IL-17-producing NKT cells depend exclusively on IL-7 for homeostasis and survival

Mucosal Immunology

Volumn 7, Issue 5, 2014, Pages 1058-1067

  Webster, K E ^a,b   Kim, H O ^a   Kyparissoudis, K ^c   Corpuz, T M ^a   Pinget, G V ^a   Uldrich, A P ^c   Brink, R ^a,b   Belz, G T ^c,d   Cho, J H ^a,b   Godfrey, D I ^c   Sprent, J ^a,b,e  

^a GARVAN INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b UNIVERSITY OF NEW SOUTH WALES   (Australia)

^c UNIVERSITY OF MELBOURNE   (Australia)

^d WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^e Pohang University of Science and Technology (POSTECH)   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 15; INTERLEUKIN 17; INTERLEUKIN 2; INTERLEUKIN 7; INTERLEUKIN 7 RECEPTOR ALPHA; MAMMALIAN TARGET OF RAPAMYCIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; RETINOID RELATED ORPHAN RECEPTOR GAMMA; STAT3 PROTEIN; STAT5 PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING 1; SUPPRESSOR OF CYTOKINE SIGNALING 3; T LYMPHOCYTE RECEPTOR; CD4 ANTIGEN; RETINOID RELATED ORPHAN RECEPTOR GAMMA T; STAT PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CD4+ T LYMPHOCYTE; CELL EXPANSION; CELL SURVIVAL; CONTROLLED STUDY; DOWN REGULATION; HOMEOSTASIS; IMMUNE RESPONSE; INTERLEUKIN 17 PRODUCING NATURAL KILLER T CELL; LYMPHOCYTE PROLIFERATION; MOUSE; NATURAL KILLER T CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN TRANSPORT; RECEPTOR DENSITY; SIGNAL TRANSDUCTION; TH17 CELL; ANIMAL; CELL PROLIFERATION; CYTOLOGY; FLOW CYTOMETRY; IMMUNOLOGY; INTRAPERITONEAL DRUG ADMINISTRATION; METABOLISM; POLYMERASE CHAIN REACTION; CELL LINEAGE; CYTOKINE PRODUCTION; LUNG; LYMPHOCYTE FUNCTION; LYMPHOID CELL; PROTEIN ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; RECEPTOR DOWN REGULATION; SKIN;

ANIMALS; CELL PROLIFERATION; FLOW CYTOMETRY; HOMEOSTASIS; INJECTIONS, INTRAPERITONEAL; INTERLEUKIN-17; INTERLEUKIN-7; MICE; NATURAL KILLER T-CELLS; POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

EID: 84906349903     PISSN: 19330219     EISSN: 19353456     Source Type: Journal    
DOI: 10.1038/mi.2013.122     Document Type: Article

References (51)

