SAP Protein-Dependent Natural Killer T-like Cells Regulate the Development of CD8+ T Cells with Innate Lymphocyte Characteristics

Immunity

Volumn 33, Issue 2, 2010, Pages 203-215

  Verykokakis, Mihalis ^a   Boos, Markus D ^a   Bendelac, Albert ^a   Kee, Barbara L ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

Cellimmuno; Molimmuno

Indexed keywords

INHIBITOR OF DIFFERENTIATION 3; INTERLEUKIN 4; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; PROTEIN PLZF; SIGNALING LYMPHOCYTE ACTIVATION MOLECULE ASSOCIATED PROTEIN; UNCLASSIFIED DRUG; ZINC FINGER PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CD8+ T LYMPHOCYTE; CELL MATURATION; CELL POPULATION; CYTOKINE PRODUCTION; EPITHELIUM CELL; INNATE IMMUNITY; MOUSE; NATURAL KILLER T CELL; NEWBORN; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; THYMOCYTE;

ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; CELLS, CULTURED; HISTOCOMPATIBILITY ANTIGENS CLASS I; IMMUNITY, INNATE; INHIBITOR OF DIFFERENTIATION PROTEINS; INTERLEUKIN-4; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NATURAL KILLER T-CELLS; PHENOTYPE; THYMUS GLAND;

EID: 77955920553     PISSN: 10747613     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.immuni.2010.07.013     Document Type: Article

References (51)

