentiation program of thymic epithelial cells in the medulla for the establishment of self-tolerance. J. Exp. Med. 205: 2827-2838.
42. White, A. J., D. R. Withers, S. M. Parnell, H. S. Scott, D. Finke, P. J. Lane, E. J. Jenkinson, and G. Anderson. 2008. Sequential phases in the development of Aireexpressing medullary thymic epithelial cells involve distinct cellular input. Eur. J. Immunol. 38: 942-947.