1. Kinjo, Y. et al. Invariant natural killer T cells recognize glycolipids from pathogenic Gram-positive bacteria. Nat. Immunol. 12, 966-974 (2011).
2. Brigl, M. et al. Innate and cytokine-driven signals, rather than microbial antigens, dominate in natural killer T cell activation during microbial infection. J. Exp. Med. 208, 1163-1177 (2011).
3. Zeissig, S. et al. Hepatitis B virus-induced lipid alterations contribute to natural killer T cell-dependent protective immunity. Nat. Med. 18, 1060-1068 (2012).
4. Coquet, J.M. et al. Diverse cytokine production by NKT cell subsets and identification of an IL-17-producing CD4-NK1.1- NKT cell population. Proc. Natl Acad. Sci. USA 105, 11287-11292 (2008).
5. Michel, M.L. et al. Identification of an IL-17-producing NK1.1(neg) iNKTcell population involved in airway neutrophilia. J. Exp. Med. 204, 995-1001 (2007).
6. Moreira-Teixeira, L. et al. Proinflammatory environment dictates the IL-17-producing capacity of human invariant NKT cells. J. Immunol. 186, 5758-5765 (2011).
7. Rachitskaya, A.V. et al. Cutting edge: NKTcells constitutively express IL-23 receptor and RORgammat and rapidly produce IL-17 upon receptor ligation in an IL-6-independent fashion. J. Immunol. 180, 5167-5171 (2008).
8. Doisne, J.M. et al. Skin and peripheral lymph node invariant NKTcells are mainly retinoic acid receptor-related orphan receptor (gamma)t+ and respond preferentially under inflammatory conditions. J. Immunol. 183, 2142-2149 (2009).
9. Doisne, J.M. et al. Cutting edge: crucial role of IL-1 and IL-23 in the innate IL-17 response of peripheral lymph node NK1.1- invariant NKT cells to bacteria. J. Immunol. 186, 662-666 (2011).
10. Korn, T.,Bettelli, E.,Oukka, M. & Kuchroo, V.K. IL-17 and Th17 Cells. Annu. Rev. Immunol. 27, 485-517 (2009).
11. Pichavant, M. et al. Ozone exposure in a mouse model induces airway hyperreactivity that requires the presence of natural killer Tcells and IL-17. J. Exp. Med. 205, 385-393 (2008).
12. Price, A.E., Reinhardt, R.L., Liang, H.E. & Locksley, R.M. Marking and quantifying IL-17A-producing cells in vivo. PloS one 7, e39750 (2012).
13. Michel, M.L. et al. Critical role of ROR-gammat in a new thymic pathway leading to IL-17-producing invariant NKT cell differentiation. Proc. Natl Acad. Sci. USA 105, 19845-19850 (2008).
14. Engel, I., Zhao, M., Kappes, D., Taniuchi, I. & Kronenberg, M. The transcription factor Th-POK negatively regulates Th17 differentiation in Valpha14i NKT cells. Blood 120, 4524-4532 (2012).
15. Enders, A. et al. ZBTB7B (Th-POK) regulates the development of IL-17- producing CD1d-restricted mouse NKTcells. J. Immunol. 189, 5240-5249 (2012).
16. Havenar-Daughton, C., Li, S.,Benlagha, K. & Marie, J.C. Development and function of murine RORgammat+ iNKTcells are under TGF-beta signaling control. Blood 119, 3486-3494 (2012).
17. Matsuda, J.L. et al. Homeostasis of Valpha 14i NKTcells. Nat. Immunol. 3, 966-974 (2002).
18. Ranson, T. et al. IL-15 availability conditions homeostasis of peripheral natural killer T cells. Proc. Natl Acad. Sci. USA 100, 2663-2668 (2003).
19. Watarai, H. et al. Development and function of invariant natural killer Tcells producing T(h)2- and T(h)17-cytokines. PLoS Biol. 10, e1001255 (2012).
20. Dubois, S., Mariner, J.,Waldmann, T.A. & Tagaya, Y. IL-15Ralpha recycles and presents IL-15 In trans to neighboring cells. Immunity 17, 537-547 (2002).
21. Castillo, E.F., Acero, L.F., Stonier, SW, Zhou, D & Schluns, KS Thymic and peripheral microenvironments differentially mediate development and maturation of iNKT cells by IL-15 transpresentation. Blood 116, 2494-2503 (2010).
22. Boyman, O., Ramsey, C., Kim, D.M., Sprent, J. & Surh, C.D. IL-7/anti-IL-7 mAb complexes restore T cell development and induce homeostatic T Cell expansion without lymphopenia. J. Immunol. 180, 7265-7275 (2008).
23. Yang, X.P. et al. Opposing regulation of the locus encoding IL-17 through direct, reciprocal actions of STAT3 and STAT5. Nat. Immunol. 12, 247-254 (2011).
24. von Freeden-Jeffry, U., Vieira, P., Lucian, L.A., McNeil, T., Burdach, S.E. & Murray, R. Lymphopenia in interleukin (IL)-7 gene-deleted mice identifies IL-7 as a nonredundant cytokine. J. Exp. Med. 181, 1519-1526 (1995).
25. Carrette, F. & Surh, C.D. IL-7 signaling and CD127 receptor regulation in the control of T cell homeostasis. Semin. Immunol. 24, 209-217 (2012).
