T cell receptor ligation triggers novel nonapoptotic cell death pathways that are Fas-independent or Fas-dependent

Journal of Immunology

Volumn 169, Issue 11, 2002, Pages 6218-6230

  Davidson, Wendy F ^a,b   Haudenschild, Christian ^a   Kwon, Jaeyul ^a   Williams, Mark S ^a,b  

^a HOLLAND LABORATORY   (United States)

^b GEORGE WASHINGTON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; CASPASE; CD4 ANTIGEN; CD8 ANTIGEN; FAS LIGAND; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; MONOCLONAL ANTIBODY; NEUTRALIZING ANTIBODY; SYNAPTOPHYSIN; T LYMPHOCYTE RECEPTOR; FAS ANTIGEN; FASL PROTEIN, MOUSE; LYMPHOCYTE ANTIGEN RECEPTOR; MEMBRANE PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE P38; REACTIVE OXYGEN METABOLITE; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; APOPTOSIS; ARTICLE; AUTOIMMUNITY; CELL CULTURE; CELL DEATH; CLINICAL PATHWAY; CONTROLLED STUDY; ENZYME REGULATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CROSS LINKING; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; T LYMPHOCYTE SUBPOPULATION; ANIMAL; BAGG ALBINO MOUSE; BIOLOGICAL MODEL; C3H MOUSE; C57BL MOUSE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CYTOLOGY; ELECTRON MICROSCOPY; GENETICS; IMMUNOLOGY; IN VITRO STUDY; LYMPHOCYTE ACTIVATION; METABOLISM; MOUSE MUTANT; T LYMPHOCYTE;

ANIMALS; ANTIGENS, CD95; APOPTOSIS; CASPASES; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELL DEATH; FAS LIGAND PROTEIN; LYMPHOCYTE ACTIVATION; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED BALB C; MICE, INBRED C3H; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, MUTANT STRAINS; MICROSCOPY, ELECTRON; MITOGEN-ACTIVATED PROTEIN KINASES; MODELS, IMMUNOLOGICAL; P38 MITOGEN-ACTIVATED PROTEIN KINASES; REACTIVE OXYGEN SPECIES; RECEPTORS, ANTIGEN, T-CELL; SIGNAL TRANSDUCTION; T-LYMPHOCYTES; TUMOR NECROSIS FACTOR-ALPHA;

EID: 0036884315     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.169.11.6218     Document Type: Article

References (69)

