Molecular mechanisms of hepatic apoptosis

Cell Death and Disease

Volumn 5, Issue 1, 2014, Pages

  Wang, K ^a  

^a UNIVERSITY OF ILLINOIS   (United States)

Author keywords

ER stress; Hepatic apoptosis; Liver injury; Lysosomal permeabilization; Mitochondrial dysfunction; ROS

Indexed keywords

BILE ACID; IMMUNOLOGIC FACTOR;

APOPTOSIS; ARTICLE; DISEASE COURSE; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENDOPLASMIC RETICULUM STRESS; HEPATIC APOPTOSIS; LIVER INJURY; MOLECULAR MECHANICS; MOLECULAR MIMICRY; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ANIMALS; APOPTOSIS; ENDOPLASMIC RETICULUM STRESS; HUMANS; LIVER; MITOCHONDRIA; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION;

EID: 84891789980     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2013.499     Document Type: Article

References (138)

1. Smith PG, Tee LB, Yeoh GC. Appearance of oval cells in the liver of rats after long-term exposure to ethanol. Hepatology 1996; 23: 145-154.
2. Sun C, Jin XL, Xiao JC. Oval cells in hepatitis B virus-positive and hepatitis C virus-positive liver cirrhosis: histological and ultrastructural study. Histopathology 2006; 48: 546-555.
3. Soden JS, Devereaux MW, Haas JE, Gumpricht E, Dahl R, Gralla J et al. Subcutaneous vitamin E ameliorates liver injury in an in vivo model of steatocholestasis. Hepatology 2007; 46: 485-495.
4. Dahl TB, Haukeland JW, Yndestad A, Ranheim T, Gladhaug IP, Damas JK et al. Intracellular nicotinamide phosphoribosyltransferase protects against hepatocyte apoptosis and is down-regulated in nonalcoholic fatty liver disease. J Clin Endocrinol Metab 2010; 95: 3039-3047.
5. Waldhauser KM, Torok M, Ha HR, Thomet U, Konrad D, Brecht K et al. Hepatocellular toxicity and pharmacological effect of amiodarone and amiodarone derivatives. J Pharmacol Exp Ther 2006; 319: 1413-1423.
6. Kopycinska J, Kempinska-Podhorodecka A, Haas T, Elias E, DePinho RA, Paik J et al. Activation of FoxO3a/Bim axis in patients with Primary Biliary Cirrhosis. Liver Int 2013; 33: 231-238.
7. Voruganti VS, Cole SA, Ebbesson SO, Goring HH, Haack K, Laston S et al. Genetic variation in APOJ, LPL, and TNFRSF10B affects plasma fatty acid distribution in Alaskan Eskimos. Am J Clin Nutr 2010; 91: 1574-1583.
8. Neuman MG, Cameron RG, Haber JA, Katz GG, Malkiewicz IM, Shear NH. Inducers of cytochrome P450 2E1 enhance methotrexate-induced hepatocytoxicity. Clin Biochem 1999; 32: 519-536.
9. Haake AR, Roublevskaia I, Cooklis M. Apoptosis: a role in skin aging? J Invest Dermatol Symp Proc 1998; 3: 28-35.
10. Haanen C, Vermes I. Apoptosis: programmed cell death in fetal development. Eur J Obstet Gynecol Reprod Biol 1996; 64: 129-133.
11. Kim KW, Ha KY, Lee JS, Rhyu KW, An HS, Woo YK. The apoptotic effects of oxidative stress and antiapoptotic effects of caspase inhibitors on rat notochordal cells. Spine (Phila Pa 1976) 2007; 32: 2443-2448.
12. Haanen C, Vermes I. Apoptosis and inflammation. Mediators Inflamm 1995; 4: 5-15.
13. Cho GW, Shin SM, Kim HK, Ha SA, Kim S, Yoon JH et al. HCCR-1, a novel oncogene, encodes a mitochondrial outer membrane protein and suppresses the UVC-induced apoptosis. BMC Cell Biol 2007; 8: 50.
14. Sadagopal S, Lorey SL, Barnett L, Sutherland D, Basham R, Erdem H et al. Enhanced PD-1 expression by T cells in cerebrospinal fluid does not reflect functional exhaustion during chronic human immunodeficiency virus type 1 infection. J Virol 2010; 84: 131-140.
