Activation-induced cell death in T cells

Immunological Reviews

Volumn 193, Issue , 2003, Pages 70-81

  Green, Douglas R ^a   Droin, Nathalie ^a   Pinkoski, Michael ^a  

^a LA JOLLA INSTITUTE FOR ALLERGY AND IMMUNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FAS ANTIGEN; FAS LIGAND; LIGAND; MYC PROTEIN; T LYMPHOCYTE RECEPTOR; TUMOR NECROSIS FACTOR RECEPTOR; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND;

ANTIGEN PRESENTATION; APOPTOSIS; CELL DEATH; CELL INFILTRATION; HOMEOSTASIS; HUMAN; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; LYMPHOID CELL; MOLECULAR CLONING; NONHUMAN; PLEIOTROPY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REVIEW; T LYMPHOCYTE ACTIVATION; THYMOCYTE; TRANSCRIPTION REGULATION;

ANIMALS; APOPTOSIS; CLONAL DELETION; FAS LIGAND PROTEIN; HUMANS; MEMBRANE GLYCOPROTEINS; SIGNAL TRANSDUCTION; T-LYMPHOCYTES;

EID: 0038171458     PISSN: 01052896     EISSN: None     Source Type: Journal    
DOI: 10.1034/j.1600-065X.2003.00051.x     Document Type: Review

References (118)

1. Green DR, Evan GI. A matter of life and death. Cancer Cell 2002;1:19-30.
2. Smith CA, Williams GT, Kingston R, Jenkinson EJ, Owen JJ. Antibodies to CD3/T-cell receptor complex induce death by apoptosis in immature T cells in thymic cultures. Nature 1989;337:181-184.
3. Shi TF, Sahai BM, Green DR. Cyclosporin A inhibits activation-induced cell death in T-cell hybridomas and thymocytes. Nature 1989;339:625-626.
4. Mercep M, Weissman AM, Frank SJ, Klausner RD, Ashwell JD. Activation-driven programmed cell death and T cell receptor zeta eta expression. Science 1989;246:1162-1165.
5. shi TF, et al. Activation-induced cell death in T cell hybridomas is due to apoptosis. Morphologic aspects and DNA fragmentation. J Immunol 1990;144:3326-3333.
6. Shi TF, Bissonnette RP, Parfrey N, Szalay M, Kubo RT, Green DR. In vivo administration of monoclonal antibodies to the CD3 T cell receptor complex induces cell death (apoptosis) in immature thymocytes. J Immunol 1991;146:3340-3346.
7. + T cells in mice tolerant to Staphylococcus aureus enterotoxin B. Nature 1991;349:245-248.
8. Lenardo MJ. Interleukin-2 programs mouse alpha beta T lymphocytes for apoptosis. Nature 1991;353:858-861.
9. Lenardo M, et al. Mature T lymphocyte apoptosis - immune regulation in a dynamic and unpredictable antigenic environment. Annu Rev Immunol 1999;17:221-253.
10. Milon G, Marchal G, Seman M, Truffa-Bachi P. A ddayed-type hypersensitivity reaction initiated by a single T lymphocyte. Agents Actions 1981;11:612-614.
11. Evan GI, et al. Induction of apoptosis in fibroblasts by c-myc protein. Cell 1992;69:119-128.
12. Shi Y, Glynn JM, Guilbert LJ, Cotter TG, Bissonnette RP, Green DR. Role for c-myc in activation-induced apoptotic cell death in T cell hybridomas. Science 1992;257:212-214.
13. Bissonnette RP, Echeverri F, Mahboubi A, Green DR. Apoptotic cell death induced by c-myc is inhibited by bcl-2. Nature 1992;359:552-554.
14. Fanidi A, Harrington EA, Evan GI. Cooperative interaction between c-myc and bcl-2 protooncogenes. Nature 1992;359:554-556.
15. Brunner T, et al. Cell-autonomous Fas (CD9S)/Fas-ligand interaction mediates activation-induced apoptosis in T-cell hybridomas. Nature 1995;373:441-444.
16. Dhein J, Walczak H, Baumler C, Debatin KM, Krammer PH. Autocrine T-cell suicide mediated by APO-1/(Fas/CD95). Nature 1995;373:438-441.