1. Lenardo, M., K. M. Chan, F. Hornung, H. McFarland, R. Siegel, J. Wang, and L. Zheng. 1999. Mature T lymphocyte apoptosis-immune regulation in a dynamic and unpredictable antigenic environment. Annu. Rev. Immunol. 17:221.
2. Budd, R. C. 2001. Activation-induced cell death. Curr. Opin. Immunol. 13:356.
3. Lenardo, M. J. 1991. Interleukin-2 programs mouse αβ T lymphocytes for apoptosis. Nature 353:858.
4. Willerford, D. M., J. Chen, J. A. Ferry, L. Davidson, A. Ma, and F. W. Alt. 1995. Interleukin-2 receptor α chain regulates the size and content of the peripheral lymphoid compartment. Immunity 3:521.
5. Suzuki, H., T. M. Kundig, C. Furlonger, A. Wakeham, E. Timms, T. Matsuyama, R. Schmits, J. J. Simard, P. S. Ohashi, H. Griesser, et al. 1995. Deregulated T cell activation and autoimmunity in mice lacking interleukin-2 receptor β. Science 268:1472.
6. Kneitz, B., T. Herrmann, S. Yonehara, and A. Schimpl. 1995. Normal clonal expansion but impaired Fas-mediated cell death and anergy induction in interleukin-2-deficient mice. Eur. J. Immunol. 25:2572.
7. Kerr, J. F. R., A. H. Wyllie, and A. R. Currie. 1972. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br. J. Cancer 26:239.
8. Arends, M. J., and A. H. Wyllie. 1991. Apoptosis: mechanisms and roles in pathology. Int. Rev. Exp. Pathol. 32:223.
9. Cohen, J. J. 1993. Apoptosis. Immunol. Today 14:126.
10. Majno, G., and I. Joris. 1995. Apoptosis, oncosis, and necrosis: an overview of cell death. Am. J. Pathol. 146:3.
11. Fadok, V. A., D. R. Voelker, P. A. Campbell, J. J. Cohen, D. L. Bratton, and P. M. Henson. 1992. Exposure of phosphatidylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal by macrophages. J. Immunol. 148:2207.
12. Enari, M., R. V. Talanian, W. W. Wong, and S. Nagata. 1996. Sequential activation of ICE-like and CPP32-like proteases during Fas-mediated apoptosis. Nature 380:723.
13. Thornberry, N. A., T. A. Rano, E. P. Peterson, D. M. Rasper, T. Timkey, M. Garcia-Calvo, V. M. Houtzager, P. A. Nordstrom, S. Roy, J. P. Vaillancourt, et al. 1997. A combinatorial approach defines specificities of members of the caspase family and granzyme B: functional relationships established for key mediators of apoptosis. J. Biol. Chem. 272:17907.
14. Earnshaw, W. C., L. M. Martins, and S. H. Kaufmann. 1999. Mammalian caspases: structure, activation, substrates, and functions during apoptosis. Annu. Rev. Biochem. 68:383.
15. Savill, J., I. Dransfield, N. Hogg, and C. Haslett. 1990. Vitronectin receptor-mediated phagocytosis of cells undergoing apoptosis. Nature 343:170.
16. 3). J. Immunol. 161:6250.
17. Fadok, V. A., D. L. Bratton, D. M. Rose, A. Pearson, R. A. Ezekewitz, and P. M. Henson. 2000. A receptor for phosphatidylserine-specific clearance of apoptotic cells. Nature 405:85.
18. Matsuoka, S., Y. Asano, K. Sano, H. Kishimoto, I. Yamashita, H. Yorifuji, M. Utsuyama, K Hirokawa, and T. Tada. 1995. A novel type of cell death of lymphocytes induced by a monoclonal antibody without participation of complement. J. Exp. Med. 181:2007.
19. Zhang, C., Y. Xu, J. Gu, and S. F. Schlossman. 1998. A cell surface receptor defined by a mAb mediates a unique type of cell death similar to oncosis. Proc. Natl. Acad. Sci. USA 95:6290.
20. Deas, O., C. Dumont, M. MacFarlane, M. Rouleau, C. Hebib, F. Harper, F. Hirsch, B. Charpentier, G. M. Cohen, and A. Senik. 1998. Caspase-independent cell death induced by anti-CD2 or staurosporine in activated human peripheral T lymphocytes. J. Immunol. 161:3375.
21. Sperandio, S., I. de Belle, and D. E. Bredesen. 2000. An alternative, nonapoptotic form of programmed cell death. Proc. Natl. Acad. Sci. USA 97:14376.
22. Zheng, T. S., S. F. Schlosser, T. Dao, R. Hingorani, I. N. Crispe, J. L. Boyer, and R. A. Flavell. 1998. Caspase-3 controls both cytoplasmic and nuclear events associated with Fas-mediated apoptosis in vivo. Proc. Natl. Acad. Sci. USA 95:13618.
23. Zheng, T. S., S. Hunot, K. Kuida, and R. A. Flavell. 1999. Caspase knockouts: matters of life and death. Cell Death Differ. 6:1043.
24. Woo, M., R. Hakem, M. S. Soengas, G. S. Duncan, A. Shahinian, D. Kagi, A. Hakem, M. McCurrach, W. Khoo, S. A. Kaufman, et al. 1998. Essential contribution of caspase 3/CPP32 to apoptosis and its associated nuclear changes. Genes Dev. 12:806.