15. Gallegos-Orozco JF, Rakela-Brodner J. Hepatitis viruses: not always what it seems to be. Rev Med Chil 2010; 138: 1302-1311.
16. Svirtlih N, Delic D, Simonovic J, Dokic L, Gvozdenovic E, Dulovic O et al. Characteristics of patients dying from acute viral hepatitis in Serbia. Turk J Gastroenterol 2011; 22: 152-157.
17. Lin AW, Gonzalez SA, Cunningham-Rundles S, Dorante G, Marshall S, Tignor A et al. CD56(+dim) and CD56(+bright) cell activation and apoptosis in hepatitis C virus infection. Clin Exp Immunol 2004; 137: 408-416.
18. Raziorrouh B, Schraut W, Gerlach T, Nowack D, Gruner NH, Ulsenheimer A et al. The immunoregulatory role of CD244 in chronic hepatitis B infection and its inhibitory potential on virus-specific CD8+ T-cell function. Hepatology 2010; 52: 1934-1947.
19. Kohaar I, Ploss A, Korol E, Mu K, Schoggins JW, O'Brien TR et al. Splicing diversity of the human OCLN gene and its biological significance for hepatitis C virus entry. J Virol 2010; 84: 6987-6994.
20. Bekker V, Chanock SJ, Yeager M, Hutchinson AA, von Hahn T, Chen S et al. Genetic variation in CLDN1 and susceptibility to hepatitis C virus infection. J Viral Hepat 2010; 17: 192-200.
21. Flint M, Quinn ER, Levy S. In search of hepatitis C virus receptor(s). Clin Liver Dis 2001; 5: 873-893.
22. Germi R, Crance JM, Garin D, Guimet J, Lortat-Jacob H, Ruigrok RW et al. Cellular glycosaminoglycans and low density lipoprotein receptor are involved in hepatitis C virus adsorption. J Med Virol 2002; 68: 206-215.
23. Schvoerer E, Moenne-Loccoz R, Murray JM, Velay A, Turek M, Fofana I et al. Hepatitis C virus envelope glycoprotein signatures are associated with treatment failure and modulation of viral entry and neutralization. J Infect Dis 2013; 207: 1306-1315.
24. Ploss A, Evans MJ, Gaysinskaya VA, Panis M, You H, de Jong YP et al. Human occludin is a hepatitis C virus entry factor required for infection of mouse cells. Nature 2009; 457: 882-886.
25. Wong-Staal F, Syder AJ, McKelvy JF. Targeting HCV entry for development of therapeutics. Viruses 2010; 2: 1718-1733.
26. Reynolds GM, Harris HJ, Jennings A, Hu K, Grove J, Lalor PF et al. Hepatitis C virus receptor expression in normal and diseased liver tissue. Hepatology 2008; 47: 418-427.
27. Barrett S, Collins M, Kenny C, Ryan E, Keane CO, Crowe J. Polymorphisms in tumour necrosis factor-alpha, transforming growth factor-beta, interleukin-10, interleukin-6, interferon-gamma, and outcome of hepatitis C virus infection. J Med Virol 2003; 71: 212-218.
28. Abbas Z, Moatter T, Hussainy A, Jafri W. Effect of cytokine gene polymorphism on histological activity index, viral load and response to treatment in patients with chronic hepatitis C genotype 3. World J Gastroenterol 2005; 11: 6656-6661.
29. Ben-Ari Z, Pappo O, Druzd T, Sulkes J, Klein T, Samra Z et al. Role of cytokine gene polymorphism and hepatic transforming growth factor beta1 expression in recurrent hepatitis C after liver transplantation. Cytokine 2004; 27: 7-14.
30. Apolinario A, Majano PL, Alvarez-Perez E, Saez A, Lozano C, Vargas J et al. Increased expression of T cell chemokines and their receptors in chronic hepatitis C: relationship with the histological activity of liver disease. Am J Gastroenterol 2002; 97: 2861-2870.
31. Moreno C, Gustot T, Nicaise C, Quertinmont E, Nagy N, Parmentier M et al. CCR5 deficiency exacerbates T-cell-mediated hepatitis in mice. Hepatology 2005; 42: 854-862.
32. Hayashi N, Higashi H, Kaminaka K, Sugimoto H, Esumi M, Komatsu K et al. Molecular cloning and heterogeneity of the human hepatitis C virus (HCV) genome. J Hepatol 1993; 17(Suppl 3): S94-S107.
