The SLAM-Associated Protein Signaling Pathway Is Required for Development of CD4+ T Cells Selected by Homotypic Thymocyte Interaction

Immunity

Volumn 27, Issue 5, 2007, Pages 763-774

  Li, Wei ^a   Sofi, M Hanief ^b   Rietdijk, Svend ^c   Wang, Ninghai ^c   Terhorst, Cox ^c   Chang, Cheong Hee ^b  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

CELLIMMUNO

Indexed keywords

ADAPTOR PROTEIN; CYTOKINE; GAMMA INTERFERON; INTERLEUKIN 15 RECEPTOR; INTERLEUKIN 4; PROTEIN KINASE FYN; SIGNALING LYMPHOCYTE ACTIVATION MOLECULE ASSOCIATED PROTEIN;

ANIMAL EXPERIMENT; ARTICLE; CD4+ T LYMPHOCYTE; CELL DIFFERENTIATION; CELL INTERACTION; CONTROLLED STUDY; FLOW CYTOMETRY; IMMUNE DEFICIENCY; MOUSE; NATURAL KILLER T CELL; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TH1 CELL; TH2 CELL; THYMOCYTE;

ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; CYTOKINES; FLOW CYTOMETRY; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; KILLER CELLS, NATURAL; LYMPHOCYTE ACTIVATION; MICE; MICE, TRANSGENIC; PROTEIN KINASE C; PROTO-ONCOGENE PROTEINS C-FYN; SIGNAL TRANSDUCTION; T-LYMPHOCYTE SUBSETS; THYMUS GLAND; TRANSPLANTATION CHIMERA;

EID: 36049030861     PISSN: 10747613     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.immuni.2007.10.008     Document Type: Article

References (52)

