Development of invariant natural killer T cells

Current Opinion in Immunology

Volumn 39, Issue , 2016, Pages 68-74

  Gapin, Laurent ^a  

^a UNIVERSITY OF COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR; CYTOKINE; T LYMPHOCYTE RECEPTOR; TRANSCRIPTION FACTOR;

CELL COMMUNICATION; CELLULAR DISTRIBUTION; CYTOKINE RELEASE; HUMAN; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE FUNCTION; MOLECULAR RECOGNITION; NATURAL KILLER T CELL; NONHUMAN; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION; T LYMPHOCYTE SUBPOPULATION; TRANSCRIPTION REGULATION; ANIMAL; CYTOLOGY; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; THYMUS; TISSUE DISTRIBUTION;

ANIMALS; HUMANS; LYMPHOCYTE ACTIVATION; NATURAL KILLER T-CELLS; T-LYMPHOCYTE SUBSETS; THYMUS GLAND; TISSUE DISTRIBUTION; TRANSCRIPTION FACTORS;

EID: 84954518512     PISSN: 09527915     EISSN: 18790372     Source Type: Journal    
DOI: 10.1016/j.coi.2016.01.001     Document Type: Review

References (67)

1. Bendelac A., Rivera M.N., Park S.H., Roark J.H. Mouse CD1-specific NK1 T cells: development, specificity, and function. Annu Rev Immunol 1997, 15:535-562.
2. Kronenberg M. Toward an understanding of NKT cell biology: progress and paradoxes. Annu Rev Immunol 2005, 23:877-900.
3. Bendelac A., Savage P.B., Teyton L. The biology of NKT cells. Annu Rev Immunol 2007, 25:297-336.
4. Matsuda J.L., Mallevaey T., Scott-Browne J., Gapin L. CD1d-restricted iNKT cells, the 'Swiss-Army knife' of the immune system. Curr Opin Immunol 2008, 20:358-368.
5. Brennan P.J., Brigl M., Brenner M.B. Invariant natural killer T cells: an innate activation scheme linked to diverse effector functions. Nat Rev Immunol 2013, 13:101-117.
6. Lee Y.J., Holzapfel K.L., Zhu J., Jameson S.C., Hogquist K.A. Steady-state production of IL-4 modulates immunity in mouse strains and is determined by lineage diversity of iNKT cells. Nat Immunol 2013, 14:1146-1154.
7. Lee Y.J., Wang H., Starrett G.J., Phuong V., Jameson S.C., Hogquist K.A. Tissue-specific distribution of iNKT cells impacts their cytokine response. Immunity 2015, 43:566-578.
8. Gumperz J.E., Miyake S., Yamamura T., Brenner M.B. Functionally distinct subsets of CD1d-restricted natural killer T cells revealed by CD1d tetramer staining. J Exp Med 2002, 195:625-636.
9. Michel M.L., Keller A.C., Paget C., Fujio M., Trottein F., Savage P.B., Wong C.H., Schneider E., Dy M., Leite-de-Moraes M.C. Identification of an IL-17-producing NK1.1(neg) iNKT cell population involved in airway neutrophilia. J Exp Med 2007, 204:995-1001.
10. Terashima A., Watarai H., Inoue S., Sekine E., Nakagawa R., Hase K., Iwamura C., Nakajima H., Nakayama T., Taniguchi M. A novel subset of mouse NKT cells bearing the IL-17 receptor B responds to IL-25 and contributes to airway hyperreactivity. J Exp Med 2008, 205:2727-2733.
11. Doisne J.M., Becourt C., Amniai L., Duarte N., Le Luduec J.B., Eberl G., Benlagha K. Skin and peripheral lymph node invariant NKT cells are mainly retinoic acid receptor-related orphan receptor (gamma)t+ and respond preferentially under inflammatory conditions. J Immunol 2009, 183:2142-2149.