33. Kato N. Genome of human hepatitis C virus (HCV): gene organization, sequence diversity, and variation. Microb Comp Genomics 2000; 5: 129-151.
34. Nam JH, Bukh J, Purcell RH, Emerson SU. High-level expression of hepatitis C virus (HCV) structural proteins by a chimeric HCV/BVDV genome propagated as a BVDV pseudotype. J Virol Methods 2001; 97: 113-123.
35. Zhu N, Ware CF, Lai MM. Hepatitis C virus core protein enhances FADD-mediated apoptosis and suppresses TRADD signaling of tumor necrosis factor receptor. Virology 2001; 283: 178-187.
36. Rubbia-Brandt L, Taylor S, Gindre P, Quadri R, Abid K, Spahr L et al. Lack of in vivo blockade of Fas-and TNFR1-mediated hepatocyte apoptosis by the hepatitis C virus. J Pathol 2002; 197: 617-623.
37. Prikhod'ko EA, Prikhod'ko GG, Siegel RM, Thompson P, Major ME, Cohen JI. The NS3 protein of hepatitis C virus induces caspase-8-mediated apoptosis independent of its protease or helicase activities. Virology 2004; 329: 53-67.
38. Iken K, Huang L, Bekele H, Schmidt EV, Koziel MJ. Apoptosis of activated CD4+ and CD8+ T cells is enhanced by co-culture with hepatocytes expressing hepatitis C virus (HCV) structural proteins through FasL induction. Virology 2006; 346: 363-372.
39. Pianko S, Patella S, Ostapowicz G, Desmond P, Sievert W. Fas-mediated hepatocyte apoptosis is increased by hepatitis C virus infection and alcohol consumption, and may be associated with hepatic fibrosis: mechanisms of liver cell injury in chronic hepatitis C virus infection. J Viral Hepat 2001; 8: 406-413.
40. Valva P, De Matteo E, Galoppo MC, Gismondi MI, Preciado MV. Apoptosis markers related to pathogenesis of pediatric chronic hepatitis C virus infection: M30 mirrors the severity of steatosis. J Med Virol 2010; 82: 949-957.
41. Lam W, Li Y, Liou JY, Dutschman GE, Cheng YC. Reverse transcriptase activity of hepatitis B virus (HBV) DNA polymerase within core capsid: interaction with deoxynucleoside triphosphates and anti-HBV L-deoxynucleoside analog triphosphates. Mol Pharmacol 2004; 65: 400-406.
42. Chen YL, Yu CK, Lei HY. Propionibacterium acnes induces acute TNFalpha-mediated apoptosis of hepatocytes followed by inflammatory T-cell-mediated granulomatous hepatitis in mice. J Biomed Sci 1999; 6: 349-356.
43. Feitelson MA, Reis HM, Tufan NL, Sun B, Pan J, Lian Z. Putative roles of hepatitis B x antigen in the pathogenesis of chronic liver disease. Cancer Lett 2009; 286: 69-79.
44. Peppa D, Gill US, Reynolds G, Easom NJ, Pallett LJ, Schurich A et al. Up-regulation of a death receptor renders antiviral T cells susceptible to NK cell-mediated deletion. J Exp Med 2013; 210: 99-114.
45. Liang X, Liu Y, Zhang Q, Gao L, Han L, Ma C et al. Hepatitis B virus sensitizes hepatocytes to TRAIL-induced apoptosis through Bax. J Immunol 2007; 178: 503-510.
46. Du J, Liang X, Liu Y, Qu Z, Gao L, Han L et al. Hepatitis B virus core protein inhibits TRAIL-induced apoptosis of hepatocytes by blocking DR5 expression. Cell Death Differ 2009; 16: 219-229.
47. Arzumanyan A, Reis HM, Feitelson MA. Pathogenic mechanisms in HBV-and HCV-associated hepatocellular carcinoma. Nat Rev Cancer 2012; 13: 123-135.
48. Woo GA, O'Brien C. Long-term management of alcoholic liver disease. Clin Liver Dis 2012; 16: 763-781.
49. Conde de la Rosa L, Moshage H, Nieto N. [Hepatocyte oxidant stress and alcoholic liver disease]. Rev Esp Enferm Dig 2008; 100: 156-163.
50. Cho EY, Yun CH, Chae HZ, Chae HJ, Ahn T. Anionic phospholipid-induced regulation of reactive oxygen species production by human cytochrome P450 2E1. FEBS Lett 2008; 582: 1771-1776.
