The significance of apoptosis in the liver

Liver

Volumn 19, Issue 6, 1999, Pages 453-463

  Benedetti, Antonio ^a   Marucci, Luca ^a  

^a UNIVERSITÀ POLITECNICA DELLE MARCHE   (Italy)

Author keywords

Alcoholic liver disease; Allograft rejection; Apoptosis; CCl4; Cholestasis; Mitochondria; Phagocytosis; Viral hepatitis; Wilson's disease

Indexed keywords

ALCOHOL LIVER DISEASE; APOPTOSIS; CHOLESTASIS; GRAFT REJECTION; LIVER TRANSPLANTATION; PATHOGENESIS; REVIEW; VIRUS HEPATITIS;

EID: 0033375042     PISSN: 01069543     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1478-3231.1999.tb00077.x     Document Type: Review

References (162)

1. TERADA T, NAKANUMA Y. Detection of apoptosis and expression of apoptosis-related proteins during human intrahepatic bile duct development. Am J Pathol 1995; 146: 67-74.
2. BENEDETTI A, JEZEQUEL A M, ORLANDI F. A quantitative evaluation of apoptotic bodies in rat liver. Liver 1988; 8: 172-7.
3. BENEDETTI A, JEZEQUEL A M, ORLANDI F. Preferential distribution of apoptotic bodies in acinar zone 3 of normal human and rat liver. J Hepatol 1988; 7: 319-24.
4. WYLLIE A H, KERR J F R, CURRIE A R. Cell death: the significance of apoptosis. Int Rev Cytol 1980; 68: 251-306.
5. WOODLE E S, KULKARNI S. Programmed cell death. Transplantation 1998; 66: 681-91.
6. EARNSHAW W C. Nuclear changes in apoptosis. Curr Opin Cell Biol 1995; 7: 337-43.
7. ASHKENAS J, WERB Z. Proteolysis and the biochemistry of life-or-death decision. J Exp Med 1996; 183: 1947-51.
8. HOWIE S E, HARRISON D J, WYLLIE A H. Lymphocyte apoptosis: mechanisms and implications in disease. Immunol Rev 1994; 142: 141-56.
9. HUGHES F M JR, EVANS-STORMS R B, CIDLOWSKI J A. Evidence that non-caspase proteases are required for chromatin degradation during apoptosis. Cell Death Differ 1998; 5: 1017-27.
10. HUGHES F M, CIDLOWSKI J A. Utilization of an in vitro assay to evaluate chromatin degradation by candidate apoptotic nucleases. Cell Death Differ 1997; 4: 200-20.
11. HUGHES F M, CIDLOWSKI J A. Apoptotic DNA degradation: evidence for novel enzymes. Cell Death Differ 1994; 1: 11-38.
12. SCHWARTZMAN R A, CIDLOWSKI J A. Apoptosis: the biochemistry and molecular biology of programmed cell death. Endocr Rev 1993; 14: 133-51.
13. WYLLIE A H. Glucocorticoid-induced thyrnocyte apoptosis is associated with endogenous endonuclease activation. Nature 1980; 284: 555-6.
14. COHEN J J, DUKE R C. Glucocorticoid activation of a calcium-dependent endonuclease in thymocyte nuclei leads to cell death. J Immunol 1984; 132: 38-42.
15. OBERHAMMER F, WILSON J W, DIVE C, et al. Apoptotic death in epithelial cells: cleavage of DNA to 300 and/or 50 kb fragments prior to or in the absence of internucleosomal fragmentation. EMBO J 1993; 12: 3679-84.
16. WALKER P R, KOKILEVA L, LEBLANC J, SIKORSKA M. Detection of the initial stages of DNA fragmentation in apoptosis. Biotechniques 1993; 15: 1032-40.
17. KOKILEVA L. Multi-step chromatin degradation in apoptosis. Int Arch Allergy Immunol 1994; 105: 339-43.
18. CAIN K, INAYAT-HUSSAIN H, WOLFE J T, COHEN G M. DNA fragmentation into 200-250 and/or 30-50 kilobase pair fragments in a rat liver nuclei is stimulated by Mg2+ alone and Ca2+/Mg2+ but not by Ca2+ alone. FEBS Lett 1994; 349: 385-91.
