Apoptosis in normal and diseased liver;L'apoptose dans le foie normal et pathologique

Gastroenterologie Clinique et Biologique

Volumn 22, Issue 4, 1998, Pages 381-393

  Guettier, Catherine ^a,b   Ziol, Marianne ^a,b  

^a HÔPITAL JEAN VERDIER   (France)

^b UNIVERSITÉ PARIS 13   (France)

Author keywords

Apoptosis; Bcl 2; Chronic Hepatitis; Fas; Hepatocellular carcinoma; Liver; p53

Indexed keywords

DNA; FAS ANTIGEN; PROTEIN BCL 2; PROTEIN P53;

ALCOHOL LIVER DISEASE; APOPTOSIS; BILIARY TRACT DISEASE; GENE CONTROL; HUMAN; LIVER CELL CARCINOMA; LIVER DISEASE; LIVER TRANSPLANTATION; ONCOGENE C MYC; REVIEW; SEPSIS; TOXIC HEPATITIS; TUMOR SUPPRESSOR GENE; VIRUS HEPATITIS;

ANIMALS; APOPTOSIS; GENES, BCL-2; GENES, MYC; GENES, P53; HUMANS; LIVER; LIVER DISEASES;

EID: 0031837522     PISSN: 03998320     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (128)

1. Kerr JF, Wyllie AH, Currie AR. Apoptosis: a basic biological phenomenon with wideranging implications in tissue kinetics. Br J Cancer 1972;26:239-57.
2. Kerr JFR, Winterford CM, Harmon BV. Apoptosis. Its significance in cancer and cancer therapy. Cancer 1994;73:2013-26.
3. Ledda-Colombano GM, Coni P, Curto M, Giacomini L, Faa G, Oliviero S, et al. Induction of two different modes of cell death, apoptosis and necrosis, in rat liver after a single dose of thioacetamide. Am J Pathol 1991;139:1099-109.
4. Galle PR, Hofmann WJ, Walczak H, Schaller H, Otto G, Stremmel W, et al. Involvement of the CD95 (APO-1/Fas) receptor and ligand in liver damage. J Exp Med 1995;182:1223-30.
5. Guilhot S, Miller T, Cornman G, Isom HC. Apoptosis induced by tumor necrosis factor-alpha in rat hepatocyte cell lines expressing hepatitis B virus. Am J Pathol 1996;148:801-14.
6. Oberhammer FA, Pavelka M, Sharma S, Tiefenbacher R, Purchio AF, Bursh W, et al. Induction of apoptosis in cultured hepatocytes and in regressing liver by transforming growth factor beta-1. Proc Natl Acad Sci USA 1992;89:5408-12.
7. Hiramitsu N, Hayashi N, Katayama K, Mochizuki K, Kawanishi Y, Kasahara A, et al. Immunohistochemical detection of Fas antigen in liver tissue of patients with chronic hepatitis C. Hepatology 1994;19:1354-9.
8. Itoh N, Yonehara S, Ishii A, Yonehara M, Mizushima S, Sameshima M, et al. The polypeptide encoded by the cDNA for human cell surface antigen Fas can mediate apoptosis. Cell 1991;66:233-43.
9. Leist M, Gantner F, Kunstle G, Bohlinger I, Tiegs G, Bluethmann H, et al. The 55-kD tumor necrosis factor receptor and CD95 independently signal murine hepatocyte apoptosis and subsequent liver failure. Mol Med 1996;2:109-24.
10. Watanabe-Fukunaga R, Brannan CI, Itoh N, Yonehara S, Copeland NG, Jenkins NA, et al. The cDNA structure, expression and chromosomal assignment of the mouse Fas antigen. J Immunol 1992;148:1274-9.
11. Leithäuser F, Dhein J, Mechtersheimer G, Koretz K, Brüdelein S, Henne C, et al. Constitutive and induced expression of APO-1, a new member of the NGF/TNF receptor superfamily, in normal and neoplastic cells. Lab Invest 1993;69:415-29.
12. Suda T, Nagata S. Purification and characterization of the Fas-ligand that induces apoptosis. J Exp Med 1994;179:873-9.
13. Goldstein P. Deux mécanismes moléculaires pour la cytotoxicité T: perforine/granzymes et Fas. Médecine/Science 1995;11:99-104.