17. Ju ST, et al. Fas (CD95)/FasL interactions required for programmed cell death after T-cell activation. Nature 1995;373:444-448.
18. Yang Y, Mercep M, Ware CF, Ashwell JD. Fas and activation-induced Fas ligand mediate apoptosis of T cell hybridomas: inhibition of Fas ligand expression by retinoic acid and glucocorticoids. J Exp Med 1995;181:1673-1682.
19. Daniel PT, Krammer PH. Activation induces sensitivity toward APO-1 (CD95)-mediated apoptosis in human B cells. J Immunol 1994:152:5624-5632.
20. Brunner T, Yoo NJ, LaFace D, Ware CF, Green DR. Activation-induced cell death in murine T cell hybridomas. Differential regulation of Fas (CD95) versus Fas ligand expression by cyclosporin A and FK506. Int Immunol 1996;8:1017-1026.
21. Russell JH, Wang R. Autoimmune gld mutation uncouples suicide and cytokine/proliferation pathways in activated, mature T cells. Eur J Immunol 1993;23:2379-2382.
22. Mixter PF, Russell JQ, Budd RC. Delayed kinetics of T lymphocyte anergy and deletion in lpr mice. J Autoimmun 1994;7:697-710.
23. Alderson MR, et al. Fas ligand mediates activation-induced cell death in human T lymphocytes. J Exp Med 1995;181:71-77.
24. Mogil RJ, et al. Fas (CD95) participates in peripheral T cell deletion and associated apoptosis in vivo. Int Immunol 1995;7:1451-1458.
25. Renno T, Hahne M, Tschopp J, MacDonald HR. Peripheral T cells undergoing superantigen-induced apoptosis in vivo express B220 and upregulate Fas and Fas ligand. J Exp Med 1996;183:431-437.
26. Le-Niculescu H, Bonfoco E, Kasuya Y, Claret FX, Green DR, Karin M. Withdrawal of survival factors results in activation of the JNK pathway in neuronal cells leading to Fas ligand induction and cell death. Mol Cell Biol 1999;19:751-763.
27. Ethell DW, Kinloch R, Green DR. Metalloproteinase shedding of Fas ligand regulates beta-amyloid neurotoxicity. Curr Biol 2002;12:1595-1600.
28. Morishima Y, et al. Beta-amyloid induces neuronal apoptosis via a mechanism that involves the c-Jun N-terminal kinase pathway and the induction of Fas ligand. J Neurosci 2001;21:7551-7560.
29. Hueber AO, Zornig M, Lyon D, Suda T, Nagata S, Evan GI. Requirement for the CD95 receptor-ligand pathway in c-Myc-induced apoptosis. Science 1997;278:1305-1309.
30. Pinkoski MJ, Droin NM, Lin T, Genestier L, Ferguson TA, Green DR. Nonlymphoid Fas ligand in peptide-induced peripheral lymphocyte deletion. Proc Natl Acad Sci USA 2002;26:26.
31. Stassi G, et al. Control of target cell survival in thyroid autoimmunity by T helper cytokines via regulation of apoptotic proteins. Nat Immunol 2000;1:483-488.
32. Stassi G, et al. Fas/Fas ligand-driven T cell apoptosis as a consequence of ineffective thyroid immunoprivilege in Hashimoto's thyroiditis. J Immunol 1999;162:263-267.
33. Kaplan HJ, Leibole MA, Tezel T, Ferguson TA. Fas ligand (CD95 ligand) controls angiogenesis beneath the retina. Nat Med 1999;5:292-297.
34. Kasibhatla S, Brunner T, Genestier L, Echeverri F, Mahboubi A, Green DR. DNA damaging agents induce expression of Fas ligand and subsequent apoptosis in T lymphocytes via the activation of NF-kappa B and AP-1. Mol Cell 1998;1:543-551.
35. Friesen C, Herr I, Krammer PH, Debatin KM. Involvement of the CD95 (APO-1/FAS) receptor/ligand system in drug-induced apoptosis in leukemia cells. Nat Med 1996;2:574-577.
