Acute liver failure: Mechanisms of immune-mediated liver injury

Liver International

Volumn 30, Issue 6, 2010, Pages 782-794

  Wu, Zeguang ^a   Han, Meifang ^a   Chen, Tao ^a   Yan, Weiming ^a   Ning, Qin ^a  

^a HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

Acute liver failure; Animal model; Liver injury

Indexed keywords

CYTOKINE; ESTROGEN; FIBRONECTIN; THYROID HORMONE; AUTACOID;

B LYMPHOCYTE; CELLULAR IMMUNITY; COMPLEMENT ACTIVATION; CYTOKINE PRODUCTION; DENDRITIC CELL; DISEASE MODEL; EOSINOPHIL; HEMOSTASIS; HUMAN; IMMUNOMODULATION; IMMUNOPATHOGENESIS; INFLAMMATION; INNATE IMMUNITY; KUPFFER CELL; LAGOVIRUS; LIVER FAILURE; LIVER SINUSOID; MACROPHAGE; MONOCYTE; NATURAL KILLER CELL; NATURAL KILLER T CELL; NEUROENDOCRINE SYSTEM; NEUTROPHIL; NONHUMAN; PATHOPHYSIOLOGY; REVIEW; SYMPATHETIC NERVE; T LYMPHOCYTE; THROMBOCYTE ACTIVATION; TRANSGENIC MOUSE; ACUTE LIVER FAILURE; ADAPTIVE IMMUNITY; ANIMAL; IMMUNOLOGY; LIVER; METABOLISM; PATHOLOGY; PROGNOSIS;

ADAPTIVE IMMUNITY; ANIMALS; CYTOKINES; DISEASE MODELS, ANIMAL; HUMANS; IMMUNITY, INNATE; INFLAMMATION MEDIATORS; LIVER; LIVER FAILURE, ACUTE; PROGNOSIS;

EID: 77954369240     PISSN: 14783223     EISSN: 14783231     Source Type: Journal    
DOI: 10.1111/j.1478-3231.2010.02262.x     Document Type: Review

References (124)

