Apoptosis as a mechanism of tissue injury in liver allograft rejection

Seminars in Liver Disease

Volumn 18, Issue 2, 1998, Pages 153-167

  Krams, Sheri M ^a   Martinez, Olivia M ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cell death; CTL; Cytokines; Fas; Granzymes

Indexed keywords

APOPTOSIS; ARTICLE; CELL INFILTRATION; GRAFT REJECTION; GRAFT SURVIVAL; HUMAN; IMMUNE RESPONSE; LIVER TRANSPLANTATION; LYMPHOCYTE ACTIVATION; PRIORITY JOURNAL;

EID: 0031902941     PISSN: 02728087     EISSN: None     Source Type: Journal    
DOI: 10.1055/s-2007-1007151     Document Type: Article

References (133)

1. Wiesner RH. Advances in diagnosis, prevention and management of hepatic allograft rejection. Clin Chem 1994;40:2174-2185
2. Adams DH, Neuberger J. Patterns of liver allograft rejection. J Hepatol 1990;10:113-119
3. Vierling JM. Immunologic mechanisms of hepatic allograft rejection. Seminars in Liver Disease 1992;12:16-27
4. International Panel. Banff schema for grading liver allograft rejection: An international consensus document. Hepatology 1997;25:658-663
5. Tullius SG,Tilney NL. Both alloantigen-dependent and -independent factors influence chronic allograft rejection. Transplantation 1995;59:313-318
6. Snover DC. Problems in the interpretation of liver biopsies after liver transplantation. The American Journal of Surgical Pathology 1989;13:31-38
7. Starzl TE, Demetris AJ, Murase N, et al. Cell migration, chimerism and graft acceptance. The Lancet 1992;339:1579-1582
8. Rastellinni C, Lu L, Ricordi C, et al. Granulocyte/macrophage colony-stimulating factor-stimulated hepatic dendritic cell progenitors prolong pancreatic islet allograft survival. Transplantation 1995;60:1366-1370
9. Steinman RM, Inaba KM, Austyn JM. Donor-derived chimerism in recipients of organ transplants. Hepatology 1993; 17:1153-1156
10. Gouw AS, Houthoff HJ, Huitema S, et al. Expression of the major histocompatibility complex antigens and replacement of donor cells by recipient ones in human liver grafts. Transplantation 1987;43:291-296
11. Bishop GA, Sun J, DeCruz DJ, et al Tolerance to rat liver allografts. III Donor cell migration and tolerance-associated cytokine production in peripheral lymphoid tissues. .J Immunol 1996;156:4925-4931
12. Krams SM, Ascher NL, Martinez OM. New immunologic insights into mechanisms of allograft rejection. In Advances in Liver Transplantation. Gastroenterology Clinics of North America 1993;22:381-399
13. Molajoni ER, Cinti P, Orlandini A, et al. Mechanisms of liver allograft rejection: The indirect recognition pathway. Human Immunol 1997;53:57-63
14. Fleming KA, McMichael A, Morton JA, et al. Distribution of HLA class I antigens in normal human tissue and in mammary cancer. J Clin Pathol 1981;34:779-784
15. Daar AS, Fuggle SV, Fabre JW, et al. The detailed distribution of HLA-A, B, C antigens in normal human organs. Transplantation 1984;38:287-292
16. Steinhoff G, Wonigeit K, Pichlmayr R. Analysis of sequential changes in major histocompatibiltiy complex expression in human liver grafts after transplantation Transplantation 1988;45: 394-401
17. So SKS, Platt JL, Ascher NL, et al. Increased expression of class I major histocompatibiltiy complex antigens on hepatocytes in rejecting human liver allografts. Transplantation 1987;43:79-85
18. Daar AS, Fuggle SV, Fabre JW, et al. The detailed distribution of MHC class II antigens m normal human organs. Transplantation 1984;38:293-298
19. Demetris AJ, Lasky S, Van Thiel DH, et al. Induction of DR/Ia antigens in human liver allografts. An immunocytochemical and clinicopathologic analysis of twenty failed grafts. Transplantation 1985;40:504-509
20. Rouger P, Gugenheim J, Gane P, et al. Distribution of the MIIC antigens after liver transplantation: Relationship with biochemical and histologic parameters. Clin Exp Immunol 1990;80:404-408