12. Chang P.P., Barral P., Fitch J., Pratama A., Ma C.S., Kallies A., Hogan J.J., Cerundolo V., Tangye S.G., Bittman R., et al. Identification of Bcl-6-dependent follicular helper NKT cells that provide cognate help for B cell responses. Nat Immunol 2012, 13:35-43.
13. Lynch L., Nowak M., Varghese B., Clark J., Hogan A.E., Toxavidis V., Balk S.P., O'Shea D., O'Farrelly C., Exley M.A. Adipose tissue invariant NKT cells protect against diet-induced obesity and metabolic disorder through regulatory cytokine production. Immunity 2012, 37:574-587.
14. Lynch L., Michelet X., Zhang S., Brennan P.J., Moseman A., Lester C., Besra G., Vomhof-Dekrey E.E., Tighe M., Koay H.F., et al. Regulatory iNKT cells lack expression of the transcription factor PLZF and control the homeostasis of T cells and macrophages in adipose tissue. Nat Immunol 2014, 16:85-95.
15. Michel M.L., Mendes-da-Cruz D., Keller A.C., Lochner M., Schneider E., Dy M., Eberl G., Leite-de-Moraes M.C. Critical role of ROR-gammat in a new thymic pathway leading to IL-17-producing invariant NKT cell differentiation. Proc Natl Acad Sci USA 2008, 105:19845-19850.
16. Watarai H., Sekine-Kondo E., Shigeura T., Motomura Y., Yasuda T., Satoh R., Yoshida H., Kubo M., Kawamoto H., Koseki H., Taniguchi M. Development and function of invariant natural killer T cells producing T(h)2- and T(h)17-cytokines. PLoS Biol 2012, 10:e1001255.
17. Sag D., Krause P., Hedrick C.C., Kronenberg M., Wingender G. IL-10-producing NKT10 cells are a distinct regulatory invariant NKT cell subset. J Clin Invest 2014, 124:3725-3740.
18. Chiu Y.H., Park S.H., Benlagha K., Forestier C., Jayawardena-Wolf J., Savage P.B., Teyton L., Bendelac A. Multiple defects in antigen presentation and T cell development by mice expressing cytoplasmic tail-truncated CD1d. Nat Immunol 2002, 3:55-60.
19. Gapin L., Godfrey D.I., Rossjohn J. Natural killer T cell obsession with self-antigens. Curr Opin Immunol 2013, 25:168-173.
20. Zhou D., Mattner J., Cantu C., Schrantz N., Yin N., Gao Y., Sagiv Y., Hudspeth K., Wu Y.P., Yamashita T., et al. Lysosomal glycosphingolipid recognition by NKT cells. Science 2004, 306:1786-1789.
21. Brennan P.J., Tatituri R.V., Brigl M., Kim E.Y., Tuli A., Sanderson J.P., Gadola S.D., Hsu F.F., Besra G.S., Brenner M.B. Invariant natural killer T cells recognize lipid self antigen induced by microbial danger signals. Nat Immunol 2011, 12:1202-1211.
22. Facciotti F., Ramanjaneyulu G.S., Lepore M., Sansano S., Cavallari M., Kistowska M., Forss-Petter S., Ni G., Colone A., Singhal A., et al. Peroxisome-derived lipids are self antigens that stimulate invariant natural killer T cells in the thymus. Nat Immunol 2012, 13:474-480.
23. Lairson L.L., Henrissat B., Davies G.J., Withers S.G. Glycosyltransferases: structures, functions, and mechanisms. Annu Rev Biochem 2008, 77:521-555.
24. Brennan P.J., Tatituri R.V., Heiss C., Watts G.F., Hsu F.F., Veerapen N., Cox L.R., Azadi P., Besra G.S., Brenner M.B. Activation of iNKT cells by a distinct constituent of the endogenous glucosylceramide fraction. Proc Natl Acad Sci USA 2014, 111:13433-13438.