25. Hirsch, T., P. Marchetti, S. A. Susin, B. Dallaporta, N. Zamzami, I. Marzo, M. Geuskens, and G. Kroemer. 1997. The apoptosis-necrosis paradox: apoptogenic proteases activated after mitochondrial permeability transition determine the mode of cell death. Oncogene 15:1573.
26. Matsumura, H., Y. Shimizu, Y. Ohsawa, A. Kawahara, Y. Uchiyama, and S. Nagata. 2000. Necrotic death pathway in Fas receptor signaling. J. Cell Biol. 151:1247.
27. Holler, N., R. Zaru, O. Micheau, M. Thome, A. Attinger, S. Valitutti, J. L. Bodmer, P. Schneider, B. Seed, and J. Tschopp. 2000. Fas triggers an alternative, caspase-8-independent cell death pathway using the kinase RIP as effector molecule. Nat. Immunol. 1:489.
28. Tanabe, K., H. Nakanishi, H. Maeda, T. Nishioku, K. Hashimoto, S. Y. Liou, A. Akamine, and K. Yamamoto. 1999. A predominant apoptotic death pathway of neuronal PC12 cells induced by activated microglia is displaced by a non-apoptotic death pathway following blockage of caspase-3-dependent cascade. J. Biol. Chem. 274:15725.
29. Wyllie, A. H., and P. Golstein. 2001. More than one way to go. Proc. Natl. Acad. Sci. USA 98:11.
30. Davidson, W. F., F. J. Dumont, H. G. Bedigian, B. J. Fowlkes, and H. C. Morse 3rd. 1986. Phenotypic, functional, and molecular genetic comparisons of the abnormal lymphoid cells of C3H-lpr/lpr and C3H-gld/gld mice. J. Immunol. 136:4075.
31. Cohen, P. L., and R. A. Eisenberg. 1991. Lpr and gld: single gene models of systemic autoimmunity and lymphoproliferative disease. Annu. Rev. Immunol. 9:243.
32. Straus, S. E., M. Sneller, M. J. Lenardo, J. M. Puck, and W. Strober. 1999. An inherited disorder of lymphocyte apoptosis: the autoimmune lymphoproliferative syndrome. Ann. Intern. Med. 130:591.
33. Zheng, L., G. Fisher, R. E. Miller, J. Peschon, D. H. Lynch, and M. J. Lenardo. 1995. Induction of apoptosis in mature T cells by tumour necrosis factor. Nature 377:348.
34. Teh, H. S., A. Seebaran, and S. J. Teh. 2000. The TNF receptor 2-deficient CD8 T cells are resistant to Fas/Fas ligand-induced cell death. J. Immunol. 165:4814.
35. Giese, T., and W. F. Davidson. 1992. Evidence for early onset polyclonal activation of T cell subsets in mice homozygous for lpr. J. Immunol. 149:3097.
36. Williams, M. S., and P. A. Henkart. 1994. Apoptotic cell death induced by intracellular proteolysis. J. Immunol. 153:4247.
37. Han, D. K., C. C. Haudenschild, M. K. Hong, B. T. Tinkle, M. B. Leon, and G. Liau. 1995. Evidence for apoptosis in human atherogenesis and in a rat vascular injury model. Am. J. Pathol. 147:267.
38. Sytwu, H. K., R. S. Liblau, and H. O. McDevitt. 1996. The roles of Fas/APO-1 (CD95) and TNF in antigen-induced programmed cell death in T cell receptor transgenic mice. Immunity 1:17.
39. Newton, K., and A. Strasser. 2000. Ionizing radiation and chemotherapeutic drugs induce apoptosis in lymphocytes in the absence of Fas of FADD/MORT1 signaling: implications for cancer therapy. J. Exp. Med. 191:195.
40. Reap, E. A., K. Roof, K. Maynor, M. Borrero, J. Booker, and P. L. Cohen. 1997. Radiation and stress-induced apoptosis: a role for Fas/Fas ligand interactions. Proc. Natl. Acad. Sci. USA 94:5750.
41. Denecker, G., D. Vercammen, M. Steemans, T. Vanden Berghe, G: Brouckaert, G. Van Loo, B. Zhivotovsky, W. Fiers, J. Grooten, W. Declercq, and P. Vandenabeele. 2001. Death receptor-induced apoptotic and necrotic cell death: differential role of caspases and mitochondria. Cell Death Differ. 8:829.
42. Hildeman, D. A., T. Mitchell, T. K. Teague, P. Henson, B. J. Day, J. Kappler, and P. C. Marrack. 1999. Reactive oxygen species regulate activation-induced T cell apoptosis. Immunity 10:735.
43. Vercammen, D., R. Beyaert, G. Denecker, V. Goossens, G. Van Loo, W. Declercq, J. Grooten, W. Fiers, and P. Vandenabeele. 1998. Inhibition of caspases increases the sensitivity of L929 cells to necrosis mediated by tumor necrosis factor. J. Exp. Med. 187:1477.
44. Vercammen D., G. Brouckaert, G. Denecker, M. Van de Craen, W. Declercq, W. Fiers, and P. Vandenabeele. 1998. Dual signaling of the Fas receptor: initiation of both apoptotic and necrotic cell death pathways. J. Exp. Med. 188:919.
45. Fiers, W., R. Beyaert, W. Declercq, and P. Vandenabeele. 1999. More than one way to die: apoptosis, necrosis and reactive oxygen damage. Oncogene 18:7719.