19. BEERE H M, CHRESTA C M, ALEJOHERBERG A, et al. Investigation of the mechanism of higher order chromatin fragmentation observed in drug-induced apoptosis. Mol Pharmacol 1995; 47: 986-96.
20. COHEN G M, SUN X M, FEARNHEAD H, et al. Formation of large molecular weight fragments of DNA is a key committed step of apoptosis in thymocytes. J Immunol 1994; 153: 507-16.
21. ORMEROD M G, O'NEIL C F, ROBERTSON D, HARRAP K R. Cisplatin induces apoptosis in a human ovarian carcinoma cell line without concomitant internucleosomal degradation of DNA. Exp Cell Res 1994; 211: 231-7.
22. APLIN A E, HOVE A, ALAHARI S K, JULIANO R L. Signal transduction and signal modulation by cell adhesion receptors: the role of integrins, cadherins, immunoglobulin-cell adhesion molecules, and selectins. Pharmacol Rev 1998; 50: 197-263.
23. MEREDITH J E JR, SCHWARTZ M A. Integrins, adhesion and apoptosis. Trends Cell Biol 1997; 7: 146-50.
24. MARZO I, BRENNER C, KROEMER G. The central role of the mitochondrial megachannel in apoptosis: evidence obtained with intact cells, isolated mitochondria and purified protein complexes. Biomed Pharmacother 1998; 52: 248-51.
25. GREEN R G, REED J C. Mitochondria and apoptosis. Science 1998; 281: 1309-12.
26. PETIT P X, SUSIN S A, ZAMZAMI B, MIGNOTTE B, KROEMER G. Mitochondria and programmed cell death: back to the future. FEBS Lett 1996; 396: 7-13.
27. LI P, BUDIHARDJO I, SRINIVASULA S M, AHMED M, ALNEMRI E S, WANG X. Cytochrome c and dATP-dependent formation of Apaf-1/caspase 9 complex initiates an apoptotic protease cascade. Cell 1998; 91: 479-89.
28. LI H, ZHU H, XU C J, YUAN J. Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathways of apoptosis. Cell 1998; 94: 491-501.
29. LUO X, BUDIHARDJO I, ZOU H, SLAUGHTER C, WANG X. Bid, a Bcl2 interactin protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors. Cell 1998; 94: 481-90.
30. LEMASTER J J. Mechanisms of hepatic toxicity. Necroapoptosis and mitochondrial permeability transition: shared pathways to necrosis and apoptosis. Am J Physiol 1999; 39: G1-6.
31. BRENNER C, MARZO I, KROEMER G. A revolution in apoptosis: from a nucleocentric to a mitochondriocentric perspective. Exp Gerontol 1998; 33: 543-53.
32. QIAN T, HERMAN B, LEMASTERS J J. The mitochondrial permeability transition mediates both necrotic and apoptotic death of hepatocytes exposed to Br-A23187. Toxicol Appl Pharmacol 1999; 154: 117-25.
33. ZAMZAMI N, SUSIN S A, MARCHETTI P, et al. Mitochondrial control of nuclear apoptosis. J Exp Med 1996; 183: 1533-44.
34. SHIMIZU S, EGUCHI Y, KAMIIKE W et al. Bcl-2 prevents apoptotic mitochondrial dysfunction by regulating proton flux. Proc Natl Acad Sci USA 1998; 95: 1455-9.
35. YANG J, LIU X, BHALLA K, et al. Prevention of apoptosis by Bcl-2: Release of cytochrome c from mitochondria blocked. Science 1997; 275: 1129-32.
36. ZHA H, FISK H A, YAFFE M P, MAHAJAN N, HERMAN B, REED J C. Structure function comparison of the proapoptotic protein Bax in yeast and mammalian cells. Mol Cell Biol 1996; 6494-508.
37. NARITA M, SHIMIZU S, ITO T, et al. Bax interacts with the permeability transition pore to induce permeability transition and cytochrome c release in isolated mitochondria. Proc Natl Acad Sci USA 1998; 95: 14681-6.
38. MARCHETTI P, HIRSCH T, ZAMZAMI N, et al. Mitochondrial permeability transition triggers lymphocyte apoptosis. J Immunol 1996; 157: 4830-6.
39. ZAMZAMI N, MARCHETTI P, CASTEDO M, et al. Inhibitors of permeability transition interfere with the disruption of mitochondrial transmembrane potential during apoptosis. FEBS Lett 1996; 384: 53-7.