25. Kain L., Webb B., Anderson B.L., Deng S., Holt M., Costanzo A., Zhao M., Self K., Teyton A., Everett C., et al. The identification of the endogenous ligands of natural killer T cells reveals the presence of mammalian alpha-linked glycosylceramides. Immunity 2014, 41:543-554.
26. Kain L., Costanzo A., Webb B., Holt M., Bendelac A., Savage P.B., Teyton L. Endogenous ligands of natural killer T cells are alpha-linked glycosylceramides. Mol Immunol 2015, 68:94-97.
27. Wun K.S., Cameron G., Patel O., Pang S.S., Pellicci D.G., Sullivan L.C., Keshipeddy S., Young M.H., Uldrich A.P., Thakur M.S., et al. A molecular basis for the exquisite CD1d-restricted antigen specificity and functional responses of natural killer T cells. Immunity 2011, 34:327-339.
28. Bendelac A. Positive selection of mouse NK1+ T cells by CD1-expressing cortical thymocytes. J Exp Med 1995, 182:2091-2096.
29. Li W., Sofi M.H., Rietdijk S., Wang N., Terhorst C., Chang C.H. The SLAM-associated protein signaling pathway is required for development of CD4+ T cells selected by homotypic thymocyte interaction. Immunity 2007, 27:763-774.
30. Griewank K., Borowski C., Rietdijk S., Wang N., Julien A., Wei D.G., Mamchak A.A., Terhorst C., Bendelac A. Homotypic interactions mediated by Slamf1 and Slamf6 receptors control NKT cell lineage development. Immunity 2007, 27:751-762.
31. Godfrey D.I., Berzins S.P. Control points in NKT-cell development. Nat Rev Immunol 2007, 7:505-518.
32. Moran A.E., Holzapfel K.L., Xing Y., Cunningham N.R., Maltzman J.S., Punt J., Hogquist K.A. T cell receptor signal strength in Treg and iNKT cell development demonstrated by a novel fluorescent reporter mouse. J Exp Med 2011, 208:1279-1289.
33. Bedel R., Berry R., Mallevaey T., Matsuda J.L., Zhang J., Godfrey D.I., Rossjohn J., Kappler J.W., Marrack P., Gapin L. Effective functional maturation of invariant natural killer T cells is constrained by negative selection and T-cell antigen receptor affinity. Proc Natl Acad Sci USA 2014, 111:E119-E128.
34. Hu T., Gimferrer I., Simmons A., Wiest D., Alberola-Ila J. The Ras/MAPK pathway is required for generation of iNKT cells. PLoS ONE 2011, 6:e19890.
35. Seiler M.P., Mathew R., Liszewski M.K., Spooner C.J., Barr K., Meng F., Singh H., Bendelac A. Elevated and sustained expression of the transcription factors Egr1 and Egr2 controls NKT lineage differentiation in response to TCR signaling. Nat Immunol 2012, 13:264-271.
36. Lazarevic V., Zullo A.J., Schweitzer M.N., Staton T.L., Gallo E.M., Crabtree G.R., Glimcher L.H. The gene encoding early growth response 2, a target of the transcription factor NFAT, is required for the development and maturation of natural killer T cells. Nat Immunol 2009, 10:306-313.
37. Dutta M., Kraus Z.J., Gomez-Rodriguez J., Hwang S.H., Cannons J.L., Cheng J., Lee S.Y., Wiest D.L., Wakeland E.K., Schwartzberg P.L. A role for Ly108 in the induction of promyelocytic zinc finger transcription factor in developing thymocytes. J Immunol 2013, 190:2121-2128.
38. Kovalovsky D., Uche O.U., Eladad S., Hobbs R.M., Yi W., Alonzo E., Chua K., Eidson M., Kim H.J., Im J.S., et al. The BTB-zinc finger transcriptional regulator PLZF controls the development of invariant natural killer T cell effector functions. Nat Immunol 2008, 9:1055-1064.