1. Cannons J.L., Yu L.J., Hill B., Mijares L.A., Dombroski D., Nichols K.E., Antonellis A., Koretzky G.A., Gardner K., and Schwartzberg P.L. SAP regulates T(H)2 differentiation and PKC-theta-mediated activation of NF-kappaB1. Immunity 21 (2004) 693-706
2. Cannons J.L., Yu L.J., Jankovic D., Crotty S., Horai R., Kirby M., Anderson S., Cheever A.W., Sher A., and Schwartzberg P.L. SAP regulates T cell-mediated help for humoral immunity by a mechanism distinct from cytokine regulation. J. Exp. Med. 203 (2006) 1551-1565
3. Chan B., Lanyi A., Song H.K., Griesbach J., Simarro-Grande M., Poy F., Howie D., Sumegi J., Terhorst C., and Eck M.J. SAP couples Fyn to SLAM immune receptors. Nat. Cell Biol. 5 (2003) 155-160
4. Choi E.Y., Jung K.C., Park H.J., Chung D.H., Song J.S., Yang S.D., Simpson E., and Park S.H. Thymocyte-thymocyte interaction for efficient positive selection and maturation of CD4 T cells. Immunity 23 (2005) 387-396
5. Chung B., Aoukaty A., Dutz J., Terhorst C., and Tan R. Signaling lymphocytic activation molecule-associated protein controls NKT cell functions. J. Immunol. 174 (2005) 3153-3157
6. Coffey A.J., Brooksbank R.A., Brandau O., Oohashi T., Howell G.R., Bye J.M., Cahn A.P., Durham J., Heath P., Wray P., et al. Host response to EBV infection in X-linked lymphoproliferative disease results from mutations in an SH2-domain encoding gene. Nat. Genet. 20 (1998) 129-135
7. Coudronniere N., Villalba M., Englund N., and Altman A. NF-kappa B activation induced by T cell receptor/CD28 costimulation is mediated by protein kinase C-theta. Proc. Natl. Acad. Sci. USA 97 (2000) 3394-3399
8. Eberl G., Lowin-Kropf B., and MacDonald H.R. Cutting edge: NKT cell development is selectively impaired in Fyn- deficient mice. J. Immunol. 163 (1999) 4091-4094
9. Engel P., Eck M.J., and Terhorst C. The SAP and SLAM families in immune responses and X-linked lymphoproliferative disease. Nat. Rev. Immunol. 3 (2003) 813-821
10. Gadue P., Morton N., and Stein P.L. The Src family tyrosine kinase Fyn regulates natural killer T cell development. J. Exp. Med. 190 (1999) 1189-1196
11. Godthelp B.C., Van Eggermond M.C., Van Tol M.J., Vossen J.M., and van den Elsen P.J. T cell immune reconstitution after allogeneic bone marrow transplantation in bare lymphocyte syndrome. Hum. Immunol. 61 (2000) 898-907
12. Graham D.B., Bell M.P., McCausland M.M., Huntoon C.J., van Deursen J., Faubion W.A., Crotty S., and McKean D.J. Ly9 (CD229)-deficient mice exhibit T cell defects yet do not share several phenotypic characteristics associated with SLAM- and SAP-deficient mice. J. Immunol. 176 (2006) 291-300
13. Griewank K., Borowski C., Rietdijk S., Julien A., Wei D.G., Mamchak A.A., Terhorst C., and Bendelac A. Homotypic interaction mediated by Ly108 and SLAM control NKT lineage differentiation. Immunity 27 (2007) 751-762 this issue
14. Howie D., Laroux F.S., Morra M., Satoskar A.R., Rosas L.E., Faubion W.A., Julien A., Rietdijk S., Coyle A.J., Fraser C., and Terhorst C. Cutting edge: The SLAM family receptor Ly108 controls T cell and neutrophil functions. J. Immunol. 174 (2005) 5931-5935
15. Jordan M.A., Fletcher J.M., Pellicci D., and Baxter A.G. Slamf1, the NKT cell control gene nkt1. J. Immunol. 178 (2007) 1618-1627
16. Kennedy M.K., Glaccum M., Brown S.N., Butz E.A., Viney J.L., Embers M., Matsuki N., Charrier K., Sedger L., Willis C.R., et al. Reversible defects in natural killer and memory CD8 T cell lineages in interleukin 15-deficient mice. J. Exp. Med. 191 (2000) 771-780
17. Klein C., Cavazzana-Calvo M., Le Deist F., Jabado N., Benkerrou M., Blanche S., Lisowska-Grospierre B., Griscelli C., and Fischer A. Bone marrow transplantation in major histocompatibility complex class II deficiency: A single-center study of 19 patients. Blood 85 (1995) 580-587