40. SHIMIZU S, EGUCHI Y, KAMIIKE W, et al. Bcl-2 prevents apoptotic mitochondrial dysfunction by regulating proton flux. Proc Natl Acad Sci USA 1998; 95: 1455-9.
41. SAVILL J, FADOK V, HENSON P, HASLETT C. Phagocyte recognition of cells undergoing apoptosis. Immunol Today 1993; 14: 131-6.
42. SAVILL J. Recognition and phagocytosis of cells undergoing apoptosis. Br Med Bull 1997; 53: 491-508.
43. PLATT N, DA SILVA R P, GORDON S. Recognizing death: the phagocytosis of apoptotic cells. Trends Cell Biol 1998; 8: 365-72.
44. HALL S E, SAVILL J S, HENSON P M, HASLETT C. Apoptotic neutrophils are phagocytosed by fibroblasts with participation of the fibroblast vitronectin receptor and involvement of a mannose/fucose-specific lectin. J Immunol 1994; 153: 3218-27.
45. HESS K L, TUDOR K S, JOHNSON J D, OSATI-ASHTIANI F, ASKEW D S, COOK-MILLS J M. Human and murine high endothelial venule cells phagocytose apoptotic leukocytes. Exp Cell Res 1997; 236: 404-11.
46. HART S P, HASLETT C, DRANSFIELD I. Recognition of apoptotic cells by phagocytes. Experientia 1996; 52: 950-6.
47. ZWAAL R F, SCHROIT A J. Pathophysiologic implication of membrane phospholipid asymmetry in blood cells. Blood 1997; 89: 1121-32.
48. FRANC N C, DIMARCQ J L, LAGUEUX M, HOFFMANN S, EZEKOWITZ R A. Croquemort, a novel Drosophila hemocyte/macrophage receptor that recognizes apoptotic cells. Immunity 1996; 4: 431-43.
49. PEARSON A M. Scavenger receptors in innate immunity. Curr Opin Immunol 1996; 8: 20-8.
50. DEVITT A, MOFFATT O D, RAYKUNDALIA C, CAPRA J D, SIMMONS D L, GREGORY C D. Human CD14 mediates recognition and phagocytosis of apoptotic cells. Nature 1998; 392: 505-9.
51. PLATT N, SUZUKI H, KURIHARA Y, KODAMA T, GORDON S. Role of class A macrophage scavenger receptor in the phagocytosis of apoptotic thymocytes in vitro. Proc Natl Acad Sci USA 1996; 93: 12456-60.
52. REN Y, SILVERSTEIN R L, ALLEN J, SAVILL J. CD 36 gene transfer confers capacity for phagocytosis of cell undergoing apoptosis. J Exp Med 1995; 181: 1857-62.
53. SWANSON J A, BAER S C. Phagocytosis by zippers and triggers. Trends Cell Biol 1995; 5: 89-93.
54. BRAZIL M I, WEIB S, STOCKINGER B. Excessive degradation of intracellular proteins in macrophages prevents presentation in the contest of major histocompatibily complex class II molecules. Eur J Immunol 1997; 27: 1506-14.
55. ALBERT M L, SAUTER B, BHARDWAJ N. Dentritic cells acquire antigen from apoptotic cells and induce class-I-restricted CTLs. Nature 1998; 392: 86-9.
56. MAKER J J, GORES G J. Apoptosis: silent killer or neutron bomb? Hepatology 1998; 28: 865-7.
57. LEIST M, GANTNER F, NAUMANN H, et al. Tumor necrosis factor-induced apoptosis during the poisoning of mice with hepatotoxins. Gastroenterology 1997; 112: 923-34.
58. KONDO T, SUDA T, FUKUJAMA H, ADACHI M, NAGATA S. Essential roles of the Fas ligand in the development of hepatitis. Nat Med 1997; 3: 409-13.
59. SEKINE G, YAGITA H, KOBATA T, HUSUNUMA T, NISHIOKA K, OKUMURA K. Fas-mediated stimulation induces 11-8 secretion by rheumatoid arthritis synoviocytes independently of CPP32-mediated apoptosis. Biochem Biophys Res Commun 1996; 228: 14-20.
60. ABREU-MARTIN M T, VIDRICH A, LYNCH D H, TARGAN S R. Divergent induction of apoptosis and 11-8 secretion in HT-29 cells in response to TNF-alpha and ligation of Fas antigen. J Immunol 1995; 155: 4147-54.