51. Gut I, Nedelcheva V, Soucek P, Stopka P, Tichavska B. Cytochromes P450 in benzene metabolism and involvement of their metabolites and reactive oxygen species in toxicity. Environ Health perspect 1996; 104(Suppl 6): 1211-1218.
52. Cederbaum AI. Microsomal generation of reactive oxygen species and their possible role in alcohol hepatotoxicity. Alcohol Alcohol Suppl 1991; 1: 291-296.
53. Longato L, Ripp K, Setshedi M, Dostalek M, Akhlaghi F, Branda M et al. Insulin resistance, ceramide accumulation, and endoplasmic reticulum stress in human chronic alcohol-related liver disease. Oxid Med Cell Longev 2012; 2012: 479348.
54. Chen P, Tu X, Akdemir F, Chew SK, Rothenfluh A, Abrams JM. Effectors of alcohol-induced cell killing in Drosophila. Cell Death Differ 2012; 19: 1655-1663.
55. Casey CA, Lee SM, Aziz-Seible R, McVicker BL. Impaired receptor-mediated endocytosis: its role in alcohol-induced apoptosis. J Gastroenterol Hepatol 2008; 23(Suppl 1): S46-S49.
56. Dai LL, Gong JP, Zuo GQ, Wu CX, Shi YJ, Li XH et al. Synthesis of endotoxin receptor CD14 protein in Kupffer cells and its role in alcohol-induced liver disease. World J Gastroenterol 2003; 9: 622-626.
57. Purohit V, Brenner DA. Mechanisms of alcohol-induced hepatic fibrosis: a summary of the Ron Thurman Symposium. Hepatology 2006; 43: 872-878.
58. Mu YP, Ogawa T, Kawada N. Reversibility of fibrosis, inflammation, and endoplasmic reticulum stress in the liver of rats fed a methionine-choline- deficient diet. Lab Invest 2010; 90: 245-256.
59. Davit-Spraul A, Gonzales E, Baussan C, Jacquemin E. Progressive familial intrahepatic cholestasis. Orphanet J Rare Dis 2009; 4: 1.
60. Rodriguez-Garay EA. Cholestasis: human disease and experimental animal models. Ann Hepatol 2003; 2: 150-158.
61. Miyoshi H, Rust C, Roberts PJ, Burgart LJ, Gores GJ. Hepatocyte apoptosis after bile duct ligation in the mouse involves Fas. Gastroenterology 1999; 117: 669-677.
62. Schattenberg JM, Zimmermann T, Worns M, Sprinzl MF, Kreft A, Kohl T et al. Ablation of c-FLIP in hepatocytes enhances death-receptor mediated apoptosis and toxic liver injury in vivo. J Hepatol 2011; 55: 1272-1280.
63. Tiao MM, Lin TK, Liou CW, Wang PW, Chen JB, Kuo FY et al. Early transcriptional deregulation of hepatic mitochondrial biogenesis and its consequent effects on murine cholestatic liver injury. Apoptosis 2009; 14: 890-899.
64. Faubion WA, Guicciardi ME, Miyoshi H, Bronk SF, Roberts PJ, Svingen PA et al. Toxic bile salts induce rodent hepatocyte apoptosis via direct activation of Fas. J Clin Invest 1999; 103: 137-145.
65. Scott FL, Stec B, Pop C, Dobaczewska MK, Lee JJ, Monosov E et al. The Fas-FADD death domain complex structure unravels signalling by receptor clustering. Nature 2009; 457: 1019-1022.
66. Hatano E. Tumor necrosis factor signaling in hepatocyte apoptosis. J Gastroenterol Hepatol 2007; 22(Suppl 1): S43-S44.
67. Sodeman T, Bronk SF, Roberts PJ, Miyoshi H, Gores GJ. Bile salts mediate hepatocyte apoptosis by increasing cell surface trafficking of Fas. Am J Physiol Gastrointest Liver Physiol 2000; 278: G992-G999.
68. Gabele E, Froh M, Arteel GE, Uesugi T, Hellerbrand C, Scholmerich J et al. TNFalpha is required for cholestasis-induced liver fibrosis in the mouse. Biochem Biophys Res Commun 2009; 378: 348-353.