1. Sarin S K, Kumar A, Almeida J A. Acute-on-chronic liver failure: consensus recommendations of the Asian Pacific Association for the study of the liver (APASL). Hepatol Int 2009, 3:269-82.
2. Liver Failure and Artificial Liver Group, Chinese Society of Infectious Diseases, Severe Liver Diseases and Artificial Liver Group, Chinese Society of Hepatology, and Chinese Medical Association. Diagnostic and treatment guidelines for liver failure. Zhonghua Gan Zang Bing Za Zhi 2006, 14:643-646.
3. Lee WM. Etiologies of acute liver failure. Semin Liver Dis 2008, 28:142-52.
4. Stravitz R T, Kramer DJ. Management of acute liver failure. Nat Rev Gastroenterol Hepatol 2009, 6:542-53.
5. Volkmann X, Anstaett M, Hadem J. Caspase activation is associated with spontaneous recovery from acute liver failure. Hepatology 2008, 47:1624-33.
6. Lu JW, Wang H, Yan-Li J. Differential effects of pyrrolidine dithiocarbamate on TNF-alpha-mediated liver injury in two different models of fulminant hepatitis. J Hepatol 2008, 48:442-52.
7. Lamle J, Marhenke S, Borlak J. Nuclear factor-eythroid 2-related factor 2 prevents alcohol-induced fulminant liver injury. Gastroenterology 2008, 134:1159-68.
8. Gonzalez-Rodriguez A, Alba J, Zimmerman V, Kozma SC, Valverde AM. S6K1 deficiency protects against apoptosis in hepatocytes. Hepatology 2009, 50:216-29.
9. Gershwin ME, Vierling JM, Manns MP. Liver immunology: principles and practice. 2007, Totowa, New Jersey, Humana Press Inc.
10. Malhi H, Gores GJ. Cellular and molecular mechanisms of liver injury. Gastroenterology 2008, 134:1641-54.
11. Guicciardi ME, Gores GJ. Apoptosis: a mechanism of acute and chronic liver injury. Gut 2005, 54:1024-33.
12. Bechmann LP, Marquitan G, Jochum C. Apoptosis versus necrosis rate as a predictor in acute liver failure following acetaminophen intoxication compared with acute-on-chronic liver failure. Liver Int 2008, 28:713-6.
13. Crispe IN. The liver as a lymphoid organ. Annu Rev Immunol 2009, 27:147-163.
14. Gao B, Jeong WI, Tian Z. Liver: an organ with predominant innate immunity. Hepatology 2008, 47:729-736.
15. Racanelli V, Rehermann B. The liver as an immunological organ. Hepatology 2006, 43((Suppl. 1)):S54-62.
16. Wasmuth H E, Kunz D, Yagmur E. Patients with acute on chronic liver failure display " sepsis-like" immune paralysis. J Hepatol 2005, 42:195-201.
17. Rolando N, Wade J, Davalos M. The systemic inflammatory response syndrome in acute liver failure. Hepatology 2000, 32((Part 1)):734-9.
18. Liu Q. Role of cytokines in the pathophysiology of acute-on-chronic liver failure. Blood Purif 2009, 28:331-41.
19. Li J, Zhu X, Liu F. Cytokine and autoantibody patterns in acute liver failure. J Immunotoxicol 2009
20. Yoshimura A, Naka T, Kubo M. SOCS proteins, cytokine signalling and immune regulation. Nat Rev Immunol 2007, 7:454-65.
21. Hong F, Jaruga B, Kim W H. Opposing roles of STAT1 and STAT3 in T cell-mediated hepatitis: regulation by SOCS. J Clin Invest 2002, 110:1503-13.
22. Torisu T, Nakaya M, Watanabe S. Suppressor of cytokine signaling 1 protects mice against concanavalin A-induced hepatitis by inhibiting apoptosis. Hepatology 2008, 47:1644-54.
23. Louis H, Le Moine O, Peny MO. Hepatoprotective role of interleukin 10 in galactosamine/lipopolysaccharide mouse liver injury. Gastroenterology 1997, 112:935-42.
24. Isayama F, Froh M, Yin M. TNF alpha-induced Ras activation due to ethanol promotes hepatocyte proliferation independently of liver injury in the mouse. Hepatology 2004, 39:721-31.
25. Cressman DE, Greenbaum LE, Deangelis RA. Liver failure and defective hepatocyte regeneration in interleukin-6-deficient mice. Science 1996, 274:1379-83.
26. Yan Z, Tan W, Zhao W. Regulatory polymorphisms in the IL-10 gene promoter and HBV-related acute liver failure in the Chinese population. J Viral Hepat 2009, 16:775-83.
27. Ito H, Ando K, Ishikawa T. Role of TNF-alpha produced by nonantigen-specific cells in a fulminant hepatitis mouse model. J Immunol 2009, 182:391-7.