61. CIFONE M G, RONCAIOLI P, D E MARIA R, et al. Multiple pathways originate at the Fas/APO-1 (CD95) receptor: sequential involvement of phosphatidylcholine-specific phospholipase C and acidic sphingomyelinase in the propagation of the apoptotic signal. EMBO J 1995; 14: 5859-68.
62. LAWSON J A, FISHER M A, SIMMONS C A, FARHOOD A, JAESCHKE H. Parenchymal cell apoptosis as a signal for sinusoidal sequestration and transendothelial migration of neutrophils in murine models of endotoxin and Fas-antibody-induced liver injury. Hepatology 1998; 28: 761-7.
63. VOLL R, HERRMANN M, ROTH A, STACH C, KALDEN J R, GIRKONTAITE I. Immunosuppressive effects of apoptotic cells. Nature 1997; 390: 351-2.
64. STRAZZABOSCO M, SPIRLÌ C, ZSEMBERY A, et al. Pathophysiology of the biliary epithelium. In: Vanishing bile duct syndrome. Pathophysiology and treatment. Eds: Alvaro D, Benedetti A, Strazzabosco M. Kluwer academic publishers, Dordrecht, The Netherlands 1996; 117-27.
65. JEZEQUEL A M, BENEDETTI A, BASSOTTI C, RAPINO K, ORLANDI F. Subcellular features of the biliary epithelium in health and disease. In: Vanishing bile duct syndrome. Pathophysiology and treatment. Eds: Alvaro D, Benedetti A, Strazzabosco M. Kluwer academic publishers, Dordrecht, The Netherlands 1996; 13-24.
66. QUE F G, GORES G J. Cell death by apoptosis: basic concepts and disease relevance for the gastroenterologist. Gastroenterology 1996; 110: 1238-43.
67. HARADA K, OZAKI S, GERSHWIN M E, NAKANUMA Y. Enhanced apoptosis relates to bile duct loss in primary biliary cirrhosis. Hepatology 1997; 26: 1399-405.
68. KOGA H, SAKISAKA S, OHISHI M, SATA M, TANIKAWA K. Nuclear DNA fragmentation and expression of Bcl-2 in primary biliary cirrhosis. Hepatology 1997; 25: 1077-84.
69. NAKANUMA Y, OHTA G, KONO N, KOBAYASHI K, KATO Y. Electron microscopic observation of destruction of biliary epithelium in primary biliary cirrhosis. Liver 1983; 3: 238-48.
70. AFFORD S C, HUBSCHER S, STRAIN A J, ADAMS D H, NEUBERGER J M. Apoptosis in the human liver during allograft rejection and end-stage liver disease. J Pathol 1995; 176: 373-80.
71. MARUCCI L, JEZEQUEL A M, BENEDETTI A. Biliary epithelium injury and death in primary biliary cirrhosis (PBC). J Hepatol 1999; Suppl 1: A105.
72. CELLI A, QUE F. Dysregulation of apoptosis in the cholangiopathies and cholangiocarcinoma. Liver Semin Dis 1998; 18: 177-86.
73. PATEL T, ROBERTS L R, JONES B A, GORES G J. Dysregulation of apoptosis as a mechanism of liver disease: an overview Semin Liver Dis 1998; 18: 105-14.
74. LICHTENHELD M G, OLSEN K J, LOWREY D M, HAMEED A, HENGARTNER H, PODACK E R. Structure and function of human perform. Nature 1988; 355: 448-51.
75. SMYTH M J, TRAPANI J A. Granzymes: exogenous proteinases that induce target cell apoptosis. Immunol Today 1995; 16: 202-6.
76. ORTIZ-ARDUAN A, DANOFF T M, KALLURI R, et al. Regulation of Fas and Fas-ligand expression in cultured murine renal cells and in the kidney during endotoxemia. Am J Physiol 1996; 271: F1193-201.
77. PATEL T, GORES G J. Inhibition of bile-salt-induced hepatocyte apoptosis by the antioxidant lazaroid U83836E. Toxicol Appl Pharmacol 1997; 142; 116-22.
78. RODRIGUES C M P, FAN G, MA X, KREN B T, STEER C J. A novel role for ursodeoxycholic acid in inhibiting apoptosis by modulating mitochondrial membrane perturbation. J Clin Invest 1998; 101: 2790-9.