21. Jenkins MK, Mueller D, Schwartz RH, et al. Induction and maintenance of aneigy in mature T cells. Adv Exp Med Biol 1991;292:167-176
22. Tan P, Anasetti C, Hansen JA, et al. Induction of alloantigenspecific hyporesponsiveness in human T lymphocytes by blocking interaction of CD28 with its natural ligand B7/BB1. J Exp Med 1993;177:165-173
23. Krummel MF, Allison JP. CD28 and CTLA4-Ig have opposing effects on the response of T cells to stimulation J Exp Med 1995;182:459-465
24. Lenschow DJ, Zeng Y, Thistlewaite JR, et al. Long-term survival of xenogeneic pancreatic islet grafts induced by CTLA4Ig. Science 1992;257:789-792
25. Tuika LA, Linsley PS, Lin H, et al. T cell activation by the CD28 ligand B7 is required for cardiac allograft rejection in vivo. Proc Natl Acad Sci 1992;89:11102-11105
26. Leon MP, Bassendine MF, Wilson JL, et al. Immunogenicity of biliary epithelium: Investigation of antigen presentation to CD4+ T cells. Hepatology 1996;24:561-567
27. Inaba K, Witmer-Pack M, Inaba M, et al. The tissue distribution of the B7-2 co-stimulator in mice: Abundant expression on dendritic cells in situ and during maturation in vitro. J Exp Med 1994;180:1849-1860
28. Lohse AW, Knolle PA, Bilo K, et al. Antigen-presenting function and B7 expression on murine sinusoidal endothelial cells and Kupffer cells. Gastroenterology 1996;110:1175-1181
29. Leon MP, Kirby JA, Gibbs P, et al. Immunogenicity of biliary epithelial cells: Study of the expression of B7 molecules. J Hepatology 1995;22:591-595
30. Garcia-Alonso AM, Minguela A, Muro M, et al. CD28 expression on peripheral blood T lymphocytes after orthotopic liver transplant: Upregulation in acute rejection. Human Immunol 1997;53:64-72
31. Adams DH, Shaw J, Hubscher SG, et al. Intercellular adhesion molecule 1 on liver allografts during rejection. Lancet 1989;2: 1122-1125
32. Bacchi CE, Marsh CL, Perkins JD, et al. Expression of vascular cell adhesion molecule (VCAM-1) in liver and pancreas allograft rejection Am J Pathol 1993;142:579-591
33. Lang T, Krams SM, Villanueva JC, et al. Differential patterns of circulating intercellular adhesion molecule-1 (cICAM-1) and vascular cell adhesion molcule-1 (cVCAM-1) during liver allograft rejection. Transplantation 1995;59:584-589
34. Lautenschlager IT, Hockerstedt KA. ICAM-1 induction on hepatocytes as a marker for immune activation of acute liver allograft rejection. Transplantation 1993;56:1495-1499
35. Steinhoff G, Behrend M, Schrader B, et al. Intercellular immune adhesion molecules in human liver transplants: Overview on expression patterns of leukocyte receptor and ligand molecules. Hepatology 1993;18:440-453
36. Isobe M, Yagita H, Okumura K, et al. Specific acceptance of cardiac allograft after treatment with antibodies to ICAM-1 and LFA-1. Science 1992;255:1125-1127
37. Pelletier RP, Ohye RG, VanBuskirk A, et al. Importance of endothelial VCAM-1 for inflammatory leukocytic infiltration in vivo. J Immunol 1992;149:2473-2481
38. Harihara Y, Sugawara Y, Inoue K, et al. Dose dependent immunosuppressive effects of antibodies to ICAM-1 and LFA-1 on hepatic allografts. Transplant Proc 1996;28:1794-1795
39. Degawa H, Watanabe K, Uchida H, et al. Blocking of ICAM-1 and LFA-1 in rat liver transplantation. Transplant Proc 1996; 28:1362-1363
40. Mosmann TR, Cherwinski H, Bond MW, et al. Two types of murine helper T cell clones. I. Definition according to profiles of lymphokine activities and secreted proteins. J Immunol 1986;136 2348-2357
41. Martinez OM, Gibbons R, Garovoy MR, et al. IL-4 inhibits IL-2 receptor expression and IL-2-dependent proliferation of human T cells. J Immunol 1990;144:2211-2215
42. Fiorentino DF, Zlotnik A, Vieira P, et al. IL-10 acts on the antigen-presenting cell to inhibit cytokine production by Th1 cells. J Immunol 1991;146:3444-3451