28. Leifeld L, Cheng S, Ramakers J. Imbalanced intrahepatic expression of interleukin 12, interferon gamma, and interleukin 10 in fulminant hepatitis B. Hepatology 2002, 36((Part 1)):1001-8.
29. Zou Z, Li B, Xu D. Imbalanced intrahepatic cytokine expression of interferon-gamma, tumor necrosis factor-alpha, and interleukin-10 in patients with acute-on-chronic liver failure associated with hepatitis B virus infection. J Clin Gastroenterol 2009, 43:182-90.
30. Antoniades CG, Berry PA, Wendon JA, Vergani D. The importance of immune dysfunction in determining outcome in acute liver failure. J Hepatol 2008, 49:845-61.
31. Muschen M, Warskulat U, Schmidt B, Schulz WA, Haussinger D. Regulation of CD95 (Apo-1/Fas) ligand and receptor expression in human embryonal carcinoma cells by interferon gamma and all-trans retinoic acid. Biol Chem 1998, 379:1083-91.
32. Cardier JE, Schulte T, Kammer H, Kwak J, Cardier M. Fas (CD95, APO-1) antigen expression and function in murine liver endothelial cells: implications for the regulation of apoptosis in liver endothelial cells. FASEB J 1999, 13:1950-60.
33. Ueno Y, Ishii M, Yahagi K. Fas-mediated cholangiopathy in the murine model of graft versus host disease. Hepatology 2000, 31:966-74.
34. Malhi H, Gores GJ, Lemasters JJ. Apoptosis and necrosis in the liver: a tale of two deaths? Hepatology 2006, 43((Suppl. 1)):S31-44.
35. Mita A, Hashikura Y, Tagawa Y. Expression of fas ligand by hepatic macrophages in patients with fulminant hepatic failure. Am J Gastroenterol 2005, 100:2551-9.
36. Ryo K, Kamogawa Y, Ikeda I. Significance of Fas antigen-mediated apoptosis in human fulminant hepatic failure. Am J Gastroenterol 2000, 95:2047-55.
37. Suzuki H, Toyoda M, Horiguchi N. Hepatocyte growth factor protects against Fas-mediated liver apoptosis in transgenic mice. Liver Int 2009, 29:1562-8.
38. Hagiwara S, Otsuka T, Yamazaki Y. Overexpression of NK2 promotes liver fibrosis in carbon tetrachloride-induced chronic liver injury. Liver Int 2008, 28:126-31.
39. Yamada Y, Webber EM, Kirillova I, Peschon JJ, Fausto N. Analysis of liver regeneration in mice lacking type 1 or type 2 tumor necrosis factor receptor: requirement for type 1 but not type 2 receptor. Hepatology 1998, 28:959-70.
40. Streetz K, Leifeld L, Grundmann D. Tumor necrosis factor alpha in the pathogenesis of human and murine fulminant hepatic failure. Gastroenterology 2000, 119:446-60.
41. Yoon S, Kim TH, Natarajan A. Acute liver injury upregulates microRNA-491-5p in mice, and its overexpression sensitizes Hep G2 cells for tumour necrosis factor-alpha-induced apoptosis. Liver Int 2009, 30:376-87.
42. Nagaki M, Iwai H, Naiki T. High levels of serum interleukin-10 and tumor necrosis factor-alpha are associated with fatality in fulminant hepatitis. J Infect Dis 2000, 182:1103-8.
43. Rudiger HA, Clavien PA. Tumor necrosis factor alpha, but not Fas, mediates hepatocellular apoptosis in the murine ischemic liver. Gastroenterology 2002, 122:202-10.
44. Abel M, Sene D, Pol S. Intrahepatic virus-specific IL-10-producing CD8 T cells prevent liver damage during chronic hepatitis C virus infection. Hepatology 2006, 44:1607-16.
45. Yang Y, Zheng L, Lv G, Jin X, Sheng J. Hepatocytes treated with HBV X protein as cytotoxic effectors kill primary hepatocytes by TNF-alpha-related apoptosis-induced ligand-mediated mechanism. Intervirology 2007, 50:323-7.
46. Kim WH, HONG F, Jaruga B. Hepatitis B virus X protein sensitizes primary mouse hepatocytes to ethanol- and TNF-alpha-induced apoptosis by a caspase-3-dependent mechanism. Cell Mol Immunol 2005, 2:40-8.
47. Malhi H, Barreyro FJ, Isomoto H, Bronk SF, Gores GJ. Free fatty acids sensitise hepatocytes to TRAIL mediated cytotoxicity. Gut 2007, 56:1124-31.
48. Mundt B, Wirth T, Zender L. Tumour necrosis factor related apoptosis inducing ligand (TRAIL) induces hepatic steatosis in viral hepatitis and after alcohol intake. Gut 2005, 54:1590-6.