39. Savage A.K., Constantinides M.G., Han J., Picard D., Martin E., Li B., Lantz O., Bendelac A. The transcription factor PLZF directs the effector program of the NKT cell lineage. Immunity 2008, 29:391-403.
40. Zhang S., Laouar A., Denzin L.K., Sant'Angelo D.B. Zbtb16 (PLZF) is stably suppressed and not inducible in non-innate T cells via T cell receptor-mediated signaling. Sci Rep 2015, 5:12113.
41. Wei G., Wei L., Zhu J., Zang C., Hu-Li J., Yao Z., Cui K., Kanno Y., Roh T.Y., Watford W.T., et al. Global mapping of H3K4me3 and H3K27me3 reveals specificity and plasticity in lineage fate determination of differentiating CD4+ T cells. Immunity 2009, 30:155-167.
42. Zhang J.A., Mortazavi A., Williams B.A., Wold B.J., Rothenberg E.V. Dynamic transformations of genome-wide epigenetic marking and transcriptional control establish T cell identity. Cell 2012, 149:467-482.
43. Dobenecker M.W., Kim J.K., Marcello J., Fang T.C., Prinjha R., Bosselut R., Tarakhovsky A. Coupling of T cell receptor specificity to natural killer T cell development by bivalent histone H3 methylation. J Exp Med 2015, 212:297-306.
44. Pereira R.M., Martinez G.J., Engel I., Cruz-Guilloty F., Barboza B.A., Tsagaratou A., Lio C.W., Berg L.J., Lee Y., Kronenberg M., et al. Jarid2 is induced by TCR signalling and controls iNKT cell maturation. Nat Commun 2014, 5:4540.
45. Benlagha K., Wei D.G., Veiga J., Teyton L., Bendelac A. Characterization of the early stages of thymic NKT cell development. J Exp Med 2005, 202:485-492.
46. Constantinides M.G., McDonald B.D., Verhoef P.A., Bendelac A. A committed precursor to innate lymphoid cells. Nature 2014, 508:397-401.
47. White A.J., Jenkinson W.E., Cowan J.E., Parnell S.M., Bacon A., Jones N.D., Jenkinson E.J., Anderson G. An essential role for medullary thymic epithelial cells during the intrathymic development of invariant NKT cells. J Immunol 2014, 192:2659-2666.
48. Godfrey D.I., Stankovic S., Baxter A.G. Raising the NKT cell family. Nat Immunol 2010, 11:197-206.
49. Constantinides M.G., Bendelac A. Transcriptional regulation of the NKT cell lineage. Curr Opin Immunol 2013, 25:161-167.
50. Kim E.Y., Lynch L., Brennan P.J., Cohen N.R., Brenner M.B. The transcriptional programs of iNKT cells. Semin Immunol 2015, 27(1):26-32.
51. Fedeli M., Napolitano A., Wong M.P., Marcais A., de Lalla C., Colucci F., Merkenschlager M., Dellabona P., Casorati G. Dicer-dependent microRNA pathway controls invariant NKT cell development. J Immunol 2009, 183:2506-2512.
52. Seo K.H., Zhou L., Meng D., Xu J., Dong Z., Mi Q.S. Loss of microRNAs in thymus perturbs invariant NKT cell development and function. Cell Mol Immunol 2010, 7:447-453.
53. Pobezinsky L.A., Etzensperger R., Jeurling S., Alag A., Kadakia T., McCaughtry T.M., Kimura M.Y., Sharrow S.O., Guinter T.I., Feigenbaum L., Singer A. Let-7 microRNAs target the lineage-specific transcription factor PLZF to regulate terminal NKT cell differentiation and effector function. Nat Immunol 2015, 16:517-524.
54. Henao-Mejia J., Williams A., Goff L.A., Staron M., Licona-Limon P., Kaech S.M., Nakayama M., Rinn J.L., Flavell R.A. The microRNA miR-181 is a critical cellular metabolic rheostat essential for NKT cell ontogenesis and lymphocyte development and homeostasis. Immunity 2013, 38:984-997.