43. Peleman R, Wu J, Fargeas C, et al. Recombinant interleukin 4 suppresses the production of interferon gamma by human mononuclear cells. J Exp Med 1989;170:1751-1756
44. + T cells in vivo. Differential expression of IL-2 and IL-4 mRNA in recipients of cardiac allografts. J Immunol 1992;148:1308-1314
45. Takeuchi T, Lowry RP, Konieczny B. Heart allografts in murine systems The differential activation of Th2-like effector cells in peripheral tolerance. Transplantation 1992;53:1281-1294
46. Sayegh MH, Akalin E, Hancock WW, et al. CD28-B7 blockade after alloantigenic challenge in vivo inhibits Th1 cytokines but spares Th2. J Exp Med 1995;181:1869-1874
47. Ferraresso M, Tian L, Ghobrial R, et al. Rapamycin inhibits production of cytotoxic but not noncytotoxic antibodies and preferentially activates T helper 2 cells that mediate long-term survival of heart allografts in rats J Immunol 1994;153:3307-3318
48. Josien R, Pannetier C, Douillard P, et al. Graft infiltrating T helper cells. CD45RO phenotype and Th1/Th2-related cytokines in donor specific transfusion induced tolerance in adult rats. Transplantation 1995;60:1131-1139
49. Larsen CP, Elwood ET, Alexander DZ, et al. Long term acceptance of skin and cardiac allografts after blocking CD40 and CD28 pathways. Nature 1996;381:434-438
50. VanBurkirk AM, Wakely ME, Orosz, CG. Transfusion of polarized Th2 like cell populations into SCID mouse cardiac allograft recipients results in acute allograft rejection. Transplantation 1996;62:229-238
51. Lang T, Krams SM, Berquist W, et al. Elevated biliary interleukin 5 as an indicator of liver allograft rejection. Transplant Immunol 1995;3:291-298
52. Lang T, Krams SM, Martinez OM. Production of IL-4 and IL-10 does not lead to immune quiescence in vascularized human organ grafts. Transplantation 1996;62:776-780
53. Martinez OM, Krams SM, Sterneck M, et al. Intragraft cytokine profile during human liver allograft rejection. Transplantation 1992;53:449-456
54. Chen WF, Zlotnik A. IL-10: A novel cytotoxic T cell differentiation factor. J Immunol 1991;147:528-534
55. Widmer MB, Grabstein KH. Regulation of cylolytic T lymphocyte generation by B cell stimulatory factor. Nature 1987;326: 795-798
56. Foster PF, Bhattacharyya A, Sankary HN, et al. Eosinophil cationic protein's role in human hepatic allograft rejection. Hepatology 1991;13:1117-1125
57. de Groen PC, Kephart GM, Gleich GJ, et al. The eosinophil as an effector cell of the immune response during hepatic allograft rejection. Hepatology 1994;20:654-662
58. Martinez OM, Ascher NL, Ferrell L, et al. Evidence for a non-classical pathway of graft rejection involving interleukin 5 and eosinophils. Transplantation 1993;55:909-918
59. Baan CC. Metselaar HJ, Mol WM, et al. Intragraft IL-4 mRNA expression is associated with down-regulation of liver graft rejection. Clinical Transplant 1996;10:542-549
60. Bishop GA, Rokahr KL, Napoli J, et al Intragraft cytokine mRNA levels in human liver allograft rejection analyzed by reverse transcription and semiquantitative polymerase chain reaction amplification. Transplant Immunol 1993;1:253-261
61. Gorczynski RM, Adams RB, Levy GA, et al. Correlation of peripheral blood lymphocyte and intragraft cytokine mRNA expression with rejection in orthotopic liver transplantation. Surgery 1996;120:496-502
62. Huffman MW, Wonigeit K, Steinhoff G, et al. Production of cytokines (TNF-α and IL-1β) and endothelial cell activation in human liver allograft rejection. Transplant 1993;55:329-335
63. Searle J, Kerr JF, Battersby C. An electron microscopic study of the mode of donor cell death in unmodified rejection of pig liver allografts. Aust J Exp Biol Med Sci 1977;55:401-406
64. Nawaz S, Fennell RH. Apoptosis of bile duct epithelial cells in hepatic allograft rejection. Histopathology 1994;25:137-142
