The liver as a site of T-cell apoptosis: Graveyard, or killing field?

Immunological Reviews

Volumn 174, Issue , 2000, Pages 47-62

  Crispe, I Nicholas ^a   Dao, Tao ^a   Klugewitz, Katja ^a   Mehal, Wajahat Z ^a   Metz, Daniela P ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; CD8 ANTIGEN; GAMMA INTERFERON;

ALLOGRAFT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIGENICITY; APOPTOSIS; CELL KILLING; CELL POPULATION; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; HEPATITIS C; HUMAN; IMMUNE RESPONSE; IMMUNOLOGICAL TOLERANCE; LEUKOCYTE COUNT; LIVER CIRCULATION; LIVER CLEARANCE; LIVER FUNCTION; LIVER TRANSPLANTATION; LYMPHOCYTE SUBPOPULATION; MOUSE; NATURAL KILLER CELL; NONHUMAN; PORTAL VEIN BLOOD; PRIORITY JOURNAL; REVIEW; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION;

ADOPTIVE TRANSFER; ANIMALS; ANTIGENS; ANTIGENS, CD95; APOPTOSIS; CD8-POSITIVE T-LYMPHOCYTES; CELL ADHESION; ENDOTHELIUM, VASCULAR; HEPATITIS C; HUMANS; IMMUNE TOLERANCE; IMMUNOPHENOTYPING; INTESTINAL ABSORPTION; KILLER CELLS, NATURAL; KUPFFER CELLS; LIVER; LIVER CIRCULATION; LIVER TRANSPLANTATION; LYMPHOCYTE ACTIVATION; LYMPHOCYTE SUBSETS; MICE; MICE, TRANSGENIC; MODELS, IMMUNOLOGICAL; PORTAL VEIN;

EID: 0034078355     PISSN: 01052896     EISSN: None     Source Type: Journal    
DOI: 10.1034/j.1600-0528.2002.017412.x     Document Type: Review

References (132)

1. 1. Crispe IN. Isolation of mouse intrahepatic lymphocytes. Current Protocols in Immunology 1996;3:22-28.
2. 2. Winnock M, et al. Human liver-associated lymphocytes: an overview. J Gastroenterol Hepatol 1995;10: S43-S46.
3. 3. Crispe IN, Mehal WZ. Strange brew: T cells in the liver. Immunol Today 1996;17:522-525.
4. 4. Itoh H, Abo T, Sugawara S, Kanno A, Kumagai K. Age related variation in the proportion and activity of murine liver natural killer cells and their cytotoxicity against regenerating hepatocytes. J Immunol 1988;141:315-327.
5. + cells in patients with malignancy. Clin Exp Immunol 1994;97:522-527.
6. 6. Hai T, et al. Ontogeny and development of extrathymic T cells in mouse liver. Immunology 1992;77:556-563.
7. + T cells in various immune organs. J Immunol 1995;155:2972-2983.
8. 8. Dao T, Mehal WZ, Crispe IN. IL-18 augments perforin-dependent cytotoxicity of liver NK-T cells. J Immunol 1998;161:2217-2222.
9. + T cell receptor αβ cells: new clues to their origin, specificity and function. J Exp Med 1995;182:633-638.
10. 10. Sugita M, et al. CD1-a new paradigm for antigen presentation and T cell activation. Clin Immunol Immunopathol 1998;87:8-14.
11. + thymocyte population associated with intact Fas antigen expression on the target. J Exp Med 1994;180:423-432.
12. 12. Dao T, Mehal WZ, Crispe IN. IL-18 augments perforin-dependent cytotoxicity of liver NK-T cells. J Immunol 1998;161:2217-2222.
13. + T cells produce large amounts of IL-4 and IFN-γ upon activation by anti-CD3 or CD1. J Immunol 1997;159:2240-2249.
14. - T cells in the normal mouse liver. Int Immunol 1994;6:533-540.