79. PATEL T, BRONK S F, GORES G J. Increases of intracellular magnesium promote glycochenodeoxycholate-induced apoptosis in rathepatocytes. J Clin Invest 1994; 94: 2183-92.
80. SPIVEY J R, BRONK S F, GORES G J. Glycochenodeoxycholate-induced lethal hepatocellular injury in rat hepatocyte. J Clin Invest 1993; 92: 17-24.
81. FAUBION W A, GUICCIARDI M E, MIYOSHI H, et al. Toxic bile salts induce rodent hepatocyte apoptosis via direct activation of Fas. J Clin Invest 1999; 103: 137-45.
82. BEUERS U, BOYER J L, PAUMGARTNER G. Ursodeoxycholic acid in cholestasis: potential mechanisms of action and therapeutic applications. Hepatology 1998; 28: 1449-53.
83. GUICCIARDI M E, GORES G J. Is ursodeoxycholate an antiapoptotic drug? Hepatology 1998; 28: 1721-3.
84. BOTLA R, SPIVEY J R, AGUILAR H, BRONK S F, GORES G J. Ursodeoxycholate (UDCA) inhibits the mitochondrial membrane permeability transition induced by glycochenodeoxycholate: a mechanism of UDCA cytoprotection. J Pharmacol Exp Ther 1995; 272: 930-8.
85. RODRIGUEZ C M, FAN G, WONG P Y, KREN B T, STEER C J. Ursodeoxycholic acid may inhibit deoxycholic acid-induced apoptosis by modulating mitochondrial transmembrane potential and reactive oxygen species production. Mol Med 1998; 4: 165-78.
86. HSU Y T, YOULE R J. Nonionic detergents induce dimerization among members of the Bcl-2 family. J Biol Chem 1997; 272: 13829-34.
87. LIESER M J, PARK J, NATORI S, JONES B A, BRONK S F, GORES G J. Cholestasis confers resistance to the rat liver mitochondrial permeability transition. Gastroenterology 1998; 115: 693-701.
88. ALVARO D, ALPINI G, JEZEQUEL A M, et al. Role and mechanisms of action of acetylcholine in the regulation of cholangiocyte secretory functions. J Clin Invest 1997; 100: 1349-62.
89. LESAGE G, ALVARO D, BENEDETTI A, et al. Cholinergic system modulates growth, apoptosis and secretion of cholangiocytes from bile duct ligated rats. Gastroenterology 1999; 117: 191-9.
90. SLOMIANY A, PIOTROWSKI E, GRABSKA M, PIOTROWSKI, SLOMIANY B L. Chronic ethanol-initiated apoptosis in hepatocytes is induced by changes in membrane biogenesis and intracellular transport. Alcohol Clin Exp Res 1999; 23: 334-43.
91. KAWAHARA H, MATSUDA Y, TAKASE S. Is apoptosis involved in alcoholic hepatitis? Alcohol 1994; 29 (Suppl 1): 113-8.
92. SVEGLIATI BARONI G, MARUCCI L, BENEDETTI A. MANCINI R, JEZEQUEL A M, ORLANDI F. Chronic ethanol feeding increases the rate of apoptosis and cell proliferation in rat liver. J Hepatol 1994; 20: 508-13.
93. BENEDETTI A, BRUNELLI E, RISICATO R, CILLUFFO T, JEZEQUEL A M, ORLANDI F. Subcellular changes and apoptosis induced by ethanol in rat liver. J Hepatol 1988; 6: 137-43.
94. KUROSE I, HIGUCHI H, MIURA S, et al. Oxidative stress-mediated apoptosis of hepatocytes exposed to acute ethanol intoxication. Hepatology 1997; 25: 368-78.
95. HIGUCHI H, KUROSE I, KATO S, MIURA S, ISHII H. Ethanol-induced apoptosis and oxidative stress in hepatocytes. Alcohol Clin Exp Res 1996; 20: 340A-6.
96. DI LUZIO N R, HARTMAN A D. Role of lipid peroxidation in the pathogenesis of ethanol-induced fatty liver. Fed Proc 1967; 26; 1436-42.
97. ZIMMERMAN B T, CRAWFORD G D, DAHI R, SIMON F R, MAPOLES J E. Mechanisms of acetaldehyde-mediated growth inhibition: delayed cell cycle progression and induction of apoptosis. Alcohol Clin Exp Res 1995; 434-40.