65. Wyllie AH, Kerr JF, Currie AR Cell death: The significance of apoptosis. Int Rev Cytol 1980;68:251-306
66. Wijsman JH, Jonker RR, Keijzer R, et al. A new method to detect apoptosis in paraffin sections: In situ end-labeling of fragmented DNA. J Histochem Cytochem 1993;41:7-12
67. Ansari B, Coates PJ, Greenstein BD, et al. In situ end labeling detects DNA strand breaks in apoptosis and other physiological and pathological states. J Pathol 1993;170:1-8
68. Grasl-Kraupp B, Ruttkay-Nedecky B, Koudelka H, et al. In situ detection of fragmented DNA (TUNEL assay) fails to discriminate among apoptosis, necrosis, and autolytic cell death: A cautionary note. Hepatology 1995;21:1465-1468
69. Krams SM, Egawa H, Quinn MB, et al. Apoptosis as a mechanism of cell death in liver allograft rejection. Transplantation 1995;59:621 625
70. Afford SC, Hubscher S, Strain AJ, et al. Apoptosis in the human liver during allograft rejection and end-stage liver disease. J Pathology 1995;176:373-380
71. Gapany C, Zhao M, Zimmermann A. The apoptosis protector, bcl-2 protein, is downregulated in bile duct epithelial cells of human liver allografts. J Hepatol 1997;26:535-542
72. Qian S, Lu L, Fu F, et al. Apoptosis within spontaneously accepted mouse liver allografts. J Immunol 1997;158:4654-4661
73. Krams SM, Hayashi M, Fox CK, et al. CD8+ cells are not necessary for allograft rejection nor the induction of apoptosis in an experimental model of small intestine transplantation. J Immunol 1998;160:April 15
74. Ito H, Kasagi N, Shomori K, et al. Apoptosis in the human allografted kidney. Transplantation 1995;60:794-798
75. Laguens RP, Cabeza Meckert PM, San Martino J, et al. Identification of programmed cell death (apoptosis) in situ by means of specific labeling of nuclear DNA fragments in heart biopsy samples during acute rejection episodes. J Heart Lung Transplant 1996;15:911-918
76. Fayyazi A, Schlemminger R, Gieseler R, et al. Apoptosis in the small intestinal allograft of the rat. Transplantation 1997;63: 947-951
77. Ando K, Guidotti LG, Wirth S, et al. Class I-restricted cytotoxic T lymphocytes are directly cytopathic for their target cells in vivo. J Immunol 1994;152:3245-3253
78. Bergese SD, Klenotic SM, Wakely ME, et al. Apoptosis in murine cardiac grafts. Transplantation 1997;63:320-325
79. Migita K, Eguchi K, Kawabe Y, et al. Apoptosis induction in human peripheral blood T lymphocytes by high-dose steroid therapy. Transplantation 1997;63:583-587
80. Pham CTN, Ley TJ. The role of granzyme B cluster proteases in cell-mediated cytotoxicity. Seminars in Immunology 1997; 9:127-133
81. Gu Y, Sarnecki C, Fleming MA, et al. Processing and activation of CMH-1 by granzyme B. J Biol Chem 1996;271:10816-10820
82. Darmon AJ, Ley TJ, Nicholson DW, et al. Cleavage of CPP32 by granzyme B represents a critical role for granzyme B in the induction of target cell DNA fragmentation. J Biol Chem 1996;271:21709-21712
83. Martinez OM, Villanueva JC, Lake J, et al. IL-2 and IL-5 gene expression in response to alloantigen in liver allograft recipients and in vitro. Transplantation 1993;55:1159-1166
84. Prendergast JA, Helgason CD, Bleackley RC. Quantitative polymerase chain reaction analysis of cytoioxic cell proteinase gene transcripts in T cells. J Biol Chem 1992;267: 5090-5095
85. Heusel JW, Wesselschmidt RL, Shresta S, et al. Cytotoxic lymphocytes require granzyme B for the rapid induction of DNA fragmentation and apoptosis in allogeneic target cells. Cell 1994;76:977-987
86. Krams SM, Villanueva JC, Quinn MB, et al. Expression of the cytotoxic T cell mediator granzyme B during liver allograft rejection Transplant Immunology 1995;3:162-166
87. Hayashi M, Martinez OM, Garcia-Kennedy R, et al. Expression of cytokines and immune mediators during chronic liver allograft rejection. Transplantation 1995;60:1533-1538