1. Alonzo E.S., Gottschalk R.A., Das J., Egawa T., Hobbs R.M., Pandolfi P.P., Pereira P., Nichols K.E., Koretzky G.A., Jordan M.S., Sant'Angelo D.B. Development of promyelocytic zinc finger and ThPOK-expressing innate gamma delta T cells is controlled by strength of TCR signaling and Id3. J. Immunol. 2010, 184:1268-1279.
2. Atherly L.O., Lucas J.A., Felices M., Yin C.C., Reiner S.L., Berg L.J. The Tec family tyrosine kinases Itk and Rlk regulate the development of conventional CD8+ T cells. Immunity 2006, 25:79-91.
3. Azuara V., Levraud J.P., Lembezat M.P., Pereira P. A novel subset of adult gamma delta thymocytes that secretes a distinct pattern of cytokines and expresses a very restricted T cell receptor repertoire. Eur. J. Immunol. 1997, 27:544-553.
4. Bain G., Cravatt C.B., Loomans C., Alberola-Ila J., Hedrick S.M., Murre C. Regulation of the helix-loop-helix proteins, E2A and Id3, by the Ras-ERK MAPK cascade. Nat. Immunol. 2001, 2:165-171.
5. Bendelac A., Savage P.B., Teyton L. The biology of NKT cells. Annu. Rev. Immunol. 2007, 25:297-336.
6. Bosselut R. CD4/CD8-lineage differentiation in the thymus: From nuclear effectors to membrane signals. Nat. Rev. Immunol. 2004, 4:529-540.
7. Broussard C., Fleischacker C., Fleischecker C., Horai R., Chetana M., Venegas A.M., Sharp L.L., Hedrick S.M., Fowlkes B.J., Schwartzberg P.L. Altered development of CD8+ T cell lineages in mice deficient for the Tec kinases Itk and Rlk. Immunity 2006, 25:93-104.
8. Buaas F.W., Kirsh A.L., Sharma M., McLean D.J., Morris J.L., Griswold M.D., de Rooij D.G., Braun R.E. Plzf is required in adult male germ cells for stem cell self-renewal. Nat. Genet. 2004, 36:647-652.
9. Carnaud C., Lee D., Donnars O., Park S.H., Beavis A., Koezuka Y., Bendelac A. Cutting edge: Cross-talk between cells of the innate immune system: NKT cells rapidly activate NK cells. J. Immunol. 1999, 163:4647-4650.
10. Coles M.C., Raulet D.H. NK1.1+ T cells in the liver arise in the thymus and are selected by interactions with class I molecules on CD4+CD8+ cells. J. Immunol. 2000, 164:2412-2418.
11. Dai H., Wan N., Zhang S., Moore Y., Wan F., Dai Z. Cutting edge: Programmed Death-1 defines CD8+ CD122+ T cells as regulatory versus memory T cells. J. Immunol. 2010, 185:803-807.
12. Detre C., Keszei M., Romero X., Tsokos G.C., Terhorst C. SLAM family receptors and the SLAM-associated protein (SAP) modulate T cell functions. Semin. Immunopathol. 2010, 32:157-171.
13. Endharti A.T., Rifa'I M., Shi Z., Fukuoka Y., Nakahara Y., Kawamoto Y., Takeda K., Isobe K., Suzuki H. Cutting edge: CD8+CD122+ regulatory T cells produce IL-10 to suppress IFN-gamma production and proliferation of CD8+ T cells. J. Immunol. 2005, 175:7093-7097.
14. Engel I., Johns C., Bain G., Rivera R.R., Murre C. Early thymocyte development is regulated by modulation of E2A protein activity. J. Exp. Med. 2001, 194:733-745.
15. Felices M., Yin C.C., Kosaka Y., Kang J., Berg L.J. Tec kinase Itk in gammadeltaT cells is pivotal for controlling IgE production in vivo. Proc. Natl. Acad. Sci. USA 2009, 106:8308-8313.
16. Fukuyama T., Kasper L.H., Boussouar F., Jeevan T., van Deursen J., Brindle P.K. Histone acetyltransferase CBP is vital to demarcate conventional and innate CD8+ T-cell development. Mol. Cell. Biol. 2009, 29:3894-3904.
17. Green M.C. The position of luxoid in linkage group II of the mouse. J. Hered. 1961, 52:297-300.
18. 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.
19. Horai R., Mueller K.L., Handon R.A., Cannons J.L., Anderson S.M., Kirby M.R., Schwartzberg P.L. Requirements for selection of conventional and innate T lymphocyte lineages. Immunity 2007, 27:775-785.
20. Hu J., Sahu N., Walsh E., August A. Memory phenotype CD8+ T cells with innate function selectively develop in the absence of active Itk. Eur. J. Immunol. 2007, 37:2892-2899.
21. Intlekofer A.M., Takemoto N., Wherry E.J., Longworth S.A., Northrup J.T., Palanivel V.R., Mullen A.C., Gasink C.R., Kaech S.M., Miller J.D., et al. Effector and memory CD8+ T cell fate coupled by T-bet and eomesodermin. Nat. Immunol. 2005, 6:1236-1244.
22. Jones M.E., Zhuang Y. Acquisition of a functional T cell receptor during T lymphocyte development is enforced by HEB and E2A transcription factors. Immunity 2007, 27:860-870.
23. Klein L., Hinterberger M., Wirnsberger G., Kyewski B. Antigen presentation in the thymus for positive selection and central tolerance induction. Nat. Rev. Immunol. 2009, 9:833-844.
24. 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.
25. Kreslavsky T., Savage A.K., Hobbs R., Gounari F., Bronson R., Pereira P., Pandolfi P.P., Bendelac A., von Boehmer H. TCR-inducible PLZF transcription factor required for innate phenotype of a subset of gammadelta T cells with restricted TCR diversity. Proc. Natl. Acad. Sci. USA 2009, 106:12453-12458.