14. Nagata S, Golstein P. The Fas death factor. Science 1995;167:1449-55.
15. Lacronique V, Mignon A, Fabre M, Viollet B, Rouquet N, Molina T, et al. Bcl-2 protects from lethal hepatic apoptosis induced by an anti-Fas antibody in mice. Nature Med 1996;2:80-6.
16. Bour ES, Ward LK, Cornman GA, Isom HC. Tumor necrosis factor-alpha-induced apoptosis in hepatocytes in long-term culture. Am J Pathol 1996;148:485-95.
17. Leist M, Gantner F, Bohlinger I, Tiegs G, Germann PG, Wendel A. Tumor necrosis factor-induced hepatocyte apoptosis precedes liver failure in experimental murine shock models. Am J Pathol 1995;146:1220-34.
18. Adachi Y, Bradford BU, Gao W, Bojes HK, Thurman RG. Inactivation of Kupffer cells prevents early alcohol-induced liver injury. Hepatology 1994;20:453-60.
19. Laskin DL, Gardner CR, Price VF, Jollow DJ. Modulation of macrophage functioning abrogates the acute hepatotoxicity of acetaminophen. Hepatology 1995;21:1045-50.
20. Satoh M, Yamazaki M. Tumor necrosis factor stimulates DNA synthesis of mouse hepatocytes in primary culture and is suppressed by transforming growth factor beta and interleukin 6. J Cell Physiol 1992;150:134-9.
21. Roulot D, Durand H, Coste T, Rautureau J, Strosberg AD, Benarous R, et al. Quantitative analysis of transforming growth factor beta-1 messenger RNA in the liver of patients with chronic hepatitis C: absence of correlation between high levels and severity of disease. Hepatology 1995;21:298-304.
22. Gressner AM, Polzar B, Lahme B, Mannherz HG. Induction of rat liver parenchymal cell apoptosis by hepatic myofibroblasts via transforming growth factor beta. Hepatology 1996;23:571-81.
23. Schwall R, Robbins K, Jardieu P, Chang L, Lai C, Terrell T. Activin induces cell death in hepatocytes in vitro and in vivo. Hepatology 1993;18:347-56.
24. Liu CC, Young LHY, Young JDE. Lymphocyte-mediated cytolysis and disease. N Engl J Med 1996;335:1651-9.
25. Heusel JW, Wesselschmidt RL, Shresta S, Russell JH, Ley TJ. Cytotoxic lymphocytes require granzyme B for the rapid induction of DNA fragmentation and apoptosis in allogeneic target cells. Cell 1994;76:977-87.
26. Martin A. Le gène suppresseur de tumeur p53. Ann Pathol 1995;15:178-83.
27. Donehover LA, Harvey M, Slagle BL, McArthur MJ, Montgomery Jr CA, Butel JA, et al. Mice deficient for p53 are developmentally normal but susceptible to spontaneous tumors. Nature 1992;356:215-21.
28. Oberhammer F, Wilson JW, Dive C, Morris ID, Hickman JA, Wakeling AE, et al. Apoptotic death in epithelial cells: cleavage of DNA to 300 and/or 50 kb prior to or in the absence of internucleosomal fragmentation. EMBO J 1993;12:3679-84.
29. Salomon RN, Diaz-Cano S. Introduction to apoptosis. Diagn Mol Pathol 1995;4:235-8.
30. Anzai N, Kawabata H, Hirama T, Masutani H, Ueda Y, Yoshida Y, et al. Types of nuclear endonuclease activity capable of inducing internucleosomal DNA fragmentation are completely different between human CD34 + cells and their granulocytic descendants. Blood 1995;86:917-23.
31. Schulze-Osthoff K, Walczak H, Dröge W, Krammer P. Cell nucleus and DNA fragmentation are not required for apoptosis. J Cell Biol 1994;127:15-20.
32. Alnemri ES, Livingston DJ, Nicholson DW, Salvesen G, Thornberry NA, Wong WW, et al. Human ICE/CED3 protease nomenclature. Cell 1996;87:171-8.