88. Legros-Maida S, Soulie A, Benvenuti C, et al. Granzyme B and perform can be used as predictive markers of acute rejection in heart transplantation. Eur J Immunol 1994;24 229-233
89. Lipman ML, Stevens AC, Strom TB. Heightened intragraft cytotoxic T-lymphocyte gene expression in acutely rejecting renal allografts. J Immunol 1994;152:5120-5127
90. Sharma VK, Bologa RM, Li B, et al. Molecular executors of cell death-differential intrarenal expression of Fas ligand, Fas, granzyme B, and perforin during acute and/or chronic rejection of human renal allografts. Transplantation 1996;62:1860-1866
91. Graubert TA, Russell JH, Ley TJ. The role of granzyme B in murine models of acute graft-versus-host disease and graft rejection. Blood 1996;87:1232-1237
92. Ahmed KR, Guo TB, Gaal KK Islet rejection in perforin-deficient mice. Transplantation 1997;63:951-957
93. Selvaggi G, Ricordi C, Podack ER, et al. The role of the perforin and Fas pathways of cytotoxicity in skin graft rejection. Transplantation 1996;62:1912-1915
94. Schulz M, Schuurman HJ, Joergensen J, et al. Acute rejection of vascular heart allografts by perforin-deficient mice. Eur J Immunol 1995;25:474-480
95. Itoh N, Yonehara S, Ishii A, et al. The polypcptide encoded by the cDNA for human cell surface antigen Fas can mediate apoptosis. Cell 1991;66:233-243
96. Oehm A, Behrmann I, Falk W, et al. Purification and molecular cloning of the APO-1 cell surface antigen, a member of the tumor necrosis factor/nerve growth factor receptor superfamily. Sequence identity with the Fas antigen. J Biol Chem 1992; 267:10709-10715
97. Yonehara S, Ishi A, Yonehara M. A cell killing monoclonal antibody (antiFas) to a cell surface antigen co-downregulated with the receptor of tumor necrosis factor. J Exp Med 1989;169:1747-1753
98. Trauth BC, Klas C, Peter AMJ, et al. Monoclonal antibody-mediated tumor regression by induction of apoptosis. Science 1989;245:301-305
99. Muzio M, Chinnaiyan AM, Kischkel FC, et al. FLICE, a novel FADD-homologous ICE/CED-3 like protease, is recruited to the CD95 (Fas/APO-1) death-inducing signaling complex. Cell 1996;85:817-827
100. Kischkel FC, Hellbardt S, Behrmann I, et al. Cytotoxicity-dependent APO-1(Fas/CD95)-associated proteins (CAP) form a death-inducing signaling complex (DISC) with the receptor. EMBO 1995;14:5579-5588
101. Chinnaiyan AM, O'Rouke K, Tewari M, et al. FADD, a novel death domain-containing protein interacts with the death domain of Fas and initiates apoptosis. Cell 1995;81:505-512
102. Suda T, Okazaki T, Naito Y, et al. Expression of the Fas ligand in cells of T cell lineage. J Immunol 1995;154:3806-3813
103. Hahne M, Renno T, Schroeter M, et al. Activated B cells express functional Fas ligand Eur J Immunol 1996;26:721-724
104. French LE, Hahne M, Viard I, et al. Fas and Fas ligand in embryos and adult mice: Ligand expression in several immuneprivileged tissues and coexpression in adult tissues characterized by apoptotic cell turnover. J Cell Biol 1996;133:335-343
105. Montel AH, Bochan MR, Hobbs JA, et al. Fas involvement in cytotoxicity mediated by human NK cells. Cell Immunol 1995;166:236-246
106. Bellgrau D, Gold D, Selawry H, et al. A role for CD95 ligand in preventing graft rejection Nature 1995;377:630-632
107. Griffith TS, Brunner T, Fletcher SM, et al. Fas ligand-induced apoptosis as a mechanism of immune privilege. Science 1995; 270:1189-1192
108. Suss G, Shortman K. A subclass of dendritic cells kills CD4 T cells via Fas/Fas-ligand induced apoptosis. J Exp Med 1996; 183:1789-1796
109. Piazza C, Montani MSG, Moretti S, et al. CD4+ T cells kill CD8+ T cells via Fas/Fas ligand-medialed apoptosis. J Immunol 1997;158:1503-1506