15. 15. Davidson WF, Dumont FJ, Bedigian HG, Fowlkes BJ, Morse HC. III. Phenotypic, functional, and molecular genetic comparisons of the abnormal lymphoid cells of C3H-1pr and C3H-gld/gld mice. J Immunol 1986;136:4075-4084.
16. 16. Crispe IN, Huang L. Neonatal, moribund and undead T cells. The role of the liver in T cell deletion. Semin Immunol 1994;6:39-41.
17. 17. Huang L, Soldevila G, Leeker M, Flavell RA, Crispe IN. Liver is the site of T cell destruction during peripheral deletion. Immunity 1994;1:741-749.
18. 18. Schonrich G, et al. Down-regulation of T cell receptors on self-reactive T cells as a novel mechanism for extrathymic tolerance induction. Cell 1991;65:293-304.
19. 19. Huang L, Crispe IN. Superantigen-driven peripheral deletion of T cells. Deletion occurs in cells which have lost the T cell antigen receptor. J Immunol 1993;151:1844-1851.
20. 20. 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.
21. 21. Iwakoshi NN, Goldschneider I, Tausche F, Mordes JP, Rossini AA. High frequency apoptosis of recent thymic emigrants in the liver of lymphopenic diabetes-prone BioBreeding rats. J Immunol 1998;160:5838-5850.
22. + T cells creates double-negative cells in vivo. J Immunol 1998;161:1686-1693.
23. 23. Crispe IN, Mehal WZ. Strange brew: T cells in the liver. Immunol Today 1996;17:522-525.
24. 24. Kearney ER, Pape KA, Loh DY, Jenkins ML. Visualisation of peptide-specific T cell immunity and peripheral tolerance induction in vivo. Immunity 1994;1:327-339.
25. + T cells triggered by high affinity peptide antigens. J Exp Med 1998;188:1147-1157.
26. + T cells inn the liver during the control and resolution phases of influenza pneumonia. Proc Natl Acad Sci USA 1998;95:13812-13817.
27. + T cell disposal. Eur J Immunol 1997;27:577-583.
28. 28. Koniaras C, Bennett SR, Carbone FR, Heath WR, Lew AM. Peptide-induced deletion of CD8 T cells in vivo occurs via apoptosis in situ. Int Immunol 1997;9:1601-1605.
29. 29. Ashwell G, Harford J. Carbohydrate-specific receptors of the liver. Annu Rev Biochem 1982;51:531-554.
30. 30. Dini L, Autuori F, Lentini A, Oliverio S, Piacentini M. The clearance of apoptotic cells in the liver is mediated by the asialoglycoprotein receptor. FEBS Letters 1992;296:174-178.
31. 31. Watanabe Y, Akaike T. Activation signal induced the expression of B cell specific CD45R epitope (6B2) on murine T cells. Scand J Immunol 1994;39:419-425.
32. 32. Lotan R, Belloni PN, Tressler RJ, Lotan D, Xu XC, Nicholson GL. Expression of galectins on microvessel endothelial cells and their involvement in tumour cell adhesion. Glycoconj J 1994;11:462-468.
33. 33. Perillo NL, Pace KE, Seilhamer JJ, Baum LG. Apoptosis of T cells mediated by galectin-1. Nature 1996;378:736-739.
34. 34. Martin SJ, et al. Early redistribution of plasma membrane phosphatidylserine is a general feature of apoptosis regardless of the initiating stimulus. J Exp Med 1995;182:1545-1557.
35. 35. Fadok VA, Voelker DR, Campbell PAS, Cohen JJ, Bratton DL, Henson PM. Exposure of phosphatidylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal by phagocytes. J Immunol 1992;148:2207-2216.
36. 36. Morita M, Watanabe Y, Akaike T. Inflammatory cytokines upregulate intercellular adhesion molecule-1 expression on primary cultured hepatocytes and T-lymphocyte adhesion. Hepatology 1994;19:426-431.