26. Lee Y.J., Jeon Y.K., Kang B.H., Chung D.H., Park C.G., Shin H.Y., Jung K.C., Park S.H. Generation of PLZF+ CD4+ T cells via MHC class II-dependent thymocyte-thymocyte interaction is a physiological process in humans. J. Exp. Med. 2010, 207:237-246.
27. Li W., Kim M.G., Gourley T.S., McCarthy B.P., Sant'Angelo D.B., Chang C.H. An alternate pathway for CD4 T cell development: Thymocyte-expressed MHC class II selects a distinct T cell population. Immunity 2005, 23:375-386.
28. 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.
29. Li W., Sofi M.H., Yeh N., Sehra S., McCarthy B.P., Patel D.R., Brutkiewicz R.R., Kaplan M.H., Chang C.H. Thymic selection pathway regulates the effector function of CD4 T cells. J. Exp. Med. 2007, 204:2145-2157.
30. Liao X.C., Littman D.R. Altered T cell receptor signaling and disrupted T cell development in mice lacking Itk. Immunity 1995, 3:757-769.
31. Liu G., Grifman M., Keily B., Chatterton J.E., Staal F.W., Li Q.X. Mineralocorticoid receptor is involved in the regulation of genes responsible for hepatic glucose production. Biochem. Biophys. Res. Commun. 2006, 342:1291-1296.
32. Lucas J.A., Atherly L.O., Berg L.J. The absence of Itk inhibits positive selection without changing lineage commitment. J. Immunol. 2002, 168:6142-6151.
33. Odumade O.A., Weinreich M.A., Jameson S.C., Hogquist K.A. Krüppel-like factor 2 regulates trafficking and homeostasis of gammadelta T cells. J. Immunol. 2010, 184:6060-6066.
34. Pan L., Sato S., Frederick J.P., Sun X.H., Zhuang Y. Impaired immune responses and B-cell proliferation in mice lacking the Id3 gene. Mol. Cell. Biol. 1999, 19:5969-5980.
35. Park S.H., Roark J.H., Bendelac A. Tissue-specific recognition of mouse CD1 molecules. J. Immunol. 1998, 160:3128-3134.
36. Pearce E.L., Mullen A.C., Martins G.A., Krawczyk C.M., Hutchins A.S., Zediak V.P., Banica M., DiCioccio C.B., Gross D.A., Mao C.A., et al. Control of effector CD8+ T cell function by the transcription factor Eomesodermin. Science 2003, 302:1041-1043.
37. Prince A.L., Yin C.C., Enos M.E., Felices M., Berg L.J. The Tec kinases Itk and Rlk regulate conventional versus innate T-cell development. Immunol. Rev. 2009, 228:115-131.
38. Raberger J., Schebesta A., Sakaguchi S., Boucheron N., Blomberg K.E., Berglöf A., Kolbe T., Smith C.I., Rülicke T., Ellmeier W. The transcriptional regulator PLZF induces the development of CD44 high memory phenotype T cells. Proc. Natl. Acad. Sci. USA 2008, 105:17919-17924.
39. Rifa'i M., Shi Z., Zhang S.Y., Lee Y.H., Shiku H., Isobe K., Suzuki H. CD8+CD122+ regulatory T cells recognize activated T cells via conventional MHC class I-alphabetaTCR interaction and become IL-10-producing active regulatory cells. Int. Immunol. 2008, 20:937-947.
40. Rivera R.R., Johns C.P., Quan J., Johnson R.S., Murre C. Thymocyte selection is regulated by the helix-loop-helix inhibitor protein, Id3. Immunity 2000, 12:17-26.
41. 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.
42. Schaeffer E.M., Broussard C., Debnath J., Anderson S., McVicar D.W., Schwartzberg P.L. Tec family kinases modulate thresholds for thymocyte development and selection. J. Exp. Med. 2000, 192:987-1000.
43. Schwartzberg P.L., Mueller K.L., Qi H., Cannons J.L. SLAM receptors and SAP influence lymphocyte interactions, development and function. Nat. Rev. Immunol. 2009, 9:39-46.
44. Singer A., Adoro S., Park J.H. Lineage fate and intense debate: Myths, models and mechanisms of CD4- versus CD8-lineage choice. Nat. Rev. Immunol. 2008, 8:788-801.
45. Takemoto N., Intlekofer A.M., Northrup J.T., Wherry E.J., Reiner S.L. Cutting Edge: IL-12 inversely regulates T-bet and eomesodermin expression during pathogen-induced CD8+ T cell differentiation. J. Immunol. 2006, 177:7515-7519.
46. Ueda-Hayakawa I., Mahlios J., Zhuang Y. Id3 restricts the developmental potential of gamma delta lineage during thymopoiesis. J. Immunol. 2009, 182:5306-5316.
47. Urdahl K.B., Sun J.C., Bevan M.J. Positive selection of MHC class Ib-restricted CD8(+) T cells on hematopoietic cells. Nat. Immunol. 2002, 3:772-779.
48. Veillette A., Dong Z., Latour S. Consequence of the SLAM-SAP signaling pathway in innate-like and conventional lymphocytes. Immunity 2007, 27:698-710.
49. Verykokakis M., Boos M.D., Bendelac A., Adams E.J., Pereira P., Kee B.L. Inhibitor of DNA binding 3 limits development of murine slam-associated adaptor protein-dependent " innate" gammadelta T cells. PLoS ONE 2010, 5:e9303.
50. Wei D.G., Lee H., Park S.H., Beaudoin L., Teyton L., Lehuen A., Bendelac A. Expansion and long-range differentiation of the NKT cell lineage in mice expressing CD1d exclusively on cortical thymocytes. J. Exp. Med. 2005, 202:239-248.
51. Weinreich M.A., Odumade O.A., Jameson S.C., Hogquist K.A. T cells expressing the transcription factor PLZF regulate the development of memory-like CD8(+) T cells. Nat. Immunol. 2010, in press. Published online July 4, 2010.