Restimulation-induced apoptosis of T cells is impaired in patients with X-linked lymphoproliferative disease caused by SAP deficiency

Journal of Clinical Investigation

Volumn 119, Issue 10, 2009, Pages 2976-2989

  Snow, Andrew L ^a   Marsh, Rebecca A ^b   Krummey, Scott M ^a   Roehrs, Philip ^b   Young, Lisa R ^b   Zhang, Kejian ^b   Van Hoff, Jack ^c   Dhar, Deepali ^a   Nichols, Kim E ^d   Filipovich, Alexandra H ^b   Su, Helen C ^a   Bleesing, Jack J ^b   Lenardo, Michael J ^a,e  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^c DARTMOUTH HITCHCOCK MEDICAL CENTER   (United States)

^d CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^e Building 10 ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIM PROTEIN; CD150 ANTIGEN; CD3 ANTIGEN; FAS LIGAND; LYMPHOCYTE ANTIGEN; NK T B ANTIGEN; PROTEIN TYROSINE PHOSPHATASE SHP 1; SIGNALING LYMPHOCYTE ACTIVATION MOLECULE ASSOCIATED PROTEIN; T LYMPHOCYTE RECEPTOR; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CELL EXPANSION; CELLULAR IMMUNITY; CONTROLLED STUDY; HUMAN; HUMAN CELL; LYMPHOPROLIFERATIVE DISEASE; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; UPREGULATION; X CHROMOSOME LINKED DISORDER; X LINKED LYMPHOPROLIFERATIVE DISEASE;

ANIMALS; ANTIGENS, CD; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; FAS LIGAND PROTEIN; GENE EXPRESSION PROFILING; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LYMPHOPROLIFERATIVE DISORDERS; MEMBRANE PROTEINS; MICE; MICROARRAY ANALYSIS; PROTO-ONCOGENE PROTEINS; RECEPTORS, ANTIGEN, T-CELL; RECEPTORS, CELL SURFACE; RNA INTERFERENCE; SIGNAL TRANSDUCTION; T-LYMPHOCYTES;

EID: 70349678683     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI39518     Document Type: Article

References (45)