37. 37. Iigo Y, et al. Constitutive expression of ICAM-1 in rat microvascular systems analyzed by laser confocal microscopy. Am J Physiol 1997;273: H138-H147.
38. 38. Ohteki T, Okamoto S, Nakamura M, Nemoto E, Kumagai K. Elevated production of interleukin-6 by hepatic MNC correlates with ICAM-1 expression on the hepatic sinusoidal endothelial cells in autoimmune MRL-1pr mice. Immunol Lett 1993;36:145-152.
39. 39. Myers KJ, Eppihimer MJ, Hall L, Wolitzky B. Interleukin-12-induced adhesion molecule expression in murine liver. Am J Pathol 1998;152:457-468.
40. 40. El-Wahsh M, Fuller BJ, Sreekumar NS, Burroughs AK, Dhillon PA, Rolles KD. Correlation of ICAM-1 expression with postoperative acute cellular rejection in human liver allograft. Biochem Soc Trans 1997;25:500S.
41. 41. Takei Y, et al. Expression of ICAM-1 is involved in the mechanism of liver injury during liver transplantation: therapeutic usefulness of the F(ab')2 fragment of an anti-ICAM-1 monoclonal antibody. Transplant Proc 1996;28:1103-1105.
42. 42. Marubayashi S, et al. Protective effect of monoclonal antibodies to adhesion molecules on rat liver ischemia-reperfusion injury. Surgery 1997;122:45-52.
43. 43. Kuzume M, et al. A monoclonal antibody against ICAM-1 suppresses hepatic ischemia-reperfusion injury in rats. Eur Surg Res 1997;29:93-100.
44. 44. McNab G, Reeves JL, Salmi M, Hubscher S, Jalkanen S, Adams DH. Vascular adhesion protein 1 mediates binding of T cells to human hepatic endothelium. Gastroenterology 1996;110:522-528.
45. 45. Wong J, et al. A minimal role for selectins in the recruitment of leukocytes into the inflamed liver microvasculature. J Clin Invest 1997;99:2782-2790.
46. + T cells by the normal liver. J Immunol 1999;163:3202-3210.
47. 47. Pape KA, et al. Use of adoptive transfer of T-cell-antigen-receptor-transgenic T cells for the study of T cell activation in vivo. Immunol Rev 1997;156:67-78.
48. 48. Pardi R, Bender JR, Dettori C, Giannazza E, Engleman EG. Heterogeneous distribution and transmembrane signaling properties of lymphocyte function-associated antigen (LFA-1) in human lymphocyte subsets. J Immunol 1989;143:3157-3166.
49. 49. Bono P, Salmi M, Smith DJ, Jalkanen S. Cloning and characterization of mouse vascular adhesion protein-1 reveals a novel molecule with enzymatic activity. J Immunol 1998;160:5563-5571.
50. 50. Calne RY, et al. Induction of immunological tolerance by porcine liver allografts. Nature 1969;223:472-476.
51. 51. Kamada N, Teramoto K, Baguerizo A, Ishikawa M, Sumimoto R, Ohkouchi Y. Cellular basis of transplantation tolerance induced by liver grafting in the rat. Transplantation 1988;46:165-167.
52. 52. Kamada N, Davies HFS, Roser B. Reversal of transplantation immunity by liver grafting. Nature 1981;292:840-842.
53. 53. Kobayashi E, Kamada N, Enosawa S, Toyama N, Walker NI, Miyata M. Prevention by liver transplantation of the graft-versus-host reaction and allograft rejection in a rat model of small bowel transplantation. Transplantation 1994;57:177-181.
54. 54. Schlitt HJ, et al. Persistence of donor lymphocytes in liver allograft recipients. Transplantation 1993;56:1001-1007.
55. 55. Starzl TL, et al. Systemic chimerism in human female recipients of male livers. Lancet 1992;340:876-877.