36. Fulda S, Scaffidi C, Pietsch T, Krammer PH, Peter ME, Debatin KM. Activation of the CD95 (APO-1/Fas) pathway in drug- and gamma-irradiation-induced apoptosis of brain tumor cells. Cell Death Differ 1998;5:884-893.
37. Houghton JA, Harwood FG, Tillman DM. Thymineless death in colon carcinoma cells is mediated via fas signaling. Proc Natl Acad Sci USA 1997;94:8144-8149.
38. Hill LL, Ouhtit A, Loughlin SM, Kripke ML, Ananthaswamy HN, Owen-Schaub LB. Fas ligand: a sensor for DNA damage critical in skin cancer etiology. Science 1999;285:898-900.
39. Lissy NA, Davis PK, Irwin M, Kaelin WG, Dowdy SF. A common E2F-1 and p73 pathway mediates cell death induced by TCR activation. Nature 2000;407:642-645.
40. Wan TY, DeGregori J. The survival of antigen stimulated T cells requires NFκB mediated inhibition of p73 expression. Immunity 2003;18:331-342.
41. Muller M, et al. p53 activates the CD95 (APO-1/Fas) gene in response to DNA damage by anticancer drugs. J Exp Med 1998;188:2033-2045.
42. Singer GG, Abbas AK. The fas antigen is involved in peripheral but not thymic deletion of T lymphocytes in T cell receptor transgenic mice. Immunity 1994;1:365-371.
43. Zhou T, Bluethmann H, Eldridge J, Brockhaus M, Berry K, Mountz JD. Abnormal thymocyte development and production of autoreactive T cells in T cell receptor transgenic autoimmune mice. J Immunol 1991;147:466-474.
44. Walsh CM, Wen BG, Chinnaiyan AM, O'Rourke K, Dixit VM, Hedrick SM. A role for FADD in T cell activation and development. Immunity 1998;8:439-449.
45. Newton K, Harris AW, Bath ML, Smith KG, Strasser A. A dominant interfering mutant of FADD/MORT1 enhances deletion of autoreactive thymocytes and inhibits proliferation of mature T lymphocytes. EMBO J 1998;17:706-718.
46. -/- mice. Nat Immunol 2003;4:255-260.
47. Schneider P, et al. TRAIL receptors 1 (DR4) and 2 (DR5) signal FADD-dependent apoptosis and activate NF-kappaB. Immunity 1997;7:831-836.
48. Green DR. The suicide in the thymus. A twisted TRAIL. Nat Immunol 2003;4:207-208.
49. Bouillet P, et al. BH3-only Bcl-2 family member Bim is required for apoptosis of autoreactive thymocytes. Nature 2002;415:922-926.
50. Broome HE, Dargan CM, Brunner T, Green DR. Sensitivity of S49.1 cells to anti-CD95 (Fas/Apo-1)-induced apoptosis: effects of CD95, Bcl-2 or Bcl-x transduction. Cell Death Differ 1998;5:200-205.
51. Sentman CL, Shutter JR, Hockenbery D, Kanagawa O, Korsmeyer SJ. Bcl-2 inhibits multiple forms of apoptosis but not negative selection in thymocytes. Cell 1991;67:879-888.
52. Siegel RM, Katsumata M, Miyashita T, Louie DC, Greene MI, Reed JC. Inhibition of thymocyte apoptosis and negative antigenic selection in bcl-2 transgenic mice. Proc Natl Acad Sci USA 1992;89:7003-7007.
53. Strasser A, Harris AW, Cory S. bcl-2 transgene inhibits T cell death and perturbs thymic self-censorship. Cell 1991;67:889-899.
54. Speiser DE, et al. Tumor necrosis factor receptor p55 mediates deletion of peripheral cytotoxic T lymphocytes in vivo. Eur J Immunol 1996;26:3055-3060.
55. Sytwu HK, Liblau RS, McDevitt HO. The roles of Fas/APO-1 (CD95) and TNF in antigen-induced programmed cell death in T cell receptor transgenic mice. Immunity 1996;5:17-30.
56. Zheng L, Fisher G, Miller RE, Peschon J, Lynch DH, Lenardo MJ. Induction of apoptosis in mature T cells by tumour necrosis factor. Nature 1995;377:348-351.
