CD95, BIM and T cell homeostasis

Nature Reviews Immunology

Volumn 9, Issue 7, 2009, Pages 514-519

  Bouillet, Philippe ^a   O'Reilly, Lorraine A ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; APOPTOSOME; BIM PROTEIN; CASPASE 10; CASPASE 8; CASPASE 9; DEATH DOMAIN RECEPTOR SIGNALING ADAPTOR PROTEIN; FAS ANTIGEN; FAS LIGAND; GAMMA INTERFERON; PROTEIN BAD; PROTEIN BAK; PROTEIN BAX; PROTEIN BCL 2; PROTEIN BCL W; PROTEIN BCL XL; PROTEIN BID; PROTEIN MCL 1; PROTEIN NOXA; PUMA PROTEIN;

ANTIGEN PRESENTING CELL; APOPTOSIS; AUTOIMMUNITY; CELL ACTIVATION; CELL PERMEABILIZATION; DOWN REGULATION; GENE REARRANGEMENT; HEMATOPOIETIC CELL; HERPES SIMPLEX VIRUS; HERPES VIRUS; HOMEOSTASIS; HUMAN; IMMUNE RESPONSE; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MITOCHONDRIAL PERMEABILITY; NONHUMAN; PRIORITY JOURNAL; REVIEW; T LYMPHOCYTE;

ANIMALS; ANTIGENS, CD95; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; HOMEOSTASIS; HUMANS; MEMBRANE PROTEINS; PROTO-ONCOGENE PROTEINS; T-LYMPHOCYTE SUBSETS;

EID: 67649884532     PISSN: 14741733     EISSN: None     Source Type: Journal    
DOI: 10.1038/nri2570     Document Type: Review

References (64)