33. Zamzani N, Susin SA, Marchetti P, Hirsch T, Gomez-Monterrey I, Castedo M, et al. Mitochondrial control of nuclear apoptosis. J Exp Med 1996;183:1533-44.
34. Kroemer G, Zamzani N, Susin SA. Mitochondrial control of apoptosis. Immunol Today 1997;18:44-51.
35. Kumar S, Lavin MF. The ICE family of cysteine proteases as effectors of cell death. Cell Death Different 1996;3:255-67.
36. Bredesen DE. Neural apoptosis. Ann Neurol 1995;38:839-51.
37. Watson AJM, Askew JN, Benson RSP. Poly(adenosine diphosphate ribose) polymerase inhibition prevents necrosis induced by H202 but not apoptosis. Gastroenterology 1995;109:472-82.
38. Rouquet N, Pagès JC, Molina T, Briand P, Joulin V. ICE inhibitor YVADcmk is a potent therapeutic agent against in vivo liver apoptosis. Current Biology 1996;6:1192-5.
39. Nagata S. Apoptosis by death factor. Cell 1997;88:355-65.
40. Feldmann G. L'apoptose ou la mort cellulaire programmée. Ann Pathol 1995;15:92-109.
41. Patel T, Gores GJ. Apoptosis and hepatobiliary disease. Hepatology 1995;21:1725-41.
42. Savill J, Fadok V, Henson P, Haslett C. Phagocyte recognition of cells undergoing apoptosis. Immunol Today 1993;14:131-6.
43. Scoazec JY. La mort des cellules hépatiques. Hépato-Gastro 1996;4:45-57.
44. Peled A, Zipori D, Rotter V. Cooperation between p53-dependent and p53-independent apoptotic pathways in myeloid cells. Cancer Res 1996;56:2148-56.
45. Miyashita T, Reed JC. Tumor suppressor p53 is a direct transcriptional activator of the human bax gene. Cell 1995;80:293-9.
46. Owen-Schaub LB, Zhang W, Cusack JC, Angelo LS, Santee SM, Fujiwara T, et al. Wild-type human p53 and a temperature-sensitive mutant induce Fas/APO-1 expression. Mol Cell Biol 1995;15:3032-40.
47. Berges RR, Furuya Y, Remington L, English HF, Jacks T, Isaacs JT. Cell proliferation, DNA repair and p53 function are not required for programmed death of prostatic glandular cells induced by androgen ablation. Proc Acad Natl Sci USA 1993;90:8910-4.
48. Strasser A, Harris AW, Jacks T, Cory S. DNA damage can induce apoptosis in proliferating lymphoid cells via p53-independent mechanisms inhabitable by bcl-2. Cell 1994;79:329-39.
49. Tsujimoto Y, Finger LR, Yunis J, Nowell PC, Croce CM. Cloning of the chromosomal breakpoint of neoplastic B-cells with the (14-18) chromosome translocation. Science 1984;226:1097-9.
50. Krajewski S, Tanaka S, Takayama S, Schibler MJ, Fenton W, Reed JC. Investigation of the subcellular distribution of the bcl-2 oncoprotein: residence in the nuclear envelope, endoplasmic reticulum, and outer mitochondrial membrane. Cancer Res 1993;53:4701-14.
51. Lu QL, Abel P, Foster CS, Lalani EN. Bcl-2: role in epithelial differentiation and oncogenesis. Hum Pathol 1996;27:102-10.
52. Miyashita T, Krajewski S, Krajewska M, Wang HG, Lin HK, Liebermann DA, et al. Tumor suppressor p53 is a regulator of bcl-2 and bax in gene expression in vitro and in vivo. Oncogene 1994;9:1799-805.
53. Soubeyran P, Soubeyran I. Bcl-2 et apoptose. Ann Pathol 1995;15:89-91.
54. Charlotte F, L'Herminé A, Martin N, Geleyn Y, Nollet M, Gaulard P, et al. Immunohistochemical detection of bcl-2 protein in normal and pathological human liver. Am J Pathol 1994;144:460-5.