49. Kuhla A, Eipel C, Abshagen K. Role of the perforin/granzyme cell death pathway in D-Gal/LPS-induced inflammatory liver injury. Am J Physiol Gastrointest Liver Physiol 2009, 296:G1069-76.
50. Groscurth P, Filgueira L. Killing mechanisms of Cytotoxic T lymphocytes. News Physiol Sci 1998, 13:17-21.
51. Qin X, Gao B. The complement system in liver diseases. Cell Mol Immunol 2006, 3:333-40.
52. Pritchard MT, Mcmullen MR, Medof ME, Stavitsky A, Nagy LE. Role of complement in ethanol-induced liver injury. Adv Exp Med Biol 2008, 632:175-86.
53. Arumugam TV, Shiels IA, Woodruff TM, Granger DN, Taylor SM. The role of the complement system in ischemia-reperfusion injury. Shock 2004, 21:401-9.
54. Strey CW, Markiewski M, Mastellos D. The proinflammatory mediators C3a and C5a are essential for liver regeneration. J Exp Med 2003, 198:913-23.
55. Mastellos D, Papadimitriou JC, Franchini S, Tsonis PA, Lambris JD. A novel role of complement: mice deficient in the fifth component of complement (C5) exhibit impaired liver regeneration. J Immunol 2001, 166:2479-86.
56. Xing T, Li L, Cao H, Huang J. Altered immune function of monocytes in different stages of patients with acute on chronic liver failure. Clin Exp Immunol 2007, 147:184-8.
57. Szabo G, Mandrekar P, Dolganiuc A. Innate immune response and hepatic inflammation. Semin Liver Dis 2007, 27:339-50.
58. Ramaiah SK, Jaeschke H. Role of neutrophils in the pathogenesis of acute inflammatory liver injury. Toxicol Pathol 2007, 35:757-66.
59. Jaeschke H, Hasegawa T. Role of neutrophils in acute inflammatory liver injury. Liver Int 2006, 26:912-9.
60. Jaeschke H, Ho YS, Fisher MA, Lawson JA, Farhood A. Glutathione peroxidase-deficient mice are more susceptible to neutrophil-mediated hepatic parenchymal cell injury during endotoxemia: importance of an intracellular oxidant stress. Hepatology 1999, 29:443-50.
61. Liu ZX, Han D, Gunawan B, Kaplowitz N. Neutrophil depletion protects against murine acetaminophen hepatotoxicity. Hepatology 2006, 43:1220-30.
62. Dong Z, Wei H, Sun R, Tian Z. The roles of innate immune cells in liver injury and regeneration. Cell Mol Immunol 2007, 4:241-52.
63. Radaeva S, Sun R, Jaruga B. Natural killer cells ameliorate liver fibrosis by killing activated stellate cells in NKG2D-dependent and tumor necrosis factor-related apoptosis-inducing ligand-dependent manners. Gastroenterology 2006, 130:435-52.
64. Ochi M, Ohdan H, Mitsuta H. Liver NK cells expressing TRAIL are toxic against self hepatocytes in mice. Hepatology 2004, 39:1321-31.
65. Zou Y, Chen T, Han M. Increased killing of liver NK cells by Fas/Fas ligand and NKG2D/NKG2D ligand contributes to hepatocyte necrosis in virus-induced liver failure. J Immunol 2010, 184:466-75.
66. Tiegs G. Cellular and cytokine-mediated mechanisms of inflammation and its modulation in immune-mediated liver injury. Z Gastroenterol 2007, 45:63-70.
67. Kakimi K, Guidotti LG, Koezuka Y, Chisari FV. Natural killer T cell activation inhibits hepatitis B virus replication in vivo. J Exp Med 2000, 192:921-30.
68. Sumpter TL, Abe M, Tokita D, Thomson AW. Dendritic cells, the liver, and transplantation. Hepatology 2007, 46:2021-31.
69. Asselin-Paturel C, Brizard G, Chemin K. Type I interferon dependence of plasmacytoid dendritic cell activation and migration. J Exp Med 2005, 201:1157-67.
70. Ju C. Immunological mechanisms of drug-induced liver injury. Curr Opin Drug Discov Devel 2005, 8:38-43.
71. Rudich N, Zamir G, Pappo O. Focal liver necrosis appears early after partial hepatectomy and is dependent on T cells and antigen delivery from the gut. Liver Int 2009, 29:1273-84.
72. Thimme R, Wieland S, Steiger C. CD8(+) T cells mediate viral clearance and disease pathogenesis during acute hepatitis B virus infection. J Virol 2003, 77:68-76.
73. Boettler T, Panther E, Bengsch B. Expression of the interleukin-7 receptor alpha chain (CD127) on virus-specific CD8+T cells identifies functionally and phenotypically defined memory T cells during acute resolving hepatitis B virus infection. J Virol 2006, 80:3532-40.