1. Metcalf, D. Lineage commitment in the progeny of murine hematopoietic preprogenitor cells: influence of thrombopoietin and interleukin 5. Proc. Natl Acad. Sci. USA 95, 6408-6412 (1998).
2. Strasser, A. The role of BH3-only proteins in the immune system. Nature Rev. Immunol. 5, 189-200 (2005).
3. Itoh, N. et al. The polypeptide encoded by the cDNA for human cell surface antigen Fas can mediate apoptosis. Cell 65, 233-243 (1991).
4. O'Connor, L. et al. Bim: a novel member of the Bcl-2 family that promotes apoptosis. EMBO J. 17, 384-395 (1998).
5. Krammer, P. H. CD95's deadly mission in the immune system. Nature 407, 789-795 (2000).
6. Wallach, D., Kovalenko, A. V., Varfolomeev, E. E. & Boldin, M. P. Death-inducing functions of ligands of the tumor necrosis factor family: a Sanhedrin verdict. Curr. Opin. Immunol. 10, 279-288 (1998).
7. Schneider, P. et al. Conversion of membrane-bound Fas (CD95) ligand to its soluble form is associated with downregulation of its proapoptotic activity and loss of liver toxicity. J. Exp. Med. 187, 1205-1213 (1998).
8. Tanaka, M., Itai, T., Adachi, M. & Nagata, S. Downregulation of Fas ligand by shedding. Nature Med. 4, 31-36 (1998).
9. Siegel, R. M. et al. Fas preassociation required for apoptosis signaling and dominant inhibition by pathogenic mutations. Science 288, 2354-2357 (2000).
10. Nagata, S. Apoptosis by death factor. Cell 88, 355-365 (1997).
11. Kischkel, F. C. et al. Cytotoxicity-dependent APO-1 (Fas/CD95) - associated proteins form a deathinducing signaling complex (DISC) with the receptor. EMBO J. 14, 5579-5588 (1995).
12. Strasser, A., Jost, P. J. & Nagata, S. The many roles of FAS receptor signaling in the immune system. Immunity 30, 180-192 (2009).
13. Watanabe-Fukunaga, R., Brannan, C. I., Copeland, N. G., Jenkins, N. A. & Nagata, S. Lymphoproliferation disorder in mice explained by defects in Fas antigen that mediates apoptosis. Nature 356, 314-317 (1992). This paper identifies a mutation in CD95 as the cause of the lymphoproliferative disorder in Cd95lpr mice.
14. Trambas, C. M. & Griffiths, G. M. Delivering the kiss of death. Nature Immunol. 4, 399-403 (2003).
15. Schulte, M. et al. ADAM10 regulates FasL cell surface expression and modulates FasL-induced cytotoxicity and activation-induced cell death. Cell Death Differ. 14, 1040-1049 (2007).
16. Zhang, J., Cado, D., Chen, A., Kabra, N. H. & Winoto, A. Fas-mediated apoptosis and activation-induced T-cell proliferation are defective in mice lacking FADD/ Mort1. Nature 392, 296-300 (1998).
17. Varfolomeev, E. E. et al. Targeted disruption of the mouse caspase 8 gene ablates cell death induction by the TNF receptors, Fas/Apo1, and DR3 and is lethal prenatally. Immunity 9, 267-276 (1998).
18. Kang, T. B. et al. Caspase-8 serves both apoptotic and nonapoptotic roles. J. Immunol. 173, 2976-2984 (2004).
19. Newton, K., Harris, A. W., Bath, M. L., Smith, K. G. C. & Strasser, A. A dominant interfering mutant of FADD/ Mort1 enhances deletion of autoreactive thymocytes and inhibits proliferation of mature T lymphocytes. EMBO J. 17, 706-718 (1998).
20. Walsh, C. M. et al. A role for FADD in T cell activation and development. Immunity 8, 439-449 (1998).
21. Salmena, L. et al. Essential role for caspase 8 in T-cell homeostasis and T-cell-mediated immunity. Genes Dev. 17, 883-895 (2003).
22. Adams, J. M. & Cory, S. Bcl-2-regulated apoptosis: mechanism and therapeutic potential. Cur. Opin. Immunol. 19, 488-496 (2007).
23. Chipuk, J. E. & Green, D. R. How do BCL-2 proteins induce mitochondrial outer membrane permeabilization? Trends Cell Biol. 18, 157-164 (2008).
24. van Delft, M. F. & Huang, D. C. S. How the Bcl-2 family of proteins interact to regulate apoptosis. Cell Res. 16, 203-213 (2006).
25. Giam, M., Huang, D. C. S. & Bouillet, P. BH3-only proteins and their roles in programmed cell death. Oncogene (in the press).
26. Mérino, D. & Bouillet, P. The Bcl-2 family in autoimmune and degenerative disorders. Apoptosis 14, 570-583 (2009).
27. Takahashi, T. et al. Generalized lymphoproliferative disease in mice, caused by a point mutation in the Fas ligand. Cell 76, 969-976 (1994). This paper shows that inactivating mutations in CD95L cause the generalized lymphoproliferative disease seen in Cd95gld mice.
28. Cohen, P. L. & Eisenberg, R. A. The lpr and gld genes in systemic autoimmunity: life and death in the Fas lane. Immunol. Today 13, 427-428 (1993).
29. Rieux-Laucat, F. et al. Mutations in Fas associated with human lymphoproliferative syndrome and autoimmunity. Science 268, 1347-1349 (1995).
30. Renno, T., Hahne, M. & MacDonald, H. R. Proliferation is a prerequisite for bacterial superantigen-induced T cell apoptosis in vivo. J. Exp. Med. 181, 2283-2287 (1995).
31. Renno, T., Hahne, M., Tschopp, J. & MacDonald, H. R. Peripheral T cells undergoing superantigen-induced apoptosis in vivo express B200 and upregulate Fas and Fas ligand. J. Exp. Med. 183, 431-437 (1996).
32. Renno, T. et al. Expression of B220 on activated T cell blasts precedes apoptosis. Eur. J. Immunol. 28, 540-547 (1998).
33. Russell, J. H., Rush, B., Weaver, C. & Wang, R. Mature T cells of autoimmune lpr/lpr mice have a defect in antigen-stimulated suicide. Proc. Natl Acad. Sci. USA 90, 4409-4413 (1993).