18. Latour S., Roncagalli R., Chen R., Bakinowski M., Shi X., Schwartzberg P.L., Davidson D., and Veillette A. Binding of SAP SH2 domain to FynT SH3 domain reveals a novel mechanism of receptor signalling in immune regulation. Nat. Cell Biol. 5 (2003) 149-154
19. Lewis D.B., Yu C.C., Forbush K.A., Carpenter J., Sato T.A., Grossman A., Liggitt D.H., and Perlmutter R.M. Interleukin 4 expressed in situ selectively alters thymocyte development. J. Exp. Med. 173 (1991) 89-100
20. Li W., Kim M.G., Gourley T.S., McCarthy B.P., Sant'angelo D.B., and Chang C.H. An alternate pathway for CD4 T cell development: Thymocyte-expressed MHC class II selects a distinct T cell population. Immunity 23 (2005) 375-386
21. Li W., Sofi M.H., Yeh N., Sehra S., McCarthy B.P., Patel D.R., Brutkiewicz R.R., Kaplan M.H., and Chang C.H. Thymic selection pathway regulates the effector function of CD4 T cells. J. Exp. Med. 204 (2007) 2145-2157
22. Lodolce J.P., Boone D.L., Chai S., Swain R.E., Dassopoulos T., Trettin S., and Ma A. IL-15 receptor maintains lymphoid homeostasis by supporting lymphocyte homing and proliferation. Immunity 9 (1998) 669-676
23. Ma C.S., Nichols K.E., and Tangye S.G. Regulation of Cellular and Humoral Immune Responses by the SLAM and SAP Families of Molecules. Annu. Rev. Immunol. 25 (2007) 337-379
24. Manicassamy S., Gupta S., Huang Z., and Sun Z. Protein kinase C-theta-mediated signals enhance CD4+ T cell survival by up-regulating Bcl-xL. J. Immunol. 176 (2006) 6709-6716
25. Marinova T., Altankova I., Dimitrova D., and Pomakov Y. Presence of HLA-DR immunopositive cells in human fetal thymus. Arch. Physiol. Biochem. 109 (2001) 74-79
26. Markert M.L., Alexieff M.J., Li J., Sarzotti M., Ozaki D.A., Devlin B.H., Sedlak D.A., Sempowski G.D., Hale L.P., Rice H.E., et al. Postnatal thymus transplantation with immunosuppression as treatment for DiGeorge syndrome. Blood 104 (2004) 2574-2581
27. Marsland B.J., Soos T.J., Spath G., Littman D.R., and Kopf M. Protein kinase C theta is critical for the development of in vivo T helper (Th)2 cell but not Th1 cell responses. J. Exp. Med. 200 (2004) 181-189
28. Matsuda J.L., and Gapin L. Developmental program of mouse Valpha14i NKT cells. Curr. Opin. Immunol. 17 (2005) 122-130
29. Matsuda J.L., Gapin L., Sidobre S., Kieper W.C., Tan J.T., Ceredig R., Surh C.D., and Kronenberg M. Homeostasis of V alpha 14i NKT cells. Nat. Immunol. 3 (2002) 966-974
30. McCausland M.M., Yusuf I., Tran H., Ono N., Yanagi Y., and Crotty S. SAP regulation of follicular helper CD4 T cell development and humoral immunity is independent of SLAM and Fyn kinase. J. Immunol. 178 (2007) 817-828
31. Nichols K.E., Harkin D.P., Levitz S., Krainer M., Kolquist K.A., Genovese C., Bernard A., Ferguson M., Zuo L., Snyder E., et al. Inactivating mutations in an SH2 domain-encoding gene in X-linked lymphoproliferative syndrome. Proc. Natl. Acad. Sci. USA 95 (1998) 13765-13770
32. 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., and Stein P.L. Regulation of NKT cell development by SAP, the protein defective in XLP. Nat. Med. 11 (2005) 340-345
33. Nichols K.E., Ma C.S., Cannons J.L., Schwartzberg P.L., and Tangye S.G. Molecular and cellular pathogenesis of X-linked lymphoproliferative disease. Immunol. Rev. 203 (2005) 180-199
34. Ohteki T., Ho S., Suzuki H., Mak T.W., and Ohashi P.S. Role for IL-15/IL-15 receptor beta-chain in natural killer 1.1+ T cell receptor-alpha beta+ cell development. J. Immunol. 159 (1997) 5931-5935
35. Park S.H., Bae Y.M., Kim T.J., Ha I.S., Kim S., Chi J.G., and Lee S.K. HLA-DR expression in human fetal thymocytes. Hum. Immunol. 33 (1992) 294-298
36. Park W.S., Bae Y., Chung D.H., Choi Y.L., Kim B.K., Sung Y.C., Choi E.Y., Park S.H., and Jung K.C. T cell expression of CIITA represses Th1 immunity. Int. Immunol. 16 (2004) 1355-1364