98. SLATER T F, SAWYER B C, STRAULI U D. Changes in liver nucleotide concentration in experimental liver injury. 2. Acute ethanol poisoning. Biochem J 1964; 93: 267-70.
99. GARCIA R C, MORALES A, BALLESTRA A, RODES J, KAPLOWITZ N, FERNANDES C J C. Effect of chronic ethanol feeding on glutathione and functional integrity of mitochondria in periportal and perivenous rat hepatocytes. J Clin Invest 1994; 94: 193-201.
100. SADRZADEH S M H, NANJI A A, PRICE P L. The oral iron chelator, 1,2-dimethyl-3-hydroxypyrid-4-one reduces hepatic free iron, lipid peroxidation and fat accumulation in chronically ethanol-fed rats. J Pharmacol Exp Ther 1994; 269: 632-6.
101. LEIST M, GANTNER F, NAUMANN H, et al. Tumor necrosis factor-induced apoptosis during the poisoning of mice with hepatotoxins. Gastroenterology 1997; 112: 923-34.
102. LARRICK J W, WRIGHT S C. Cytotoxic mechanism of tumor necrosis factor-a. FASEB J 1990; 4: 3215-23.
103. OBERHAMMER F A, PAVELKA M, SHARMA S. Induction of apoptosis in cultured hepatocytes and in regressing liver by transforming growth factor 1. Proc Natl Acad Sci USA 1992; 89: 5408-12.
104. GRESSNER A M, POLZAR B, LAHME B, MANNHERZ H G. Induction of rat liver parenchymal cell apoptosis by hepatic myofibroblasts via transforming growth factor-β. Hepatology 1996; 23: 571-81.
105. OBERHAMMER F, BURSCH W, TIEFENBACHER R, et al. Apoptosis is induced by transforming growth factor-β1 within 5 hours in regressive liver without significant fragmentation of the DNA. Hepatology 1993; 18: 1238-46.
106. GALLE P R, HOFMANN W J, WALCZAK H, et al. Involvment of the CD95 (APO61/fas) receptor and ligand in liver damage. J Exp Med 1995; 182: 1223-30.
107. CHEDID A, MENDENHALL C L, MORITZ T E. et al. Cell-mediated hepatic injury in alcoholic liver disease. Gastroenterology 1993; 105: 254-62.
108. NANJI A A. Apoptosis and alcoholic liver disease. Semin Liver Dis 1998; 18: 187-90.
109. NEUMAN M G, SHEAR N H, BELLENTANI S, TIRIBELLI C. Role of cytokines in ethanol-induced cytotoxicity in vitro in Hep G2 cells. Gastroenterology 1998; 115: 157-66.
110. TEODORO J G, BRANTON P E. Regulation of apoptosis by viral gene products. J Virol 1997; 71: 1739-46.
111. LAU J Y N, XIE X, LAI M M C, WU P C. Apoptosis and viral hepatitis. Semin Liver Dis 1998; 18: 168-76.
112. RYO K, KAMOGAWA Y, IKEDA I. et al. Fas and FasL strongly expressed in liver of fulminant hepatitis patients (abstract). Hepatology 1995; 22: 230A.
113. FANG J W S, GONZALEZ-PERALTA R P, GOTTSCHALL J A, et al. Hepatic expression of c-Fas and apoptosis in chronic hepatitis C virus (HCV) infection (abstract). Hepatology 1994; 20: 251A.
114. HAYASHI P, MARRONE A, KLEINER D, et al. Hepatic apoptosis in chronic hepatitis C: Analysis by in situ terminal transferase labeling (TdTL) (abstract). Hepatology 1994; 20: 160A.
115. NAKAMOTO Y, GUIDOTTI L G, 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: 5692-7.
116. KONDO T, SUDA T, FUKUYAMA H, ADACHI M, NAGATA S. Essential roles of Fas ligand in the development of hepatitis. Nat Med 1997; 3; 409-13.
117. BHARDWAJ G, OHNO T, GISH R G, LAU J Y N. In vivo activation of cytotoxic T-lymphocyte (CTL) pathways in HCV-related cirrhosis-implications on immunopathogenesis (abstract) Hepatology 1996; 24: 374A.