56. 56. Thomson AW, Lu L, Murase N, Demetris AJ, Rao AS, Starzl TE. Microchimerism, dendritic cell progenitors and transplantation tolerance. Stem Cells 1995;13:622-639.
57. 57. Fu F, Li W, Lu L, Fung JJ, Thomson AW, Qian S. Treatment with CTLA4-Ig inhibits rejection of liver allografts from FIt3 ligand treated donors. Transplant Proc 1999;31:453.
58. 58. Boehme SA, Zheng L, Lenardo MJ. Analysis of the CD4 coreceptor and activation-induced costimulatory molecules in antigen mediated mature T lymphocyte death. J Immunol 1995;155:1703-1712.
59. 59. Radvanyi LG, et al. CD28 costimulation inhibits TCR-induced apoptosis during a primary T cell response. J Immunol 1996;156:1788-1798.
60. 60. Mathew JM, Marsh JW, Susskind B, Mohanakumar T. Analysis of T cell responses in liver allograft recipients. Evidence for deletion of donor-specific cytotoxic T cells in the peripheral circulation. J Clin Invest 1993;91:900-906.
61. 61. Qian S, et al. Apoptosis within spontaneously accepted mouse liver allografts: evidence for deletion of cytotoxic T cells and implications for tolerance induction. J Immunol 1997;158:4654-4661.
62. 62. Battisto JR, Miller J. Immunologic unresponsiveness produced in adult pigs by parenteral introduction of minute quantities of hapten or protein antigen. Proc Soc Exp Biol Med 1962;111:111-113.
63. 63. Cantor HM, Dumont AE. Hepatic suppression of sensitization to antigen absorbed into the portal vein. Nature 1965;215:744-745.
64. 64. Nagano H, et al. Mechanisms involved in immunosuppression induced by intraportal injection of antigen. Transplant Proc 1992;24:2900-2901.
65. 65. Nakano Y, Monden M, Valdevia LA, Gotoh M, Tono T, Mori T. Permanent acceptance of liver allografts by intraportal injection of donor spleen cells in rats. Surgery 1992;111:668-676.
66. 66. Goss JA, Flye MW, Lacy PE. Induction of allogeneic islet survival by intrahepatic islet pre-immunization and transient immunosuppression. Diabetes 1996;45:144-147.
67. 67. Fecteau A, Tchervenkov J, Guttman F, Takara T, Rosenmann E. Small bowel transplantation: the effects of intraportal donor-specific transfusion 24 hours pretransplant and low-dose cyclosporine. Transplantation 1994;58:399-402.
68. 68. Gorczynski RM, Fu XM, Chung S, Sullivan B, Chen Z. Manipulation of xenogeneic skin and/or renal graft survival in the rat-mouse concordant combination by portal vein pretransplant transfusion. Transplant Immunol 1995;3:321-329.
69. 69. Qian J-H, Hashimoto T, Fujiwara H, Hamaoka T. Studies on the induction of tolerance to alloantigens. I. The abrogation of potentials for delayed-type hypersensitivity reactions to alloantigens by portal venous innoculation of antigenic cells. J Immunol 1985;134:3656-3661.
70. 70. Gorczynski RM, Holmes W. Specific manipulation in vivo of immunity to skin grafts bearing multiple minor histocompatibility differences. Immunol Lett 1991;27:163-171.
71. 71. Gorczynski RM, Hozumi N, Wolf S, Chen Z. Interleukin 12 in combination with anti-interleukin 10 reverses graft prolongation after portal venous immunization. Transplantation 1995;60:1337-1341.
72. + hybridomas derived from mice preimmunized via the portal vein adoptively transfer increased skin allograft survival in vivo. J Immunol 1996;157:574-581.
73. 73. Gorczynski RM, Chen Z, Hoang Y, Rossi-Bergman B. A subset of γδ T-cell receptor-positive cells produce T-helper type-2 cytokines and regulate mouse skin graft rejection following portal venous pretransplant preimmunization. Immunology 1996;87:381-389.