46. Zhang, J., J. X. Gao, K. Salojin, Q. Shao, M. Grattan, C. Meagher, D. W. Laird, and T. L. Delovitch. 2000. Regulation of fas ligand expression during activation-induced cell death in T cells by p38 mitogen-activated protein kinase and c-Jun NH2-terminal kinase. J. Exp. Med. 191:1017.
47. Hsu, S. C., M. A. Gavrilin, M. H. Tsai, J. Han, and M. Z. Lai. 1999. p38 mitogen-activated protein kinase is involved in Fas ligand expression. J. Biol. Chem. 274:25769.
48. McCarthy, N. J., M. K. Whyte, C. S. Gilbert, and G. I. Evan. 1997. Inhibition of Ced-3/ICE-related proteases does not prevent cell death induced by oncogenes, DNA damage, or the Bcl-2 homologue Bak. J. Cell Biol. 136:215.
49. Xiang, J., D. T. Chao, and S. J. Korsmeyer. 1996. BAX-induced cell death may not require interleukin 1β-converting enzyme-like proteases. Proc. Natl. Acad. Sci. USA 93:14559.
50. Yoshida, H., Y. Y Kong, R. Yoshida, A. J. Elia, A. Hakem, R. Hakem, J. M. Penninger, and T. W. Mak. 1998. Apaf1 is required for mitochondrial pathways of apoptosis and brain development. Cell 94:739.
51. Susin, S. A., E. Daugas, L. Ravagnan, K. Samejima, N. Zamzami, M. Loeffler, P. Costantini, K. F. Ferri, T. Irinopoulou, M. C. Prevost, et al. 2000. Two distinct pathways leading to nuclear apoptosis. J. Exp. Med. 192:571.
52. Alexander-Miller, M. A., M. A. Derby, A. Sarin, P. A. Henkart, and J. A. Berzofsky. 1998. Supra-optimal peptide-major histocompatibility complex causes a decrease in Bcl-2 levels and allows tumor necrosis factor α receptor II-mediated apoptosis of cytotoxic T lymphocytes. J. Exp. Med. 188:1391.
53. Sarin, A., M. Conan-Cibotti, and P. A. Henkart. 1995. Cytotoxic effect of TNF and lymphotoxin on T lymphoblasts. J. Immunol. 155:3716.
54. Pimentel-Muinos, F. X., and B. Seed. 1999. Regulated commitment of TNF receptor signaling: a molecular switch for death or activation. Immunity 11:783.
55. 2+], regulation in apoptosis, oncosis, and necrosis. Biochim. Biophys. Acta 1313:173.
56. Telford, W. G., S. Y. Nam, E. R. Podack, and R. A. Miller. 1997. CD30-regulated apoptosis in murine CD8 T cells after cessation of TCR signals. Cell. Immunol. 182:125.
57. Daugas, E., S. A. Susin, N. Zamzami, K. F. Ferri, T. Irinopoulou, N. Larochette, M. C. Prevost, B. Leber, D. Andrews, J. Penninger, and G. Kroemer. 2000. Mitochondrio-nuclear translocation of AIF in apoptosis and necrosis. FASEB J. 14:729.
58. Joza, N., S. A. Susin, E. Daugas, W. L. Stanford, S. K. Cho, C. Y. Li, T. Sasaki, A. J. Elia, H. Y. Cheng, L. Ravagnan, et al. 2001. Essential role of the mitochondrial apoptosis-inducing factor in programmed cell death. Nature 410:549.
59. Spaner, D., K. Raju, L. Radvanyi, Y. Lin, and R. G. Miller. 1998. A role for perforin in activation-induced cell death. J. Immunol. 160:2655.
60. Lorenzo, H. K., S. A. Susin, J. Penninger, and G. Kroemer. 1999. Apoptosis inducing factor (AIF): a phylogenetically old, caspase-independent effector of cell death. Cell Death Differ. 6:516.
61. Hirt, U. A., F. Gantner, and M. Leist. 2000. Phagocytosis of nonapoptotic cells dying by caspase-independent mechanisms. J. Immunol. 164:6520.
62. Voll, R. E., M. Herrmann, E. A. Roth, C. Stach, J. R. Kalden, and I. Girkontaite. 1997. Immunosuppressive effects of apoptotic cells. Nature 390:350.
63. Steinman, R. M., S. Turley, I. Mellman, and K. Inaba. 2000. The induction of tolerance by dendritic cells that have captured apoptotic cells. J. Exp. Med. 191:411.
64. Heath, W. R., and F. R. Carbone. 2001. Cross-presentation, dendritic cells, tolerance and immunity. Annu. Rev. Immunol. 19:47.
65. Albert, M. L., B. Sauter, and N. Bhardwaj. 1998. Dendritic cells acquire antigen from apoptotic cells and induce class I-restricted CTLs. Nature 392:86.
66. 5 and CD36, and cross-present antigens to cytotoxic T lymphocytes. J. Exp. Med. 188:1359.
67. Sauter, B., M. L. Albert, L. Francisco, M. Larsson, S. Somersan, and N. Bhardwaj. 2000. Consequences of ceil death: exposure to necrotic tumor cells, but not primary tissue cells or apoptotic cells, induces the maturation of immunostimulatory dendritic cells. J. Exp. Med. 191:423.
68. Cocco, R. E., and D. S. Ucker. 2001. Distinct modes of macrophage recognition for apoptotic and necrotic cells are not specified exclusively by phosphatidylserine exposure. Mol. Biol. Cell 12:919.
69. Matzinger, P. 1994. Tolerance, danger, and the extended family. Annu. Rev. Immunol. 12:991.