118. ZHU N, KHOSHNAN A, SCHNEIDER R, et al. Hepatitis C virus core protein binds to the cytoplasmic domain of tumor necrosis factor (TNF) receptor 1 and enhances TNF-induced apoptosis. J Virol 1998; 72: 3691-7.
119. SHERON N, LAU J Y N, DANIELS H, et al. Increased production of tumor necrosis factor alpha in chronic HBV infection. J Hepatol 1991; 12: 241-5.
120. LIM H L, NELSON D R, FANG J W S, et al. The tumor necrosis factor-a system in chronic hepatitis C. Hepatology 1994; 20: 251A.
121. FANG J W S, SHEU W W, MEAGER A, LAU J Y N. Activation of the tumor necrosis factor-system in the liver in chronic hepatitis B virus infection. Am J Gastroenterol 1996; 91: 748-53.
122. SHERON N, LAU JYN, DANIELS HM, WESTEBER G, ALEXANDER GJM, WILLIAMS R. Tumor necrosis factor to treat chronic hepatitis B virus infection. Lancet 1990; 336: 321-9
123. BENEDETTI A, Di SARIO A, SVEGLIATI BARONI G, JEZEQUEL A M. Transforming growth factor beta 1 increases the number of apoptotic bodies and decreases intracellular pH in isolated periportal and perivenular rat hepatocytes. Hepatology 1995; 22: 1488-98.
124. CASTILLA A, PRIETO J, FAUSTO N. Transforming growth factors beta 1 and alpha in chronic liver disease-effects of interferon alpha therapy. N Engl J Med 1991; 324: 933-40.
125. YOO Y D, UEDA H, PARK K, et al. Regulation of transforming growth factor-beta 1 expression by the hepatitis B virus (HBV) X transactivator-role in HBV pathogenesis. J Clin Invest 1996; 97: 388-95.
126. KAKUMU S, ITO Y, TAKAYANAGI M, et al. Effect of recombinant human transforming factor beta 1 on immune responses with chronic hepatitis B. Liver 1993; 13: 62-8.
127. NELSON D R, GONZALEZ-PERALTA R P, QIAN K P, et al. Transforming growth factor-β1 in chronic hepatitis C. J Viral Hepat 1997; 4: 29-35.
128. CHIRILLO P, PAGANO S, NATOLI G, et al. The hepatitis B virus X gene induces p53-mediated programmed cell death. Proc Natl Acad Sci USA 1997; 94: 8162-7.
129. WANG X W, GIBSON M K, VERMEULEN W, et al. Abrogation of p-53-induced apoptosis by the hepatitis B virus X gene. Cancer Res 1995; 55: 6012-6.
130. PUISIEUX A, JI J, GUILLOT C, et al. p-53-mediated cellular response to DNA damage in cells with replicative hepatitis B virus. Proc Natl Acad Sci USA 1995; 92: 1342-1346.
131. TERRADILLO O, POLLICINO T, LOCOEUR H, et al. P53-independent apoptotic effect of hepatitis B virus HBx protein in vivo and in vitro. Oncogene 1998; 22: 2115-23.
132. KRAMS S M, MARTINEZ O M. Apoptosis as a mechanism of tissue injury in liver allograft rejection. Semin Liver Dis 1998; 18: 153-68.
133. BATTERSBY C, EGERTON W S. Another look at rejection in pig liver allografts. Surgery 1974; 76: 617-23.
134. NAWAZ S, FENNELL R H. Apoptosis of bile duct epithelial cells in hepatic allograft rejection. Histopathology 1994; 25: 137-42.
135. KRAMS S M, EGAWA H, QUINN M B, VILLANUEVA J C, GARCIA-KENNEDY R, MARTINEZ O M. Apoptosis as a mechanism of cell death in liver allograft rejection. Transplantation 1995; 59: 621-5.
136. KRAMS S M, VILLANUEVA J C. QUINN M B, MARTINEZ O M. Expression of the cytotoxic T cell mediator granzyme B during liver allograft rejection. Transpl Immunol 1995; 3: 162-6.
137. HAYASHI M, MARTINEZ O M, GARCIA-KENNEDY R, et al. Expression of cytokines and immune mediators during chronic liver allograft rejection. Transplantation 1995; 60: 1533-8.
138. LEGROS-MAIDA S, SOULIE A, BENVENUTI C, et al. Granzyme B and perforin can be used as predictive markers of acute rejection in heart transplantation. Eur J Immunol 1994; 24: 229-33.