1. Lenardo, M., et al. 1999. Mature T lymphocyte apoptosis - immune regulation in a dynamic and unpredictable antigenic environment. Annu. Rev. Immunol. 17:221-253. (Pubitemid 29241124)
2. Brenner, D., Krammer, P.H., and Arnold, R. 2008. Concepts of activated T cell death. Crit. Rev. Oncol. Hematol. 66:52-64.
3. Snow, A.L., et al. 2008. Critical role for BIM in T cell receptor restimulation-induced death. Biol. Direct. 3:34.
4. Bidere, N., Su, H.C., and Lenardo, M.J. 2006. Genetic disorders of programmed cell death in the immune system. Annu. Rev. Immunol. 24:321-352.
5. Oliveira, J.B., et al. 2007. NRAS mutation causes a human autoimmune lymphoproliferative syndrome. Proc. Natl. Acad. Sci. U. S. A. 104:8953-8958.
6. Purtilo, D.T., Cassel, C.K., Yang, J.P., and Harper, R. 1975. X-linked recessive progressive combined variable immunodeficiency (Duncan's disease). Lancet. 1:935-940.
7. Purtilo, D.T., and Grierson, H.L. 1991. Methods of detection of new families with X-linked lymphoproliferative disease. Cancer Genet. Cytogenet. 51:143-153.
8. Seemayer, T.A., et al. 1995. X-linked lymphoproliferative disease: twenty-five years after the discovery. Pediatr. Res. 38:471-478.
9. Gaspar, H.B., Sharifi, R., Gilmour, K.C., and Thrasher, A.J. 2002. X-linked lymphoproliferative disease: clinical, diagnostic and molecular perspective. Br. J. Haematol. 119:585-595. (Pubitemid 35366195)
10. Nichols, K.E., Ma, C.S., Cannons, J.L., Schwartzberg, P.L., and Tangye, S.G. 2005. Molecular and cellular pathogenesis of X-linked lymphoproliferative disease. Immunol. Rev. 203:180-199. (Pubitemid 40179702)
11. Coffey, A.J., et al. 1998. Host response to EBV infection in X-linked lymphoproliferative disease results from mutations in an SH2-domain encoding gene. Nat. Genet. 20:129-135.
12. Nichols, K.E., et al. 1998. Inactivating mutations in an SH2 domain-encoding gene in X-linked lymphoproliferative syndrome. Proc. Natl. Acad. Sci. U. S. A. 95:13765-13770. (Pubitemid 28523047)
13. Sayos, J., et al. 1998. The X-linked lymphoproliferative- disease gene product SAP regulates signals induced through the co-receptor SLAM. Nature. 395:462-469. (Pubitemid 28462434)
14. Ma, C.S., Nichols, K.E., and Tangye, S.G. 2007. Regulation of cellular and humoral immune responses by the SLAM and SAP families of molecules. Annu. Rev. Immunol. 25:337-379.
15. Bassiri, H., Janice Yeo, W.C., Rothman, J., Koretzky, G.A., and Nichols, K.E. 2008. X-linked lymphoproliferative disease (XLP): a model of impaired antiviral, anti-tumor and humoral immune responses. Immunol. Res. 42:145-159.
16. Chen, G., et al. 2005. Signaling lymphocyte activation molecule-associated protein is a negative regulator of the CD8 T cell response in mice. J. Immunol. 175:2212-2218. (Pubitemid 41113827)
17. Czar, M.J., et al. 2001. Altered lymphocyte responses and cytokine production in mice deficient in the X-linked lymphoproliferative disease gene SH2D1A/DSHP/SAP. Proc. Natl. Acad. Sci. U. S. A. 98:7449-7454.
18. Wu, C., et al. 2001. SAP controls T cell responses to virus and terminal differentiation of TH2 cells. Nat. Immunol. 2:410-414. (Pubitemid 33706138)
19. Yin, L., et al. 2003. Mice deficient in the X-linked lymphoproliferative disease gene sap exhibit increased susceptibility to murine gammaherpesvirus- 68 and hypo-gammaglobulinemia. J. Med. Virol. 71:446-455. (Pubitemid 37176637)
20. Crotty, S., McCausland, M.M., Aubert, R.D., Wherry, E.J., and Ahmed, R. 2006. Hypogammaglobulinemia and exacerbated CD8 T-cell-mediated immunopathology in SAP-deficient mice with chronic LCMV infection mimics human XLP disease. Blood. 108:3085-3093. (Pubitemid 44776949)
21. Chen, G., et al. 2007. Increased proliferation of CD8+ T cells in SAP-deficient mice is associated with impaired activation-induced cell death. Eur. J. Immunol. 37:663-674. (Pubitemid 46916933)
22. Strasser, A., Jost, P.J., and Nagata, S. 2009. The many roles of FAS receptor signaling in the immune system. Immunity. 30:180-192.
23. Ramaswamy, M., et al. 2007. Cutting edge: Rac GTPases sensitize activated T cells to die via Fas. J. Immunol. 179:6384-6388.