55. Krajewski S, Krajewska M, Shabaik A, Miyashita T, Wang HG, Reed JC. Immunohistochemical determination of in vivo distribution of bax, a dominant inhibitor of bcl-2. Am J Pathol 1994;145:1323-36.
56. Reed JC. Bcl-2 and the regulation of programmed cell death. J Cell Biol 1994;124:1-6.
57. Cummings MC, Winterford CM, Walker NI. Apoptosis. Am J Surg Pathol 1997;21:88-101.
58. Bursch W, Paffe S, Putz B, Barthel C, Schulte-Hermann R. Determination of the length of the histological stages of apoptosis in normal liver and in altered hepatic foci of rats. Carcinogenesis 1990;11:847-53.
59. Staunton MJ, Gaffney EF. Tumor type is a determinant of susceptibility to apoptosis. Am J Clin Pathol 1995;103:300-7.
60. Willie AH. Glucocorticoid-induced thymocyte apoptosis is associated with endogenous endonuclease activation. Nature 1980;284:555-6.
61. Oberhammer F, Bursch W, Tiefenbacher R, Froschl RTG, Pavelka M, Purchio T, et al. Apoptosis is induced by transforming growth-factor beta within 5 hours in regressing liver without significant fragmentation of the DNA. Hepatology 1993;18:1238-46.
62. Brown DG. Dexamethasone-induced apoptosis involves cleavage of DNA to large fragments prior to internucleosomal fragmentation. J Biol Chem 1993;268:3037-9.
63. Lizard G, Miguet C, Gueldry S, Monier S, Gambert P. Mise en évidence de la fragmentation d'ADN par cytométrie en flux au cours de la mort cellulaire par apoptose. Nouvelles techniques d'évaluation de l'état de l'ADN pour le pathologiste. Ann Pathol 1997;17:61-6.
64. Gavrieli Y, Sherman Y, Ben Sasson SA. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J Cell Biol 1992;119:493-501.
65. Wijsman JH, Jonker RR, Keijzer R, Van de Velde CJH, Cornelisse CJ, Van Dierendonck JH. A new method to detect apoptosis in paraffin sections: in situ end-labeling of fragmented DNA. J Histochem Cytochem 1993;41:7-12.
66. Gold R, Schmied M, Giegerich G, Breitschopf H, Hartung HP, Toyka KV, et al. Differentiation between cellular apoptosis and necrosis by the combined use of in situ tailing and nick translation techniques. Lab Invest 1994;71:219-25.
67. Mundle SD, Raza AA, Gold R, Schmied M, Giegerich G, Breitschopf H, et al. The two in situ techniques do not differentiate between apoptosis and necrosis but rather reveal distinct patterns of DNA fragmentation in apoptosis. Lab Invest 1995;72:611-3.
68. Migheli A, Attanasio A, Schiffer D. Ultrastructural detection of DNA strand breaks in apoptotic neural cells by in situ end-labelling techniques. J Pathol 1995;176:27-35.
69. Nakajima T, Degushi T, Kagawa K, Hikita H, Ueda K, Katagishi T, et al. Identification of apoptotic hepatocytes in situ in rat liver after lead nitrate administration. J Gastroenterol 1995;30:725-30.
70. Grasl-Kraupp B, Ruttkay-Nedecky B, Koudelka H, Bukowska K, Bursch W, Schulte-Hermann R. In situ detection of fragmented DNA (TUNEL assay) fails to discriminate among apoptosis, necrosis, and autolytic cell death: a cautionary note. Hepatology 1995;21:1465-8.
71. Lin JK, Chou CK. In vitro apoptosis in the human hepatoma cell line induced by transforming growth factor beta 1. Cancer Res 1992;52:385-8.
72. Bursch W, Oberhammer F, Jirtle RL, Askari M, Grasl-Kraupp B, Purchio AEA. Transforming growth factor beta 1 as a signal for induction of cell death by apoptosis. Br J Cancer 1993;67:531-6.