74. 74. Gorczynski RM. Immunosuppression induced by hepatic portal venous immunization spares reactivity in IL-4 producing T lymphocytes. Immunol Lett 1992;33:67-77.
75. 75. Gorczynski RM, Wojcik D. A role for nonspecific (cyclosporin A) or specific (monoclonal antibodies to ICAM-1, LFA-1 and IL-10) immunomodulation in the prolongation of skin allografts after antigen-specific pre-transplant immunization or transfusion. J Immunol 1994;152:2011-2019.
76. 76. Yu S, Nakafusa Y, Flye MW. Portal vein adminstration of donor cells promotes peripheral allospecific hyporesponsiveness and graft tolerance. Surgery 1994;116:229-234.
77. 77. Lamb JR, Skidmore BJ, Green N, Chiller JM, Feldmann M. Induction of tolerance in influenza virus immune T lymphocyte clones with synthetic peptides of influenza haemagglutinin. J Exp Med 1983;157:1434-1447.
78. 78. Mueller DL, Jenkins MK, Schwartz RH. Clonal expansion vs functional clonal inactivation. Annu Rev Immunol 1989;7:445-480.
79. 79. Zubiaga AM, Munoz E, Huber BT. IL-4 and IL-2 selectively rescue Th cell subsets from glucocorticoid-induced apoptosis. J Immunol 1992;149:107-112.
80. 80. Mor F, Cohen IR. IL-2 rescues antigen-specific T cells from radiation or dexamethasone-induced apoptosis. Correlation with induction of Bcl-2. J Immunol 1996;156:515-522.
81. 81. Dao T, Huleatt JW, Hingorani R, Crispe IN. Specific resistance of T cells to CD95-induced apoptosis during S phase of the cell cycle. J Immunol 1997;159:4261-4267.
82. 82. Callery MP, Kamei T, Flye MW. Kupffer cell blockade inhibits induction of tolerance by the portal venous route. Transplantation 1989;47:1092-1094.
83. 83. Yu S, Nakafusa Y, Flye MW. In vitro analysis of gadolinium chloride abrogation of the systemic tolerance induced by portal venous administration of ultraviolet B-irradiated donor cells. Transplantation 1997;64:1684-1688.
84. 84. Roland CR, Mangino MJ, Duffy BF, Flye MW. Lymphocyte suppression by Kupffer cells prevents portal venous tolerance induction: a study of macrophage function after intravenous gadolinium. Transplantation 1993;55:1151-1158.
85. 85. Okamoto T, Maeda O, Tsuzuike N, Hara K. Effect of gadolinium chloride treatment on concanavalin A-induced cytokine mRNA expression in mouse liver. Jpn J Pharmacol 1998;78:101-103.
86. 86. Suzuki S, et al. Role of Kupffer cells and the spleen in modulation of endotoxin-induced liver injury after partial hepatectomy. Hepatology 1996;24:219-225.
87. 87. Rai RM, Yang SQ, McClain C, Karp CL, Klein AS, Diehl AM. Kupffer cell depletion by gadolinium chloride enhances liver regeneration after partial hepatectomy in rats. Am J Physiol 1996;270: G909-G918.
88. 88. Roland CR, Mangino MJ, Flye MW. Lanthanide "blockade" of antigen-presenting cells suppresses lymphocyte proliferation by inducing nitric oxide synthesis. J Surg Res 1993;54:401-410.
89. 89. Schönrich G, et al. Distinct mechanisms of extrathymic T cell tolerance due to differential expression of self antigen. Int Immunol 1992;4:581-590.
90. 90. Hämmerling GJ, et al. Non-deletional mechanisms of peripheral and central tolerance: studies with transgenic mice with tissue-specific expression of a foreign MHC class I antigen. Immunol Rev 1991;122:47-67.