57. Mariani SM, Krammer PH. Surface expression of TRAIL/Apo-2 ligand in activated mouse T and B cells. Eur J Immunol 1998;28:1492-1498.
58. Jeremias I, Herr I, Boehler T, Debatin KM. TRAIL/Apo-2-ligand-induced apoptosis in human T cells. Eur J Immunol 1998;28:143-152.
59. Hildeman DA, et al. Activated T cell death in vivo mediated by proapoptotic bcl-2 family member bim. Immunity 2002;16:759-767.
60. Davey GM, et al. Peripheral deletion of autoreactive CD8 T cells by cross presentation of self-antigen occurs by a Bcl-2-inhibitable pathway mediated by Bim. J Exp Med 2002;196:947-955.
61. Bouillet P, et al. Proapoptotic Bcl-2 relative Bim required for certain apoptotic responses, leukocyte homeostasis, and to preclude autoimmunity. Science 1999;286:1735-1738.
62. Nakajima H, Leonard WJ. Impaired peripheral deletion of activated T cells in mice lacking the common cytokine receptor gamma-chain: defective Fas ligand expression in gamma-chain-deficient mice. J Immunol 1997;159:4737-4744.
63. Bonfoco E, et al. Inducible nonlymphoid expression of Fas ligand is responsible for superantigen-induced peripheral deletion of T cells. Immunity 1998;9:711-720.
64. Green DR, Ferguson TA. The role of Fas ligand in immune privilege. Nat Rev Mol Cell Biol 2001;2:917-924.
65. Griffith TS, Brunner T, Fletcher SM, Green DR, Ferguson TA. Fas ligand-induced apoptosis as a mechanism of immune privilege. Science 1995;270:1189-1192.
66. Lee HO, Herndon JM, Barreiro R, Griffith TS, Ferguson TA. TRAIL: a mechanism of tumor surveillance in an immune privileged site. J Immunol 2002;169:4739-4744.
67. Hahne M, et al. Melanoma cell expression of Fas (Apo-1/CD95) ligand: implications for tumor immune escape. Science 1996;274:1363-1366.
68. O'Connell J, Bennett MW, O'Sullivan GC, Collins JK, Shanahan F. The Fas counterattack: cancer as a site of immune privilege. Immunol Today 1999;20:46-52.
69. Allison J, Georgiou HM, Strasser A, Vaux DL. Transgenic expression of CD95 ligand on islet beta cells induces a granulocytic infiltration but does not confer immune privilege upon islet allografts. Proc Natl Acad Sci USA 1997;94:3943-3947.
70. Kang SM, et al. Fas ligand expression in islets of Langerhans does not confer immune privilege and instead targets them for rapid destruction. Nat Med 1997;3:738-743.
71. Takeuchi T, et al. Accelerated rejection of Fas ligand-expressing heart grafts. J Immunol 1999;162:518-522.
72. Stuart PM, Griffith TS, Usui N, Pepose J, Yu X, Ferguson TA. CD95 ligand (FasL)-induced apoptosis is necessary for corneal allograft survival. J Clin Invest 1997;99:396-402.
73. Janin A, et al. CD95 engagement induces disseminated endothelial cell apoptosis in vivo: immunopathologic implications. Blood 2002;99:2940-2947.
74. Hohlbaum AM, Moe S, Marshak-Rothstein A. Opposing effects of transmembrane and soluble Fas ligand expression on inflammation and tumor cell survival. J Exp Med 2000;191:1209-1220.
75. Kearney ER, Pape KA, Loh DY, Jenkins MK. Visualization of peptide-specific T cell immunity and peripheral tolerance induction in vivo. Immunity 1994;1:327-339.
76. Reinhardt RL, Khoruts A, Merica R, Zell T, Jenkins MK. Visualizing the generation of memory CD4 T cells in the whole body. Nature 2001;410:101-105.
77. Jenkins MK, et al. In vivo activation of antigen-specific CD4 T cells. Annu Rev Immunol 2001;19:23-45.
78. Pinkoski MJ, Droin NM, Green DR. Tumor necrosis factor alpha up-regulates non-lymphoid Fas-ligand following superantigen-induced peripheral lymphocyte activation. J Biol Chem 2002;277:42380-42385.