73. Adashi M, Suematsu S, Kondo T, Ogasawara J, Tanaka T, Yoshida N, et al. Targeted mutation in the Fas gene causes hyperplasia in peripheral lymphoid organs and liver. Nature Genet 1995;11:294-300.
74. Gantner F, Leist M, Jilg S, Germann PG. Tumor necrosis factor-induced hepatic DNA fragmentation as an early marker of T cell-dependent liver injury in mice. Gastroenterology 1995;109:166-76.
75. Kondo T, Suda T, Fukuyama H, Adachi M, Nagata S. Essential roles of the Fas ligand in the developement of hepatitis. Nature Med 1997;3:409-13.
76. Ayala A, Urbanich MA, Herdon CD, Chaudry IH. Is sepsis-induced apoptosis associated with macrophage dysfunction? J Trauma 1996;40:568-74.
77. Ferrari C, Chisari FV. Immune mechanisms of cellular injury in viral hepatitis. In: Arias IM, Boyer JL, Fausto N, Jakoby WB, Schachter DA, Shafritz DA, eds. The liver: biology and pathobiology. New York: Raven Press 1994:1413-27.
78. Rehermann B. Immunopathogenesis of viral hepatitis. Baillière's Clin Gastroenterol 1996;10:483-500.
79. Lowin B, Hahne M, Mattman C, Tschopp J. Cytolytic T-cell cytotoxicity is mediated through perforin and Fas lytic pathways. Nature 1994;370:650-2.
80. Kägi D, Vignaux F, Ledermann B, Bürki K, Depraetere V, Nagata S, et al. Fas and perforin pathways as major mechanisms of T cell-mediated cytotoxicity. Science 1994;265:528-30.
81. Okazabi M, Hino K, Fujii K, Hanada H, Nakanishi Y, Kanazawa S, et al. Immunohistochemical study of Fas antigen in liver of patients with chronic hepatitis and autoimmune liver disease. Internat Hepatol Commun 1995;3:285-9.
82. Mochizuki K, Hayashi N, Hiramatsu N, Katayama Y, Kasahara A, Fusamoto H, et al. Fas antigen expression in liver tissues of patients with chronic hepatitis B. J Hepatol 1996;24:1-7.
83. Mita E, Hayashi N, Iio S, Takehara T, Hijioka T, Kasahara A, et al. Role of Fas ligand in apoptosis induced by hepatitis C virus infection. Biochem Biophys Res Commun 1994;204:468-74.
84. Watanabe Y, Morita M, Akaike T. Concanavalin A induces perforin-mediated but not Fas-mediated hepatic injury. Hepatology 1996;24:702-10.
85. Nakamoto Y, Guidotti LG, Chisari FV. CTL-induced liver disease requires co-stimulation of both Fas ligand- and perforine-activated death pathway (abstract). Hepatology 1996;24:351A.
86. Czaja AJ. Autoimmune hepatitis. Dig Dis Sci 1996;40:435-56.
87. Sheron N, Lau J, Daniels H, Goka J, Eddleston A, Alexander GJM, et al. Increased production of tumour necrosis factor-alpha in chronic hepatitis B virus infection. J Hepatol 1991;12:241-5.
88. Nakamura K, Yuh K, Sugyo S, Shijo H, Kimura N, Okumura M. Apoptosis observed in peripheral T lymphocytes from patients with chronic hepatitis B. Gastroenterology 1996;111:156-64.
89. Bernuau D, Feldmann G, Degott C, Gisselbrecht C. Ultrastructural lesions of bile ducts in primary biliary cirrhosis. A comparison with lesions observed in graft versus host disease. Hum Pathol 1981;12:782-93.
90. Nakanuma Y, Tsuneyama K, Gershwin ME, Yasoshima M. Pathology and immunopathology of primary biliary cirrhosis with emphasis on bile duct lesions: recent progress. Semin Liver Dis 1995;15:313-28.
91. Patel T, Bronk S, Gores G. Increases of intracellular magnesium promote glycodeoxycholate-induced apoptosis in rat hepatocytes. J Clin Invest 1994;94:2183-92.