91. 91. Morahan G, Brennan FE, Bhathal PS, Allison J, Cox KO, Miller JFAP. Expression in transgenic mice of class I histocompatibility antigens controlled by the metallothionein promoter. Proc Natl Acad Sci USA 1989;86:3782-3786.
92. b in the liver. Eur J Immunol 1995;25:1932-1942.
93. 93. Ferber I, Schonrich G. Schenkel J, Mellor AL, Hämmerling G, Arnold B. Levels of peripheral T cell tolerance induced by different doses of tolerogen. Science 1994;263:674-676.
94. 94. Schonrich G, et al. Tolerance induction as a multi-step process. Eur J Immunol 1994;24:285-293.
95. 51Cr-labeled human hepatocytes as target cells for cytotoxicity mediated by freshly-isolated liver-infiltrating lymphocytes. J Immunol Methods 1993;164:69-77.
96. 96. Pham BN, et al. Restriction of Vβ gene usage of liver-derived lymphocytes in chronic hepatitis B and C. Hum Immunol 1996;49:56-63.
97. 97. Vallbracht A, Fleischer B, Busch FW. Hepatitis A: hepatotropism and influence on myelopoiesis. Intervirology 1993;35:133-139.
98. 98. Gossmann J, Lohler J, Utermohlen O, Lehmann-Grube F. Murine hepatitis caused by lymphocytic choriomeningitis virus: II. Cells involved in pathogenesis. Lab Invest 1995;72:559-570.
99. + T lymphocytes lyse Listeria monocytogenes-infected hepatocytes by a classical MHC class I-restricted mechanism. J Immunol 1997;158:287-293.
100. 100. Mombaerts P, Arnoldi J, Russ F, Tonegawa S, Kaufman SH. Different roles of αβ and γδ T cells in immunity against an intracellular bacterial pathogen. Nature 1993;365:53-56.
101. + T cells is required for protective immunity against Plasmodium berghei. J Immunol 1996;156:3374-3381.
102. 102. Tsuji M, Mombaerts P, Lefrancois L, Nussenzweig RS, Zavala F, Tonegawa S. γδ T cells contribute to immunity against the liver stages of malaria in αβ T-cell-deficient mice. Proc Natl Acad Sci USA 1994;91:345-349.
103. 103. Brechot C. Hepatitis C virus: molecular biology and genetic variability. Dig Dis Sci 1996;41:6S-21S.
104. 104. Garson JA, Whitby K, Watkins P, Morgan AJ. Lack of susceptibility of the cottontop tamarin to hepatitis C infection. J Med Virol 1997;52:286-288.
105. 105. Neddermann P, Tomei L, Steinkuhler C, Gallinari P, Tramontano A, DeFrancesco R. The nonstructural proteins of the hepatitis C virus: structure and functions. Biol Chem 1997;378:469-476.
106. 106. Farci P, Orgiana G, Purcell RH. Immunity elicited by hepatitis C virus. Clin Exp Rheumatol 1995;13 (Suppl 13): S9-S12.
107. 107. Koziel MJ. The role of immune responses in the pathogenesis of hepatitis C virus infection. J Viral Hepat 1997;4 (Suppl 2):31-41.
108. 108. Weiner A, et al. Persistent hepatitis C virus infection in a chimpanzee is associated with emergence of a cytotoxic T lymphocyte escape variant. Proc Natl Acad Sci USA 1995;92:2755-2759.
109. 109. Weiner AJ, Erickson AL, Kansopon J, Crawford K, Muchmore E, Houghton M. Association of cytotoxic T lymphocyte (CTL) escape mutations with persistent hepatitis C virus (HCV) infection. Princess Takamatsu Symp 1995;25:227-235.
110. 110. Ferrari C, et al. T cell response to structural and non structural hepatitis C virus antigens in persistent and self limited hepatitis C virus infections. Hepatology 1994;19:268-295.