69. Higuchi H, Bronk SF, Takikawa Y, Werneburg N, Takimoto R, El-Deiry W et al. The bile acid glycochenodeoxycholate induces trail-receptor 2/DR5 expression and apoptosis. J Biol Chem 2001; 276: 38610-38618.
70. Takeda K, Kojima Y, Ikejima K, Harada K, Yamashina S, Okumura K et al. Death receptor 5 mediated-apoptosis contributes to cholestatic liver disease. Proc Natl Acad Sci USA 2008; 105: 10895-10900.
71. Aktas C, Kanter M, Erboga M, Mete R, Oran M. Melatonin attenuates oxidative stress, liver damage and hepatocyte apoptosis after bile-duct ligation in rats. Toxicol Ind Health 2012; e-pub ahead of print 24 October 2013; doi:10.1177/0748233712464811.
72. Welge-Lussen U, May CA, Lutjen-Drecoll E. Induction of tissue transglutaminase in the trabecular meshwork by TGF-beta1 and TGF-beta2. Invest Ophthalmol Vis Sci 2000; 41: 2229-2238.
73. Ghatak S, Biswas A, Dhali GK, Chowdhury A, Boyer JL, Santra A. Oxidative stress and hepatic stellate cell activation are key events in arsenic induced liver fibrosis in mice. Toxicol Appl Pharmacol 2011; 251: 59-69.
74. Rodrigues CM, Fan G, Wong PY, Kren BT, Steer CJ. Ursodeoxycholic acid may inhibit deoxycholic acid-induced apoptosis by modulating mitochondrial transmembrane potential and reactive oxygen species production. Mol Med 1998; 4: 165-178.
75. Roma MG, Toledo FD, Boaglio AC, Basiglio CL, Crocenzi FA, Sanchez Pozzi EJ. Ursodeoxycholic acid in cholestasis: linking action mechanisms to therapeutic applications. Clin Sci (Lond) 2011; 121: 523-544.
76. Wang K, Holterman AX. Pathophysiologic role of hepatocyte nuclear factor 6. Cell Signal 2012; 24: 9-16.
77. Serfaty L, Lemoine M. Definition and natural history of metabolic steatosis: clinical aspects of NAFLD, NASH and cirrhosis. Diab Metab 2008; 34(6 Pt 2): 634-637.
78. Brunt EM, Kleiner DE, Wilson LA, Unalp A, Behling CE, Lavine JE et al. Portal chronic inflammation in nonalcoholic fatty liver disease (NAFLD): a histologic marker of advanced NAFLD-Clinicopathologic correlations from the nonalcoholic steatohepatitis clinical research network. Hepatology 2009; 49: 809-820.
79. Bhala N, Jouness RI, Bugianesi E. Epidemiology and natural history of patients with NAFLD. Curr Pharm Des 2013; 19: 5169-5176.
80. Hirosumi J, Tuncman G, Chang L, Gorgun CZ, Uysal KT, Maeda K et al. A central role for JNK in obesity and insulin resistance. Nature 2002; 420: 333-336.
81. Vallerie SN, Furuhashi M, Fucho R, Hotamisligil GS. A predominant role for parenchymal c-Jun amino terminal kinase (JNK) in the regulation of systemic insulin sensitivity. PLoS One 2008; 3: e3151.
82. Coulon S, Francque S, Colle I, Verrijken A, Blomme B, Heindryckx F et al. Evaluation of inflammatory and angiogenic factors in patients with non-alcoholic fatty liver disease. Cytokine 2012; 59: 442-449.
83. Yu HY, Wang BL, Zhao J, Yao XM, Gu Y, Li Y. Protective effect of bicyclol on tetracyclineinduced fatty liver in mice. Toxicology 2009; 261: 112-118.
84. Park JW, Jeong G, Kim SJ, Kim MK, Park SM. Predictors reflecting the pathological severity of non-alcoholic fatty liver disease: comprehensive study of clinical and immunohistochemical findings in younger Asian patients. J Gastroenterol Hepatol 2007; 22: 491-497.
85. Wree A, Kahraman A, Gerken G, Canbay A. Obesity affects the liver-the link between adipocytes and hepatocytes. Digestion 2011; 83: 124-133.
86. Bechmann LP, Kocabayoglu P, Sowa JP, Sydor S, Best J, Schlattjan M et al. Free fatty acids repress SHP activation and adiponectin counteracts bile acid induced liver injury in super-obese patients with NASH. Hepatology 2013; 57: 1394-1406.