92. Rosser BG, Gores GJ. Liver cell necrosis: cellular mechanisms and clinical implications. Gastroenterology 1995;108:252-75.
93. Snover DC, Sibley RK, Freese DK, Sharp HL, Bloomer JR, Najarian JS, et al. Orthotopic liver transplantation: a pathological study of 63 serial liver biopsies from 17 patients with special reference to the diagnostic features and natural history. Hepatology 1984;4:1212-22.
94. Vierling J, Fennell RH. Histopathology of early and late human hepatic allograft rejection: evidence of progressive destruction of interlobular bile ducts. Hepatology 1985;5:1076-82.
95. ++ accumulation and early DNA fragmentation with cell death. Toxicol Appl Pharmacol 1991;111:242-54.
96. Yacoub LK, Fogt F, Griniuviene B, Nanji AA. Apoptosis and Bcl-2 protein expression in experimental alcoholic liver disease in the rat. Alcohol Clin Exp Res 1995;19:854-9.
97. Baroni GS, Marucci L, Benedetti A, Mancini R, Jezequel AM, Orlandi F. Chronic ethanol feeding increases apoptosis and cell proliferation in rat liver. J Hepatol 1994;20:508-13.
98. Halsted CH, Villanueva J, Chandler CJ, Stabler SP, Allen RH, Muskhelishvili L, et al. Ethanol feeding of micropigs alters methionine metabolism and increases hepatocellular apoptosis and proliferation. Hepatology 1996;23:497-505.
99. Orrego H, Israel Y, Blake JE, Medline A. Assessment of pronostic factors in alcoholic liver disease: toward a global quantitative expression of severity. Hepatology 1983;3:896-905.
100. Kawahara H, Matsuda Y, Takase S. Is apoptosis involved in alcoholic hepatitis? Alcohol Alcohol 1994;29:113-8.
101. Kamimura S, Tsukamoto H. Cytokine gene expression by Kupffer cells in experimental alcoholic liver disease. Hepatology 1995;22:1304-9.
102. Deaciuc IV, D'Souza NB, Spitzer JJ. Tumor necrosis factor-alpha cell-surface receptors of liver parenchymal and non parenchymal cells during acute and chronic alcohol administration to rats. Alcohol Clin Exp Res 1995;19:332-5.
103. Harbrecht BG, DiSilvio M, Demetris AJ, Simmons RL, Billiar TR. Tumor necrosis factor-alpha regulate in vivo nitric oxide synthesis and induces liver injury during endotoxemia. Hepatology 1994;20:1055-8.
104. French SW. Ethanol and hepatocellular injury. Clin Lab Med 1996;16:289.
105. Seino KI, Kayagaki N, Okomura K, Yagita H. Antitumor effect of locally produced CD95 ligand. Nature Med 1997;3:165-70.
106. Zimmerman B, Mapoles J, Simon F. Mechanisms of acetaldehyde mediated growth inhibition: delayed cell cycle progression and induction of apoptosis (abstract). Hepatology 1993;18:152A.
107. Bourdon JC, D'Errico A, Paterlini P, Grigioni W, May E, Debuire B. P53 protein accumulation in European hepatocellular carcinoma is not always dependent on p53 gene mutation. Gastroenterology 1995;108:1176-82.
108. Boige V, Laurent-Puig P. Altérations génétiques associées au carcinome hépatocellulaire. Gastroenterol Clin Biol 1997;21:33-44.
109. Harris CC. Tumor suppressor genes: at the cross-roads of molecular carcinogenesis, molecular epidemiology, and human risk assessment. Prev Med 1996;25:10-2.
110. Laurent-Puig P, Flejou JF, Fabre M, Bedossa P, Belghiti J, Gayral F, et al. Overexpression of p53: a rare event in a large series of white patients with hepatocellular carcinoma. Hepatology 1992;16:1171-5.