110. Fisher GH, Rosenberg FJ, Straus SE, et al. Dominant interfering Fas gene mutations impair apoptosis in a human autoimmune lymphoproliferative syndrome. Cell 1995;81:935-946
111. Rieux-Laucat F, Le Diest F, Hivroz C, et al. Mutations in Fas associated with human lymphoproliferative syndrome and autoimmunity. Science 1995;268:1347-1349
112. Kagi D, Vignaux F, Ledermann B, et al. Fas and perform pathways as major mechanisms of T cell-mediated cytotoxicity. Science 1994;265:528-530
113. Dong C, Wilson JE, Winters GL, et al. Human transplant coronary artery disease: Pathological evidence for Fas-mediated apoptotic cytotoxicity in allograft arteriopathy. Lab Invest 1996;74:921-931
114. Larsen CP, Alexander DZ, Hendrix R, et al. Fas-mediated cytotoxicity. An immunoeffector or immunoregulatory pathway in T cell-mediated immune response? Transplantation 1995;60: 221-224
115. Matiba B, Mariani SM, Krammer PH, The CD95 system and the death of a lymphocyte. Sem Immunol 1997;9:59-68
116. Adachi M, Suematsu S, Kondo T, et al. Targeted mutation in the Fas gene causes hyperplasia in peripheral lymphoid organs and liver. Nat Gen 1995;11:294-300
117. Ogasawara J, Watanabe-Fukunaga R, Adachi M, et al. Lethal effects of the anti-Fas antibody in mice Nature 1993;364: 806-809
118. Galle PR, Hofmann WJ, Walczak H, et al. Involvement of the CD95 (APO-1/Fas) receptor and ligand in liver damage. J Exp Med 1995;182:1223-1230
119. Krams SM, Fox CK, Beatty PR, et al. Human hepatocytes produce an isoform of Fas which inhibits apoptosis 1. Transplantation 1998;65:March 15
120. Cheng J, Zhou T, Liu C, et al. Protection from Fas-mediated apoptosis by a soluble form of fas molecule. Science 1994;263: 1759-1762
121. Cascino I, Fiucci G, Papoff G, et al. Three functional soluble forms of the human apoptosis-inducing Fas molecule are produced by alternative splicing. J Immunol 1995;154:2706-2713
122. Mariani SM, Matiba B, Baumler C, et al. Regulation of cell surface APO-1/Fas (CD95) ligand expression by metalloproteases. Eur J Immunol 1995;25:2303-2307
123. Lau HT, Yu M, Fontana A, et al. prevention of allograft rejection with engineered myoblasts expressing FasL in mice. Science 1996;273:109-112
124. Yagita H, Seino K, Kayagaki N, et al. CD95 ligand in graft rejection. Nature 1996;379:682
125. Allison J, Georgiou HM, Strasser A, et al. Transgeneic expression of CD95 ligand on islet β cells induces a granulocytic infiltration but does not confer immune privilege upon islet allografts. Proc Natl Acad Sci 1997;94:3943-3947
126. Kang S-M, Schneider DB, Lin Z, et al Fas ligand expression in islets of Langerhans does not confer immune privilege and instead targets them for rapid destruction. Nature Med 1997;3:738-743
127. Sato T, Irie S, Kitada S, et al. FAP-1 A protein tyrosine phosphatase that associates with Fas. Science 1995;268:411-415
128. Zhao M, Zhang NX, Economou M, et al. Immunohistochemical detection of bcl-2 protein in liver lesions: Bcl-2 protein is expressed in hepatocellular carcinomas but not in liver dysplasia. Histopathology 1994;25:237-245
129. Chiu VK, Walsh CM, Liu C-C, et al. Bcl-2 blocks degranulation but not fas-based cell mediated cytotoxicity. J Immunol 1995;154:2023-2032
130. Itoh N, Tsujimoto Y, Nagata S. Effect of bcl-2 on Fas antigenmediated cell death. J. Immunol 1993;151:621-627
131. Vaux DL, Aguila HL, Weissman IL. Bcl-2 prevents death of factor deprived cells but fails to prevent apoptosis in targets of cell-mediated killing. Int Immunol 1992;4:821-826
132. Lacronique V, Mignon A, Fabre M, et al. Bcl-2 protects from lethal hepatic apoptosis induced by an anti-Fas antibody in mice. Nat Med 1996;2:80-86
133. Rodriguez I, Matsuura K, Khatib K, et al. A bcl-2 transgene expressed in hepatocytes protects mice from fulminant liver destruction but not from rapid death induced by anti-Fas antibody injection. J Exp Med 1996;183:1031-1036