111. + T cell epitopes of hepatitis C virus and their relevance during the course of chronic infection. Hepatology 1995;21:632-638.
112. 112. Cerny A, et al. Cytotoxic T lymphocyte response to hepatitis C virus-derived peptides containing the HLA A2.1 binding motif. J Clin Invest 1995;95:521-530.
113. 113. Shirai M, et al. Induction of cytotoxic T cells to a cross-reactive epitope in the hepatitis C virus nonstructural RNA polymerase-like protein. J Virol 1992;66:4098-4106.
114. 114. Large MK, Kittlesen DJ, Hahn YS. Suppression of host immune response by the core protein of hepatitis C virus: possible implications for hepatitis C virus persistence. J Immunol 1999;162:931-938.
115. 115. Ogasawara J, et al. Lethal effects of the anti-Fas antibody in mice. Nature 1993;346:806-809.
116. 116. Ni R, et al. Fas-mediated apoptosis in primary cultured mouse hepatocytes. Exp Cell Res 1994;215:332-337.
117. 117. Rouquet N, Carlier K, Briand P, Wiels J, Joulin V. Multiple pathways of Fas-induced apoptosis in primary culture of hepatocytes. Biochim Biophys Res Commun 1996;229:27-35.
118. 118. Zheng TS, Schlosser SF, Dao T, Hingorani R, Crispe IN, Boyer JL, Flavell RA. Caspase-3 controls both cytoplasmic and nuclear events associated with Fas-mediated apoptosis in vivo. Proc Natl Acad Sci USA 1998;95:13618-13623.
119. 119. Cheng J, et al. Protection from Fas-mediated apoptosis by a soluble form of the Fas molecule. Science 1994;163:1759-1762.
120. 120. Cascino I, Fiucci G, Papoff G, Ruberti G. Three functional soluble forms of the human apoptosis-inducing Fas molecule are produced by alternative splicing. J Immunol 1995;154:2706-2713.
121. 121. Hughes DPM, Crispe IN. A soluble inhibitory isoform of murine Fas generated by alternative splicing. J Exp Med 1995;182:1395-1401.
122. 122. Kimura K, Wakatsuki T, Yamamoto M. A variant mRNA species encoding a truncated form of Fas antigen in rat liver. Biochim Biophys Res Commun 1994;198:666-672.
123. 123. Ferenbach DA, Haydon GH, Rae F, Malcomson RD, Harrison DJ. Alteration in mRNA levels of Fas splice variants in hepatitis C-infected liver. J Pathol 1997;183:299-304.
124. 124. Kondo T, Suda T, Fukuyama H, Adachi M, Nagata S. Essential roles of the Fas ligand in the development of hepatitis. Nat Med 1997;3:409-413.
125. 125. Ando K, et al. Perforin, Fas/Fas ligand, and TNF-α pathways as specific and bystander killing mechanisms of hepatitis C virus-specific human CTL. J Immunol 1997;158:5283-5291.
126. 126. 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.
127. 127. Bellgrau D, Gold D, Selawry H, Moore J, Franzusoff A. A role for CD95 ligand in preventing graft rejection [published erratum appears in Nature 1998;394:133]. Nature 1995;377:630-632.
128. 128. Hahne M, et al. Melanoma cell expression of Fas(Apo-1/CD95) ligand: implications for rumor immune escape. Science 1996;274:1363-1366.
129. 129. Nakamoto Y, Guidotti LG, Pasquetto V, Schreiber RD, Chisari FV. Differential target cell sensitivity to CTL-activated death pathways in hepatitis B virus transgenic mice. J Immunol 1997;158:5692-5697.
130. 130. Lenardo MJ. Interleukin-2 programs mouse αβ T lymphocytes for apoptosis. Nature 1991;353:858-861.
131. 131. Refaeli 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.
132. 132. Crispe IN. Fatal interactions: Fas in mature T cell deletion. Immunity 1994;1:347-349.