111. Challen C, Lunec J, Warren W, Collier J, Bassendine MF. Analysis of the p53 tumor suppressor gene in hepatocellular carcinomas from Britain. Hepatology 1992;16:1362-6.
112. Kress S, Jahn UR, Buchman A, Bannasch P, Schwarz M. P53 mutations in human hepatocellular carcinomas in Germany. Cancer Res 1992;52:3220-3.
113. Kubicka S, Trautwein C, Schrem H, Tillman H, Manns M. Low incidence of p53 mutations in European hepatocellular carcinomas with heterogeneous mutation as a rare event. J Hepatol 1995;23:412-9.
114. Goldblum JR, Bartos RE, Carr KA, Frank TS. Hepatitis B and alterations of the p53 tumor suppressor gene in hepatocellular carcinoma. Am J Surg Pathol 1993;17:1244-51.
115. Wang XW, Gibson MK, Vermeulen W, Yeh H, Forrester K, Sturzbecher HW, et al. Abrogation of p53-induced apoptosis by the hepatitis B virus X gene. Cancer Res 1995;55:6012-6.
116. Kim CM, Koike K, Saito I, Miyamura T, Jay G. HBX gene of hepatitis B virus induces liver cancer in transgenic mice. Nature 1991;351:317-20.
117. Hoppe-Seyler F, Butz K. Molecular mechanisms of virus-induced carcinogenesis: the interaction of viral factors with cellular tumor suppressor proteins. J Mol Med 1995;73:529-38.
118. Columbano A, Ledda-Columbano GM, Rao PM, Rajalakshmi S, Sarma DSR. Ocurrence of cell death (apoptosis) in preneoplastic and neoplastic liver. Am J Pathol 1984;116:441-6.
119. Allemand I, Grimber G, Kornprobst M, Bennoun M, Molina T, Briand P, et al. Compensatory apoptosis in response to SV40 large T antigen expression in the liver. Oncogene 1995;11:2583-90.
120. Grasl-Kraupp B, Ruttkay-Nedecky B, Müllauer L, Taper H, Huber W, Bursch W, et al. Inherent increase of apoptosis in liver tumors: implications for carcinogenesis and tumor regression. Hepatology 1997;25:906-12.
121. Holmgren L, O'Reilly MS, Folkman J. Dormancy of micrometastases: balanced proliferation and apoptosis in the presence of angiogenesis suppression. Nature Med 1995;1:149-53.
122. Gaffey MJ, Joyce JP, Carlson GS, Esteban JM. Spontaneous regression of hepatocellular carcinoma. Cancer 1990;65:2779-83.
123. Hino N, Higashi T, Nouso K, Nakatsukasa H, Tsuji T. Apoptosis and proliferation of human hepatocellular carcinoma. Liver 1996;16:123-9.
124. Higaki K, Yano H, Kojiro M. Fas antigen expression and its relationship with apoptosis in human hepatocellular carcinoma and non cancerous tissues. Am J Pathol 1996;149:429-37.
125. Soini Y, Virkajarvi N, Lehto VP, Paakko P. Hepatocellular carcinomas with a high proliferation index and a low degree of apoptosis and necrosis are associated with a shortened survival. Br J Cancer 1996;73:1025-30.
126. Yano H, Fukuda K, Haramaki M, Momosaki S, Ogasawara S, Higaki K, et al. Expression of Fas and anti-Fas-mediated apoptosis in human hepatocellular carcinoma cell lines. J Hepatol 1996;25:454-64.
127. Strand S, Hofmann W, Hug H, Müller M, Otto G, Strand D, et al. Lymphocyte apoptosis induced by CD95 (APO-1/Fas) ligand-expressing tumor cells. A mechanism of immune evasion? Nature Med 1996;2:1361-6.
128. Xu GW, Sun ZT, Forrester K, Wang XW, Coursen J, Harris CC. Tissue-specific growth suppression and chemosensitivity in human hepatocellular carcinoma cells by retroviral-mediated transfer of the wild-type p53 gene. Hepatology 1996;24:1264-8.