37. Pasquier B., Yin L., Fondaneche M.C., Relouzat F., Bloch-Queyrat C., Lambert N., Fischer A., de Saint-Basile G., and Latour S. Defective NKT cell development in mice and humans lacking the adapter SAP, the X-linked lymphoproliferative syndrome gene product. J. Exp. Med. 201 (2005) 695-701
38. Patel D.R., Li W., Park J.S., Sofi M.H., Gourley T.S., Hangoc G., Kaplan M.H., and Chang C.H. Constitutive expression of CIITA directs CD4 T cells to produce Th2 cytokines in the thymus. Cell. Immunol. 233 (2005) 30-40
39. Ranson T., Vosshenrich C.A., Corcuff E., Richard O., Laloux V., Lehuen A., and Di Santo J.P. IL-15 availability conditions homeostasis of peripheral natural killer T cells. Proc. Natl. Acad. Sci. USA 100 (2003) 2663-2668
40. Reith W., LeibundGut-Landmann S., and Waldburger J.M. Regulation of MHC class II gene expression by the class II transactivator. Nat. Rev. Immunol. 5 (2005) 793-806
41. Sayos J., Wu C., Morra M., Wang N., Zhang X., Allen D., van Schaik S., Notarangelo L., Geha R., Roncarolo M.G., et al. The X-linked lymphoproliferative-disease gene product SAP regulates signals induced through the co-receptor SLAM. Nature 395 (1998) 462-469
42. Schluns K.S., Nowak E.C., Cabrera-Hernandez A., Puddington L., Lefrancois L., and Aguila H.L. Distinct cell types control lymphoid subset development by means of IL-15 and IL-15 receptor alpha expression. Proc. Natl. Acad. Sci. USA 101 (2004) 5616-5621
43. Schmidt-Supprian M., Tian J., Grant E.P., Pasparakis M., Maehr R., Ovaa H., Ploegh H.L., Coyle A.J., and Rajewsky K. Differential dependence of CD4+CD25+ regulatory and natural killer-like T cells on signals leading to NF-kappaB activation. Proc. Natl. Acad. Sci. USA 101 (2004) 4566-4571
44. Sivakumar V., Hammond K.J., Howells N., Pfeffer K., and Weih F. Differential requirement for Rel/nuclear factor kappa B family members in natural killer T cell development. J. Exp. Med. 197 (2003) 1613-1621
45. Stanic A.K., Bezbradica J.S., Park J.J., Van Kaer L., Boothby M.R., and Joyce S. Cutting edge: The ontogeny and function of Va14Ja18 natural T lymphocytes require signal processing by protein kinase C theta and NF-kappa B. J. Immunol. 172 (2004) 4667-4671
46. Sun Z., Arendt C.W., Ellmeier W., Schaeffer E.M., Sunshine M.J., Gandhi L., Annes J., Petrzilka D., Kupfer A., Schwartzberg P.L., and Littman D.R. PKC-theta is required for TCR-induced NF-kappaB activation in mature but not immature T lymphocytes. Nature 404 (2000) 402-407
47. Szabo S.J., Kim S.T., Costa G.L., Zhang X., Fathman C.G., and Glimcher L.H. A novel transcription factor, T-bet, directs Th1 lineage commitment. Cell 100 (2000) 655-669
48. Tepper R.I., Levinson D.A., Stanger B.Z., Campos-Torres J., Abbas A.K., and Leder P. IL-4 induces allergic-like inflammatory disease and alters T cell development in transgenic mice. Cell 62 (1990) 457-467
49. Thulesen S., Jorgensen A., Gerwien J., Dohlsten M., Holst Nissen M., Odum N., and Ropke C. Superantigens are presented by and activate thymocytes from infants. Exp. Clin. Immunogenet. 16 (1999) 226-233
50. Townsend M.J., Weinmann A.S., Matsuda J.L., Salomon R., Farnham P.J., Biron C.A., Gapin L., and Glimcher L.H. T-bet regulates the terminal maturation and homeostasis of NK and Valpha14i NKT cells. Immunity 20 (2004) 477-494
51. Urdahl K.B., Sun J.C., and Bevan M.J. Positive selection of MHC class Ib-restricted CD8(+) T cells on hematopoietic cells. Nat. Immunol. 3 (2002) 772-779
52. Wu C., Nguyen K.B., Pien G.C., Wang N., Gullo C., Howie D., Sosa M.R., Edwards M.J., Borrow P., Satoskar A.R., et al. SAP controls T cell responses to virus and terminal differentiation of TH2 cells. Nat. Immunol. 2 (2001) 410-414