79. Huang L, Soldevila G, Leeker M, Flavell R, Crispe IN. The liver eliminates T cells undergoing antigen-triggered apoptosis in vivo. Immunity 1994;1:741-749.
80. Crispe IN, Dao T, Klugewitz K, Mehal WZ, Metz DP. The liver as a site of T-cell apoptosis: graveyard, or killing field? Immunol Rev 2000;174:47-62.
81. van den Brink MR, Moore E, Horndasch KJ, Crawford JM, Murphy GF, Burakoff SJ. Fas ligand-deficient gld mice are more susceptible to graft-versus-host-disease. Transplantation 2000;70:184-191.
82. Zhang HG, et al. Antigen presenting cells expressing Fas ligand down-modulate chronic inflammatory disease in Fas ligand-deficient mice. J Clin Invest 2000;105:813-821.
83. Sabelko-Downes KA, Cross AH, Russell JH. Dual role for Fas ligand in the initiation of and recovery from experimental allergic encephalomyelitis. J Exp Med 1999;189:1195-1205.
84. Van Antwerp DJ, Martin SJ, Verma IM, Green DR. Inhibition of TNF-induced apoptosis by NF-kappa B. Trends Cell Biol 1998;8:107-111.
85. Wang CY, Mayo MW, Komeluk RG, Goedel DV, Baldwin AS Jr. NF-kappaB antiapoptosis: induction of TRAP1 and TRAP2 and c-IAP1 and c-IAP2 to suppress caspase-8 activation. Science 1998;281:1680-1683.
86. Lee EG, Boone DL, Chai S, et al. Failure to regulate TNF-induced NF-kappaB and cell death responses in A20-deficient mice. Science 2000;289:2350-2354.
87. Wu MX, AO Z, Prasad KV, Wu R, Schlossman SF. IEX-1L, an apoptosis inhibitor involved in NF-kappaB-mechated cell survival. Science 1998;281:998-1001.
88. Wang CY, Guttridge DC, Mayo MW, Baldwin AS Jr. NF-kappaB induces expression of the Bcl-2 homologue A1/Bfl-1 to preferentially suppress chemotherapy-induced apoptosis. Mol Cell Biol 1999;19:5923-5929.
89. Scaffidi C, Schmitz I, Krammer PH, Peter ME. The role of c-FLIP in modulation of CD95-induced apoptosis. J Biol Chem 1999;274:1541-1548.
90. Refadi Y, Van Parijs L, London CA, Tschopp J, Abbas AK. Biochemical mechanisms of IL-2-regulated Fas-mediated T cell apoptosis. Immunity 1998;8:615-623.
91. Bissonnette RP, McGahon A, Mahboubi A, Green DR. Functional Myc-Max heterodimer is required for activation-induced apoptosis in T cell hybridomas. J Exp Med 1994;180:2413-2418.
92. Brunner T, et al. Expression of Fas ligand in activated T cells is regulated by c-Myc. J Biol Chem 2000;275:9767-9772.
93. Kasibhatla S, Beere HM, Brunner T, Echeverri F, Green DR. A 'non-canonical' DNA-binding element mediates the response of the fas-ligand promoter to c-Myc. Curr Biol 2000;10:1205-1208.
94. Genestier L, Kasibhatla S, Brunner T, Green DR. Transforming growth factor beta1 inhibits Fas ligand expression and subsequent activation-induced cell death in T cells via downregulation of c-Myc. J Exp Med 1999;189:231-239.
95. Rao A, Luo C, Hogan PG. Transcription factors of the NFAT family: regulation and function. Annu Rev Immunol 1997;15:707-747.
96. Ranger AM, Oukka M, Rengarajan J, Glimcher LH. Inhibitory function of two NFAT family members in lymphoid homeostasis and Th2 development. Immunity 1998;9:627-635.
97. Latinis KM, Carr LL, Peterson EJ, Norian LA, Eliason SL, Koretzky GA. Regulation of CD95 (Fas) ligand expression by TCR-mediated signaling events. J Immunol 1997;158:4602-4611.