139. LIPMAN M I, STEVENS A C, STROM T B. Heightened intragraft cytotoxic T-lymphocyte gene expression in acutely rejecting renal allografts. J Immunol 1994; 152: 5120-7.
140. SHARMA V K, BOLOGA R M, 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: 1860-6.
141. GRAUBERT T A, RUSSEL J H, LEY T J. The role of granzyme B in murine models of acute graft-versus-host disease and graft rejection. Blood 1996; 87: 1232-7.
142. AHMER K R, GUO T B, GAAL K K. Islet rejection in perforin-deficient mice. Transplantation 1997; 63: 951-7.
143. SELVAGGI G, RICORDI C, PODACK E R, INVERARDI L. The role of perforin and Fas pathways of cytotoxicity in skin graft rejection. Transplantation 1996; 62: 1912-5.
144. SCHULZ M, SCHUURMAN H J, JOERGENSEN J, et al. Acute rejection of vascular heart allografts by perf orin-deficient mice. Eur J Immunol 1995; 25: 474-80.
145. TANNAPFEL A, KOHLHAW K, SCHWARZ R, et al. Apoptosis and the expression of Fas and Fas-ligand antigen after orthotopic liver transplantation. Transplant Proc 1998; 30: 2358-9.
146. LARSEN C P, ALEXANDER D Z, HENDRIX R, et al. Fas-mediated cytotoxicity. An immunoeffector or immunoregulatory pathway in T cell-mediated immune response? Transplantation 1995; 60: 221-4.
147. CHENG J, ZHOU T, LIU C, et al. Protection from Fas-mediated apoptosis by a soluble form of Fas molecule. Science 1994; 263: 1759-62.
148. 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: 2706-13.
149. KRAMS S M, FOX C K, BEATTY P R, et al. Human hepatocytes produce an isoform of Fas which inhibits apoptosis. Transplantation 1998; 65: 713-21.
150. MEYER D, BAUMGARDT S, LOHFFELER S, et al. Apoptosis of T lymphocytes in liver and/or small bowel allografts during tollerance induction. Transplantation 1998; 66: 1530-1536.
151. QIAN S, LU L, FU F, et al. Apoptosis within spontaneously accepted mouse liver allografts. J Immunol 1997; 158: 4654-61.
152. th edition, New York 1995; 4125-4158.
153. AUST S D, MOREHOUSE L A, THOMAS CE. Role of metals in oxygen radical reactions. Free Radic Biol Med 1985; 1: 3-25.
154. VIERLING J M. Copper metabolism in primary biliary cirrhosis. Semin Liver Dis 1981; 293-308.
155. STRAND S, HOFMANN W J, GRAMBIHLER A, et al. Hepatic failure and liver cell damage in acute Wilson's disease involve CD95 (APO-1/Fas) mediated apoptosis. Nat Med 1998; 4: 588-93.
156. LESAGE G, BENEDETTI A, GLASER S S, et al. Acute carbon tetrachloride feeding selectively damages large, but not small, cholangiocytes from normal rat liver. Hepatology 1999; 29: 307-19.
157. LESAGE G, GLASER S S, MARUCCI L, et al. Acute carbon tetrachloride feeding induces damage of large but not small cholangiocytes from bile duct ligated rat liver. Am J Physiol 1999; 276: G1289-301.
158. IREDALE J P, BENYON RC, PICKERING J, et al. Mechanisms of spontaneous resolution of rat liver fibrosis. Hepatic stellate cell apoptosis and reduced hepatic expression of metalloproteinase inhibitors. J Clin Invest 1998; 102: 538-49.
159. 2+ antagonists inhibit DNA fragmentation and toxic cell death induced by acetaminophen. FASEB J 1993; 7: 453-63.
160. CASCALES M, ALVAREZ A, GASCO P, FERNANDEZ SIMON L, SANZ N, BOSCA L. Cocaine-induced liver injury in mice elicits specific changes in DNA ploidy and induces programmed death of hepatocytes. Hepatology 1994; 20: 992-1001.
161. 2+-endonuclease and poly(ADP-ribose) poly-merase inhibitors in mice. J Pharmacol Exp Ther 1992; 263: 387-94.
162. FELDMANN G. Liver apoptosis. J Hepatol 1997; 26 (Suppl 2): 1-11.