87. Malhi H, Barreyro FJ, Isomoto H, Bronk SF, Gores GJ. Free fatty acids sensitise hepatocytes to TRAIL mediated cytotoxicity. Gut 2007; 56: 1124-1131.
88. Malhi H, Bronk SF, Werneburg NW, Gores GJ. Free fatty acids induce JNK-dependent hepatocyte lipoapoptosis. J Biol Chem 2006; 281: 12093-12101.
89. Moschen AR, Wieser V, Tilg H. Adiponectin: key player in the adipose tissue-liver crosstalk. Curr Med Chem 2012; 19: 5467-5473.
90. Zheng H, Li S, Ma L, Cheng L, Deng C, Chen Z et al. A novel agonist of PPAR-gamma based on barbituric acid alleviates the development of non-alcoholic fatty liver disease by regulating adipocytokine expression and preventing insulin resistance. Eur J Pharmacol 2011; 659: 244-251.
91. Benhamed F, Denechaud PD, Lemoine M, Robichon C, Moldes M, Bertrand-Michel J et al. The lipogenic transcription factor ChREBP dissociates hepatic steatosis from insulin resistance in mice and humans. J Clin Invest 2012; 122: 2176-2194.
92. Kohjima M, Higuchi N, Kato M, Kotoh K, Yoshimoto T, Fujino T et al. SREBP-1c, regulated by the insulin and AMPK signaling pathways, plays a role in nonalcoholic fatty liver disease. Int J Mol Med 2008; 21: 507-511.
93. Guzman C, Benet M, Pisonero-Vaquero S, Moya M, Garcia-Mediavilla MV, Martinez-Chantar ML et al. The human liver fatty acid binding protein (FABP1) gene is activated by FOXA1 and PPARalpha; and repressed by C/EBPalpha: Implications in FABP1 down-regulation in nonalcoholic fatty liver disease. Biochim Biophys Acta 2013; 1831: 803-818.
94. Rottiers V, Naar AM. MicroRNAs in metabolism and metabolic disorders. Nat Rev Mol Cell Biol 2012; 13: 239-250.
95. Sharma H, Estep M, Birerdinc A, Afendy A, Moazzez A, Elariny H et al. Expression of genes for microRNA-processing enzymes is altered in advanced non-alcoholic fatty liver disease. J Gastroenterol Hepatol 2013; 28: 1410-1415.
96. Cermelli S, Ruggieri A, Marrero JA, Ioannou GN, Beretta L. Circulating microRNAs in patients with chronic hepatitis C and non-alcoholic fatty liver disease. PLoS One 2011; 6: e23937.
97. Castro RE, Ferreira DM, Afonso MB, Borralho PM, Machado MV, Cortez-Pinto H et al. miR-34a/SIRT1/p53 is suppressed by ursodeoxycholic acid in the rat liver and activated by disease severity in human non-alcoholic fatty liver disease. J Hepatol 2013; 58: 119-125.
98. Cazanave SC, Mott JL, Elmi NA, Bronk SF, Masuoka HC, Charlton MR et al. A role for miR-296 in the regulation of lipoapoptosis by targeting PUMA. J Lipid Res 2011; 52: 1517-1525.
99. Bjornsson ES, Bergmann OM, Bjornsson HK, Kvaran RB, Olafsson S. Incidence, presentation and outcomes in patients with drug-induced liver injury in the general population of Iceland. Gastroenterology 2013; 144: 1419-1425.
100. Lucena MI, Garcia-Martin E, Andrade RJ, Martinez C, Stephens C, Ruiz JD et al. Mitochondrial superoxide dismutase and glutathione peroxidase in idiosyncratic drug-induced liver injury. Hepatology 2010; 52: 303-312.
101. von Felden J, Montani M, Kessebohm K, Stickel F. Drug-induced acute liver injury mimicking autoimmune hepatitis after intake of dietary supplements containing glucosamine and chondroitin sulfate. Int J Clin Pharmacol Ther 2013; 51: 219-223.
102. Tanaka Y, Takahashi A, Watanabe K, Takayama K, Yahata T, Habu S et al. A pivotal role of IL-12 in Th1-dependent mouse liver injury. Int Immunol 1996; 8: 569-576.