26. Michel, M.L., Pang, D.J., Haque, S.F., Potocnik, A.J., Pennington, D.J. & Hayday, A.C. Interleukin 7 (IL-7) selectively promotes mouse and human IL-17-producing gammadelta cells. Proc. Natl Acad. Sci. USA 109, 17549-17554 (2012).
27. Takada, K. & Jameson, S.C. Naive T cell homeostasis: from awareness of space to a sense of place. Nat. Rev. Immunol. 9, 823-832 (2009).
28. Chong, M.M. et al. Suppressor of cytokine signaling-1 is a critical regulator of interleukin-7-dependent CD8+ T cell differentiation. Immunity 18, 475-487 (2003).
29. Deane, J.A. & Fruman, D.A. Phosphoinositide 3-kinase: diverse roles in immune cell activation. Annu. Rev. Immunol. 22, 563-598 (2004).
30. Lali, F.V., Crawley, J., McCulloch, D.A. & Foxwell, B.M. A late, prolonged activation of the phosphatidylinositol 3-kinase pathway is required for Tcell proliferation. J. Immunol. 172, 3527-3534 (2004).
31. Liu, X. et al. Crucial role of interleukin-7 in T helper type 17 survival and expansion in autoimmune disease. Nat. Med. 16, 191-197 (2010).
32. Pellegrini, M. et al. IL-7 engages multiple mechanisms to overcome chronic viral infection and limit organ pathology. Cell 144, 601-613 (2011).
33. Monteiro, M., Almeida, C.F., Agua-Doce, A. & Graca, L. Induced IL-17- producing invariant NKT cells require activation in presence of TGF-beta and IL-1beta. J. Immunol. 190, 805-811 (2013).
34. Vonarbourg, C. et al. Regulated expression of nuclear receptor RORgammat confers distinct functional fates to NK cell receptor-expressing RORgammat(+) innate lymphocytes. Immunity 33, 736-751 (2010).
35. Eberl, G., Marmon, S., Sunshine, M.J., Rennert, P.D., Choi, Y. & Littman, D.R. An essential function for the nuclear receptor RORgamma(t) in the generation of fetal lymphoid tissue inducer cells. Nat. Immunol. 5, 64-73 (2004).
36. Sportes, C. et al. Phase I study of recombinant human interleukin-7 administration in subjects with refractory malignancy. Clin. Cancer Res. 16, 727-735 (2010).
37. Surh,C.D. & Sprent, J. Homeostasis of naive and memory Tcells. Immunity 29, 848-862 (2008).
38. Gordy, L.E. et al. IL-15 regulates homeostasis and terminal maturation of NKT cells. J. Immunol. 187, 6335-6345 (2011).
39. Satoh-Takayama, N. et al. IL-7 and IL-15 independently program the differentiation of intestinal CD3-NKp46+ cell subsets from Id2-dependent precursors. J. Exp. Med. 207, 273-280 (2010).
40. Fry, T.J. et al. A potential role for interleukin-7 in T-cell homeostasis. Blood 97, 2983-2990 (2001).
41. Napolitano, L.A. et al. Increased production of IL-7 accompanies HIV-1- mediated T-cell depletion: implications for T-cell homeostasis. Nat. Med. 7, 73-79 (2001).
42. Link, A. et al. Fibroblastic reticular cells in lymph nodes regulate the homeostasis of naive T cells. Nat. Immunol. 8, 1255-1265 (2007).
43. Golden-Mason, L. et al. Expression of interleukin 7 (IL-7)mRNAand protein in the normal adult human liver: implications for extrathymic T cell development. Cytokine 14, 143-151 (2001).
44. Heufler, C. et al. Interleukin 7 is produced by murine and human keratinocytes. J. Exp. Med. 178, 1109-1114 (1993).
45. Watanabe, M. et al. Interleukin 7 is produced by human intestinal epithelial cells and regulates the proliferation of intestinal mucosal lymphocytes. J. Clin. Invest. 95, 2945-2953 (1995).
46. Shalapour, S. et al. Commensal microflora and interferon-gamma promote steady-state interleukin-7 production in vivo. Eur. J. Immunol. 40, 2391-2400 (2010).
47. Repass, J.F. et al. IL7-hCD25 and IL7-Cre BAC transgenic mouse lines: new tools for analysis of IL-7 expressing cells. Genesis 47, 281-287 (2009).
48. Roye, O. et al. Dermal endothelial cells and keratinocytes produce IL-7 in vivo after human Schistosoma mansoni percutaneous infection. J. Immunol. 161, 4161-4168 (1998).
49. Sawa, Y. et al. Hepatic interleukin-7 expression regulates Tcell responses. Immunity 30, 447-457 (2009).
50. Matsuda, J.L. et al. Tracking the response of natural killer T cells to a glycolipid antigen using CD1d tetramers. J. Exp. Med. 192, 741-754 (2000).
51. Webster, K.E. et al. In vivo expansion of T reg cells with IL-2-mAb complexes: induction of resistance to EAE and long-term acceptance of islet allografts without immunosuppression. J. Exp. Med. 206, 751-760 (2009).