98. Macian F, Garcia-Rodriguez C, Rao A. Gene expression elicited by NFAT in the presence or absence of cooperative recruitment of Fos and Jun. EMBO J 2000;19:4783-4795.
99. Xiao S, et al. FasL promoter activation by IL-2 through SP1 and NFAT but not Egr-2 and Egr-3. Eur J Immunol 1999;29:3456-3465.
100. Latinis KM, Norian LA, Eliason SL, Koretzky GA. Two NFAT transcription factor binding sites participate in the regulation of CD95 (Fas) ligand expression in activated human T cells. J Biol Chem 1997;272:31427-31434.
101. Norian LA, Latinis KM, Koretzky GA. A newly identified response element in the CD95 ligand promoter contributes to optimal inducibility in activated T lymphocytes. J Immunol 1998;161:1078-1082.
102. MeClure RF, Heppelmann CJ, Paya CV. Constitutive Fas ligand gene transcription in Sertoli cells is regulated by Sp1. J Biol Chem 1999;274:7756-7762.
103. Mittelstadt PR, Ashwell JD. Cyclosporin A-sensitive transcription factor Egr-3 regulates Fas ligand expression. Mol Cell Biol 1998;18:3744-3751.
104. Mittelstadt PR, Ashwell JD. Role of Egr-2 in up-regulation of Fas ligand in normal T cells and aberrant double-negative lpr and gld T cells. J Biol Chem 1999;274:3222-3227.
105. Rengarajan J, et al. Sequential involvement of NFAT and Egr transcription factors in FasL regulation. Immunity 2000;12:293-300.
106. Ramsdell F, Seaman MS, Miller RE, Picha KS, Kennedy MK, Lynch DHH. Differential ability of Th1 and Th2 T cells to express Fas ligand and to undergo activation-induced cell death. Int Immunol 1994;6:1545-1553.
107. Zhang X, et al. Unequal death in T helper cell (Th) 1 and Th2 effectors: Th1, but not Th2, effectors undergo rapid Fas/FasL-mediated apoptosis. J Exp Med 1997;185:1837-1849.
108. O'Donovan KJ, Tourtellotte WG, Millbrandt J, Baraban JM. The EGR family of transcription-regulatory factors: progress at the interface of molecular and systems neuroscience. Trends Neurosci 1999;22:167-173.
109. Ghosh S, May MJ, Kopp EB. NF-kappa B and Rel proteins: evolutionarily conserved mediators of immune responses. Annu Rev Immunol 1998;16:225-260.
110. Ghosh S, Karin M. Missing pieces in the NF-kappaB puzzle. Cell 2002;109:S81-S96.
111. Kasibhatla S, Genestier L, Green DR. Regulation of fas-ligand expression during activation-induced cell death in T lymphocytes via nuclear factor kappaB. J Biol Chem 1999;274:987-992.
112. Pinkoski MJ, Green DR. Fas ligand, death gene. Cell Death Differ 1999;6:1174-1181.
113. Faris M, et al. The c-Jun N-terminal kinase cascade plays a role in stress-induced apoptosis in Jurkat cells by up-regulating Fas ligand expression. J Immunol 1998;160:134-144.
114. Srivastava RK, Sasaki CY, Hardwick JM, Longo DL. Bcl-2-mediated drug resistance: inhibition of apoptosis by blocking nuclear factor of activated T lymphocytes (NFAT)-induced Fas ligand transcription. J Exp Med 1999;190:253-265.
115. Harwood FG, Kasibhatla S, Petak I, Vernes R, Green DR, Houghton JA. Regulation of FasL by NF-kappaB and AP-1 in Fas-dependent thymineless death of human colon carcinoma cells. J Biol Chem 2000;275:10023-10029.
116. Brunet A, et al. Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 1999;96:857-868.
117. Suhara T, Kim HS, Kirshenbaum LA, Walsh K. Suppression of Akt signaling induces Fas ligand expression: involvement of caspase and Jun kinase activation in Akt-mediated Fas ligand regulation. Mol Cell Biol 2002;22:680-691.
118. Delgado M, Ganea D. Vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide inhibit expression of Fas ligand in activated T lymphocytes by regulating c-Myc, NF-kappa B, NF-AT, and early growth factors 2/3. J Immunol 2001;166:1028-1040.