103. Nanji AA, Jokelainen K, Rahemtulla A, Miao L, Fogt F, Matsumoto H et al. Activation of nuclear factor kappa B and cytokine imbalance in experimental alcoholic liver disease in the rat. Hepatology 1999; 30: 934-943.
104. Rowell DL, Eckmann L, Dwinell MB, Carpenter SP, Raucy JL, Yang SK et al. Human hepatocytes express an array of proinflammatory cytokines after agonist stimulation or bacterial invasion. Am J Physiol 1997; 273(2 Pt 1): G322-G332.
105. Li M, Liu GT. Inhibition of Fas/FasL mRNA expression and TNF-alpha release in concanavalin A-induced liver injury in mice by bicyclol. World J Gastroenterol 2004; 10: 1775-1779.
106. Huang J, Shi W, Zhang J, Chou JW, Paules RS, Gerrish K et al. Genomic indicators in the blood predict drug-induced liver injury. Pharmacogenomics J 2010; 10: 267-277.
107. Cavassani KA, Moreira AP, Habiel D, Ito T, Coelho AL, Allen RM et al. Toll like receptor 3 plays a critical role in the progression and severity of acetaminophen-induced hepatotoxicity. PLoS One 2013; 8: e65899.
108. Badmann A, Keough A, Kaufmann T, Bouillet P, Brunner T, Corazza N. Role of TRAIL and the pro-apoptotic Bcl-2 homolog Bim in acetaminophen-induced liver damage. Cell Death Dis 2011; 2: e171.
109. Badmann A, Langsch S, Keogh A, Brunner T, Kaufmann T, Corazza N. TRAIL enhances paracetamol-induced liver sinusoidal endothelial cell death in a Bim-and Bid-dependent manner. Cell Death Dis 2012; 3: e447.
110. Lee WM, Senior JR. Recognizing drug-induced liver injury: current problems, possible solutions. Toxicol Pathol 2005; 33: 155-164.
111. Roth GA, Krenn C, Brunner M, Moser B, Ploder M, Spittler A et al. Elevated serum levels of epithelial cell apoptosis-specific cytokeratin 18 neoepitope m30 in critically ill patients. Shock 2004; 22: 218-220.
112. Han D, Shinohara M, Ybanez MD, Saberi B, Kaplowitz N. Signal transduction pathways involved in drug-induced liver injury. Handb Exp Pharmacol 2010; 196: 267-310.
113. Ghavami S, Hashemi M, Kadkhoda K, Alavian SM, Bay GH, Los M. Apoptosis in liver diseases-detection and therapeutic applications. Med Sci Monit 2005; 11: RA337-RA345.
114. Santodomingo-Garzon T, Swain MG. Role of NKT cells in autoimmune liver disease. Autoimmun Rev 2011; 10: 793-800.
115. Selmi C, Mackay IR, Gershwin ME. The autoimmunity of primary biliary cirrhosis and the clonal selection theory. Immunol Cell Biol 2011; 89: 70-80.
116. Mao TK, Davis PA, Odin JA, Coppel RL, Gershwin ME. Sidechain biology and the immunogenicity of PDC-E2, the major autoantigen of primary biliary cirrhosis. Hepatology 2004; 40: 1241-1248.
117. Allina J, Hu B, Sullivan DM, Fiel MI, Thung SN, Bronk SF et al. T cell targeting and phagocytosis of apoptotic biliary epithelial cells in primary biliary cirrhosis. J Autoimmun 2006; 27: 232-241.
118. Floreani A, Zancan L, Melis A, Baragiotta A, Chiaramonte M. Primary sclerosing cholangitis (PSC): clinical, laboratory and survival analysis in children and adults. Liver 1999; 19: 228-233.
119. Rudolph G, Gotthardt D, Kloeters-Plachky P, Rost D, Kulaksiz H, Stiehl A. In PSC with dominant bile duct stenosis, IBD is associated with an increase of carcinomas and reduced survival. J Hepatol 2010; 53: 313-317.
120. Bernstein CN. Osteoporosis and other complications of inflammatory bowel disease. Curr Opin Gastroenterol 2002; 18: 428-434.
121. Broome U, Glaumann H, Lindstom E, Loof L, Almer S, Prytz H et al. Natural history and outcome in 32 Swedish patients with small duct primary sclerosing cholangitis (PSC). J Hepatol 2002; 36: 586-589.
122. Kremer AE, Rust C, Eichhorn P, Beuers U, Holdenrieder S. Immune-mediated liver diseases: programmed cell death ligands and circulating apoptotic markers. Exp Rev Mol Diagn 2009; 9: 139-156.