34. Alderson, M. R. et al. Fas ligand mediates activationinduced cell death in human T lymphocytes. J. Exp. Med. 181, 71-77 (1995).
35. Brunner, T. et al. Cell-autonomous Fas (CD95)/Fasligand interaction mediates activation-induced apoptosis in T-cell hybridomas. Nature 373, 441-444 (1995).
36. Dhein, J., Walczak, H., Baumler, C., Debatin, K.-M. & Krammer, P. H. Autocrine T-cell suicide mediated by APO-1/(Fas/CD95). Nature 373, 438-441 (1995).
37. Green, D. R., Droin, N. & Pinkoski, M. Activationinduced cell death in T cells. Immunol. Rev. 193, 70-81 (2003).
38. Lohman, B. L., Razvi, E. S. & Welsh, R. M. T-lymphocyte downregulation after acute viral infection is not dependent on CD95 (Fas) receptor- ligand interactions. J. Virol. 70, 8199-8203 (1996).
39. Zimmermann, C., Rawiel, M., Blaser, C., Kaufmann, M. & Pircher, H. Homeostatic regulation of CD8+ T cells after antigen challenge in the absence of Fas (CD95). Eur. J. Immunol. 26, 2903-2910 (1996).
40. Mogil, R. J. et al. Fas (CD95) participates in peripheral T cell deletion and associated apoptosis in vivo. Int. Immunol. 7, 1451-1458 (1995).
41. Bonfoco, E. et al. Inducible nonlymphoid expression of Fas ligand is responsible for superantigen-induced peripheral deletion of T cells. Immunity 9, 711-720 (1998).
42. Hildeman, D. A. et al. Activated T cell death in vivo mediated by pro-apoptotic Bcl-2 family member, Bim. Immunity 16, 759-767 (2002).
43. Strasser, A. & Pellegrini, M. T-lymphocyte death during shutdown of an immune response. Trends Immunol. 25, 610-615 (2004).
44. Singer, G. G. & Abbas, A. K. The fas antigen is involved in peripheral but not thymic deletion of T lymphocytes in T cell receptor transgenic mice. Immunity 1, 365-371 (1994).
45. Zammit, D. J., Turner, D. L., Klonowski, K. D., Lefrancois, L. & Cauley, L. S. Residual antigen presentation after influenza virus infection affects CD8 T cell activation and migration. Immunity 24, 439-449 (2006).
46. Turner, D. L., Cauley, L. S., Khanna, K. M. & Lefrancois, L. Persistent antigen presentation after acute vesicular stomatitis virus infection. J. Virol. 81, 2039-2046 (2007).
47. Hughes, P., Bouillet, P. & Strasser, A. Role of Bim and other Bcl-2 family members in autoimmune and degenerative diseases. Curr. Dir. Autoimmun. 9, 74-94 (2006).
48. Bouillet, P. et al. Proapoptotic Bcl-2 relative Bim required for certain apoptotic responses, leukocyte homeostasis, and to preclude autoimmunity. Science 286, 1735-1738 (1999). This paper describes the physiological role of Bim and its association with autoimmune disease.
49. Bouillet, P. et al. BH3-only Bcl-2 family member Bim is required for apoptosis of autoreactive thymocytes. Nature 415, 922-926 (2002).
50. von Boehmer, H. Developmental biology of T cells in T cell-receptor transgenic mice. Annu. Rev. Immunol. 8, 531-556 (1990).
51. Hubner, A., Barrett, T., Flavell, R. A. & Davis, R. J. Multisite phosphorylation regulates Bim stability and apoptotic activity. Mol. Cell 30, 415-425 (2008).
52. Pellegrini, M., Belz, G., Bouillet, P. & Strasser, A. Shut down of an acute T cell immune response to viral infection is mediated by the pro-apoptotic Bcl-2 homology 3-only protein Bim. Proc. Natl Acad. Sci. USA 100, 14175-14180 (2003).
53. Vella, A. T., Dow, S., Potter, T. A., Kappler, J. & Marrack, P. Cytokine-induced survival of activated T cells in vitro and in vivo. Proc. Natl Acad. Sci. USA 95, 3810-3815 (1998).
54. Lenardo, M. J. Interleukin-2 programs mouse αβ T lymphocytes for apoptosis. Nature 353, 858-861 (1991).
55. Stranges, P. B. et al. Elimination of antigen-presenting cells and autoreactive T cells by Fas contributes to prevention of autoimmunity. Immunity 26, 629-641 (2007).
56. Erlacher, M. et al. Puma cooperates with Bim, the rate-limiting BH3-only protein in cell death during lymphocyte development, in apoptosis induction. J. Exp. Med. 203, 2939-2951 (2006).
57. Strasser, A., Harris, A. W., Huang, D. C. S., Krammer, P. H. & Cory, S. Bcl-2 and Fas/APO-1 regulate distinct pathways to lymphocyte apoptosis. EMBO J. 14, 6136-6147 (1995).
58. Badovinac, V. P., Porter, B. B. & Harty, J. T. CD8+ T cell contraction is controlled by early inflammation. Nature Immunol. 5, 809-817 (2004).
59. Reap, E. A. et al. bcl-2 transgenic Lpr mice show profound enhancement of lymphadenopathy. J. Immunol. 155, 5455-5462 (1995).
60. Hughes, P. D. et al. Apoptosis regulators Fas and Bim cooperate in shutdown of chronic immune responses and prevention of autoimmunity. Immunity 28, 197-205 (2008).
61. Weant, A. E. et al. Apoptosis regulators Bim and Fas function concurrently to control autoimmunity and CD8+ T cell contraction. Immunity 28, 218-230 (2008).
62. Hutcheson, J. et al. Combined deficiency of proapoptotic regulators Bim and Fas results in the early onset of systemic autoimmunity. Immunity 28, 206-217 (2008). Together with references 60 and 61, this work shows that CD95 and Bim cooperate in the contraction of T cell immune responses.
63. Oltersdorf, T. et al. An inhibitor of Bcl-2 family proteins induces regression of solid tumours. Nature 435, 677-681 (2005).
64. Dowdell, K. C. et al. Valproic acid (VPA), a histonedeacetylase (HDAC) inhibitor, diminishes lymphoproliferation in the Fas-deficient MRL/lpr-/- murine model of lymphoproliferative syndrome (ALPS). Exp. Hematol. 37, 487-494 (2005).