55. Zietara N., Lyszkiewicz M., Witzlau K., Naumann R., Hurwitz R., Langemeier J., Bohne J., Sandrock I., Ballmaier M., Weiss S., et al. Critical role for miR-181a/b-1 in agonist selection of invariant natural killer T cells. Proc Natl Acad Sci USA 2013, 110:7407-7412.
56. Shin J., Wang S., Deng W., Wu J., Gao J., Zhong X.P. Mechanistic target of rapamycin complex 1 is critical for invariant natural killer T-cell development and effector function. Proc Natl Acad Sci USA 2014, 111:E776-E783.
57. Prevot N., Pyaram K., Bischoff E., Sen J.M., Powell J.D., Chang C.H. Mammalian target of rapamycin complex 2 regulates invariant NK T cell development and function independent of promyelocytic leukemia zinc-finger. J Immunol 2014, 194:223-230.
58. Salio M., Puleston D.J., Mathan T.S., Shepherd D., Stranks A.J., Adamopoulou E., Veerapen N., Besra G.S., Hollander G.A., Simon A.K., Cerundolo V. Essential role for autophagy during invariant NKT cell development. Proc Natl Acad Sci USA 2014, 111:E5678-E5687.
59. Verykokakis M., Krishnamoorthy V., Iavarone A., Lasorella A., Sigvardsson M., Kee B.L. Essential functions for ID proteins at multiple checkpoints in invariant NKT cell development. J Immunol 2013, 191:5973-5983.
60. D'Cruz L.M., Stradner M.H., Yang C.Y., Goldrath A.W. E and Id proteins influence invariant NKT cell sublineage differentiation and proliferation. J Immunol 2014, 192:2227-2236.
61. Hu T., Wang H., Simmons A., Bajana S., Zhao Y., Kovats S., Sun X.H., Alberola-Ila J. Increased level of E protein activity during invariant NKT development promotes differentiation of invariant NKT2 and invariant NKT17 subsets. J Immunol 2013, 191:5065-5073.
62. Oh S.J., Ahn S., Jin Y.H., Ishifune C., Kim J.H., Yasutomo K., Chung D.H. Notch 1 and Notch 2 synergistically regulate the differentiation and function of invariant NKT cells. J Leukoc Biol 2015, 98:781-789.
63. Carr T., Krishnamoorthy V., Yu S., Xue H.H., Kee B.L., Verykokakis M. The transcription factor lymphoid enhancer factor 1 controls invariant natural killer T cell expansion and Th2-type effector differentiation. J Exp Med 2015, 212:793-807.
64. De Calisto J., Wang N., Wang G., Yigit B., Engel P., Terhorst C. SAP-dependent and -independent regulation of innate T cell development involving SLAMF receptors. Front Immunol 2014, 5:186.
65. Sintes J., Cuenca M., Romero X., Bastos R., Terhorst C., Angulo A., Engel P. Cutting edge: Ly9 (CD229), a SLAM family receptor, negatively regulates the development of thymic innate memory-like CD8+ T and invariant NKT cells. J Immunol 2013, 190:21-26.
66. Nichols K.E., Hom J., Gong S.Y., Ganguly A., Ma C.S., Cannons J.L., Tangye S.G., Schwartzberg P.L., Koretzky G.A., Stein P.L. Regulation of NKT cell development by SAP, the protein defective in XLP. Nat Med 2005, 11:340-345.
67. Cowan J.E., McCarthy N.I., Parnell S.M., White A.J., Bacon A., Serge A., Irla M., Lane P.J., Jenkinson E.J., Jenkinson W.E., Anderson G. Differential requirement for CCR4 and CCR7 during the development of innate and adaptive alphabetaT cells in the adult thymus. J Immunol 2014, 193:1204-1212.