123. Gantner F, Leist M, Lohse AW, Germann PG, Tiegs G. Concanavalin A-induced T-cell-mediated hepatic injury in mice: the role of tumor necrosis factor. Hepatology 1995; 21: 190-198.
124. Volarevic V, Milovanovic M, Ljujic B, Pejnovic N, Arsenijevic N, Nilsson U et al. Galectin-3 deficiency prevents concanavalin A-induced hepatitis in mice. Hepatology 2012; 55: 1954-1964.
125. Kim KM, Kim YM, Park M, Park K, Chang HK, Park TK et al. A broad-spectrum caspase inhibitor blocks concanavalin A-induced hepatitis in mice. Clin Immunol 2000; 97: 221-233.
126. Ding JW, Wang K, Brems JJ, Gamelli RL. Protection against concanavalin A-induced hepatocyte apoptosis by molsidomine is time-dependent. J Am Coll Surg 2004; 198: 67-77.
127. Zhang H, Gong Q, Li JH, Kong XL, Tian L, Duan LH et al. CpG ODN pretreatment attenuates concanavalin A-induced hepatitis in mice. Int Immunopharmacol 2010; 10: 79-85.
128. Jouan-Lanhouet S, Arshad MI, Piquet-Pellorce C, Martin-Chouly C, Le Moigne-Muller G, Van Herreweghe F et al. TRAIL induces necroptosis involving RIPK1/RIPK3-dependent PARP-1 activation. Cell Death Differ 2012; 19: 2003-2014.
129. Wen YA, Liu D, Zhou QY, Huang SF, Luo P, Xiang Y et al. Biliary intervention aggravates cholestatic liver injury, and induces hepatic inflammation, proliferation and fibrogenesis in BDL mice. Exp Toxicol Pathol 2011; 63: 277-284.
130. Kaiser WJ, Upton JW, Long AB, Livingston-Rosanoff D, Daley-Bauer LP, Hakem R et al. RIP3 mediates the embryonic lethality of caspase-8-deficient mice. Nature 2011; 471: 368-372.
131. Liedtke C, Bangen JM, Freimuth J, Beraza N, Lambertz D, Cubero FJ et al. Loss of caspase-8 protects mice against inflammation-related hepatocarcinogenesis but induces non-apoptotic liver injury. Gastroenterology 2011; 141: 2176-2187.
132. Hikita H, Takehara T, Shimizu S, Kodama T, Li W, Miyagi T et al. Mcl-1 and Bcl-xL cooperatively maintain integrity of hepatocytes in developing and adult murine liver. Hepatology 2009; 50: 1217-1226.
133. Vick B, Weber A, Urbanik T, Maass T, Teufel A, Krammer PH et al. Knockout of myeloid cell leukemia-1 induces liver damage and increases apoptosis susceptibility of murine hepatocytes. Hepatology 2009; 49: 627-636.
134. Ratziu V, Sheikh MY, Sanyal AJ, Lim JK, Conjeevaram H, Chalasani N et al. A phase 2, randomized, double-blind, placebo-controlled study of GS-9450 in subjects with nonalcoholic steatohepatitis. Hepatology 2012; 55: 419-428.
135. Shiffman ML, Pockros P, McHutchison JG, Schiff ER, Morris M, Burgess G. Clinical trial: the efficacy and safety of oral PF-03491390, a pancaspase inhibitor-a randomized placebo-controlled study in patients with chronic hepatitis C. Aliment Pharmacol Ther 2010; 31: 969-978.
136. Baskin-Bey ES, Washburn K, Feng S, Oltersdorf T, Shapiro D, Huyghe M et al. Clinical trial of the pan-caspase inhibitor, IDN-6556, in human liver preservation injury. Am J Transplant 2007; 7: 218-225.
137. Pockros PJ, Schiff ER, Shiffman ML, McHutchison JG, Gish RG, Afdhal NH et al. Oral IDN-6556, an antiapoptotic caspase inhibitor, may lower aminotransferase activity in patients with chronic hepatitis C. Hepatology 2007; 46: 324-329.
138. Meng F, Glaser SS, Francis H, Yang F, Han Y, Stokes A et al. Epigenetic regulation of miR-34a expression in alcoholic liver injury. Am J Pathol 2012; 181: 804-817.