24. Lenardo, M.J. 1991. Interleukin-2 programs mouse alpha beta T lymphocytes for apoptosis. Nature. 353:858-861.
25. Schulte, M., et al. 2007. ADAM10 regulates FasL cell surface expression and modulates FasL-induced cytotoxicity and activation-induced cell death. Cell Death Differ. 14:1040-1049. (Pubitemid 46629842)
26. Valdez, P.A., et al. 2004. NTB-A, a new activating receptor in T cells that regulates autoimmune disease. J. Biol. Chem. 279:18662-18669.
27. Howie, D., et al. 2002. Molecular dissection of the signaling and costimulatory functions of CD150 (SLAM): CD150/SAP binding and CD150-mediated costimulation. Blood. 99:957-965. (Pubitemid 34525558)
28. Bottino, C., et al. 2001. NTB-A [correction of GNTB-A], a novel SH2D1A-associated surface molecule contributing to the inability of natural killer cells to kill Epstein-Barr virus-infected B cells in X-linked lymphoproliferative disease. J. Exp. Med. 194:235-246. (Pubitemid 32730798)
29. Combadiere, B., et al. 1996. Qualitative and quantitative contributions of the T cell receptor zeta chain to mature T cell apoptosis. J. Exp. Med. 183:2109-2117. (Pubitemid 26158903)
30. Combadiere, B., Reis e Sousa, C., Germain, R.N., and Lenardo, M.J. 1998. Selective induction of apoptosis in mature T lymphocytes by variant T cell receptor ligands. J. Exp. Med. 187:349-355.
31. Cannons, J.L., et al. 2004. SAP regulates T(H)2 differentiation and PKC-theta-mediated activation of NF-kappaB1. Immunity. 21:693-706.
32. Wacholtz, M.C., and Lipsky, P.E. 1993. Anti-CD3- stimulated Ca2+ signal in individual human peripheral T cells. Activation correlates with a sustained increase in intracellular Ca2+1. J. Immunol. 150:5338-5349.
33. Hwang, P.M., et al. 2002. A "three-pronged" binding mechanism for the SAP/SH2D1A SH2 domain: structural basis and relevance to the XLP syndrome. EMBO J. 21:314-323.
34. Tangye, S.G., Nichols, K.E., Hare, N.J., and van de Weerdt, B.C. 2003. Functional requirements for interactions between CD84 and Src homology 2 domain-containing proteins and their contribution to human T cell activation. J. Immunol. 171:2485-2495.
35. Lissy, N.A., Davis, P.K., Irwin, M., Kaelin, W.G., and Dowdy, S.F. 2000. A common E2F-1 and p73 pathway mediates cell death induced by TCR activation. Nature. 407:642-645. (Pubitemid 30775376)
36. Senoo, M., Manis, J.P., Alt, F.W., and McKeon, F. 2004. p63 and p73 are not required for the development and p53-dependent apoptosis of T cells. Cancer Cell. 6:85-89. (Pubitemid 38903164)
37. Oliveira, J.B., and Fleisher, T. 2004. Autoimmune lymphoproliferative syndrome. Curr. Opin. Allergy Clin. Immunol. 4:497-503.
38. Li, C., Schibli, D., and Li, S.S. 2009. The XLP syndrome protein SAP interacts with SH3 proteins to regulate T cell signaling and proliferation. Cell Signal. 21:111-119.
39. Veillette, A. 2006. Immune regulation by SLAM family receptors and SAP-related adaptors. Nat. Rev. Immunol. 6:56-66. (Pubitemid 43279753)
40. Zhong, M.C., and Veillette, A. 2008. Control of T lymphocyte signaling by Ly108, a signaling lymphocytic activation molecule family receptor implicated in autoimmunity. J. Biol. Chem. 283:19255-19264.
41. Stefanova, I., et al. 2003. TCR ligand discrimination is enforced by competing ERK positive and SHP-1 negative feedback pathways. Nat. Immunol. 4:248-254. (Pubitemid 36322134)
42. Qi, H., Cannons, J.L., Klauschen, F., Schwartzberg, P.L., and Germain, R.N. 2008. SAP-controlled T-B cell interactions underlie germinal centre formation. Nature. 455:764-769.
43. Tabata, Y., et al. 2005. Rapid detection of intracellular SH2D1A protein in cytotoxic lymphocytes from patients with X-linked lymphoproliferative disease and their family members. Blood. 105:3066-3071. (Pubitemid 40504322)
44. Sharifi, R., et al. 2004. SAP mediates specific cytotoxic T-cell functions in X-linked lymphoproliferative disease. Blood. 103:3821-3827. (Pubitemid 38596301)
45. Wan, F., et al. 2007. Ribosomal protein S3: a KH domain subunit in NF-kappaB complexes that mediates selective gene regulation. Cell. 131:927-939. (Pubitemid 350138085)