74. Urbani S, Boni C, Missale G. Virus-specific CD8+lymphocytes share the same effector-memory phenotype but exhibit functional differences in acute hepatitis B and C. J Virol 2002, 76:12423-34.
75. Webster GJ, REIGNAT S, MAINI M K. Incubation phase of acute hepatitis B in man: dynamic of cellular immune mechanisms. Hepatology 2000, 32:1117-24.
76. Maini MK, Boni C, Ogg GS. Direct ex vivo analysis of hepatitis B virus-specific CD8(+) T cells associated with the control of infection. Gastroenterology 1999, 117:1386-96.
77. Maini MK, Boni C, Lee CK. The role of virus-specific CD8(+) cells in liver damage and viral control during persistent hepatitis B virus infection. J Exp Med 2000, 191:1269-80.
78. Boni C, Fisicaro P, Valdatta C. Characterization of hepatitis B virus (HBV)-specific T-cell dysfunction in chronic HBV infection. J Virol 2007, 81:4215-25.
79. Bertoletti A, Maini M, Williams R. Role of hepatitis B virus specific cytotoxic T cells in liver damage and viral control. Antiviral Res 2003, 60:61-6.
80. Kondo Y, Kobayashi K, Asabe S. Vigorous response of cytotoxic T lymphocytes associated with systemic activation of CD8 T lymphocytes in fulminant hepatitis B. Liver Int 2004, 24:561-7.
81. Trehanpati N, Geffers R, Sukriti S. Gene expression signatures of peripheral CD4+T cells clearly discriminate between patients with acute and chronic hepatitis B infection. Hepatology 2009, 49:781-90.
82. Robinson R T, Wang J, Cripps JG. End-organ damage in a mouse model of fulminant liver inflammation requires CD4+T cell production of IFN-gamma but is independent of Fas. J Immunol 2009, 182:3278-84.
83. Lafdil F, Wang H, Park O. Myeloid STAT3 inhibits T cell-mediated hepatitis by regulating T helper 1 cytokine and interleukin-17 production. Gastroenterology 2009, 137:2125-35. e1-2
84. Zhang JY, Zhang Z, Lin F. Interleukin-17-producing CD4(+) T cells increase with severity of liver damage in patients with chronic hepatitis B. Hepatology 2010, 51:81-91.
85. Wei HX, Chuang YH, Li B. CD4+CD25+Foxp3+regulatory T cells protect against T cell-mediated fulminant hepatitis in a TGF-beta-dependent manner in mice. J Immunol 2008, 181:7221-9.
86. Erhardt A, Biburger M, Papadopoulos T, Tiegs G. IL-10, regulatory T cells, and Kupffer cells mediate tolerance in concanavalin A-induced liver injury in mice. Hepatology 2007, 45:475-85.
87. Shalev I, Wong K M, Foerster K. The novel CD4+CD25+regulatory T cell effector molecule fibrinogen-like protein 2 contributes to the outcome of murine fulminant viral hepatitis. Hepatology 2009, 49:387-97.
88. Knolle P A, Limmer A. Neighborhood politics: the immunoregulatory function of organ-resident liver endothelial cells. Trends Immunol 2001, 22:432-7.
89. Knolle PA, Uhrig A, Hegenbarth S. IL-10 down-regulates T cell activation by antigen-presenting liver sinusoidal endothelial cells through decreased antigen uptake via the mannose receptor and lowered surface expression of accessory molecules. Clin Exp Immunol 1998, 114:427-33.
90. Tang L, Yang J, Liu W. Liver sinusoidal endothelial cell lectin, LSECtin, negatively regulates hepatic T-cell immune response. Gastroenterology 2009, 137:1498-508. e1-5
91. Kojima N, Sato M, Suzuki A. Enhanced expression of B7-1, B7-2, and intercellular adhesion molecule 1 in sinusoidal endothelial cells by warm ischemia/reperfusion injury in rat liver. Hepatology 2001, 34((Part 1)):751-7.
92. Yan C, Zhou L, Han YP. Contribution of hepatic stellate cells and matrix metalloproteinase 9 in acute liver failure. Liver Int 2008, 28:959-71.
93. Louis H, Le Moine A, Flamand V. Critical role of interleukin 5 and eosinophils in concanavalin A-induced hepatitis in mice. Gastroenterology 2002, 122:2001-10.
94. Dos Santos DC, Da Silva Gomes Martinho JM, Pacheco-Moreira LF. Eosinophils involved in fulminant hepatic failure are associated with high interleukin-6 expression and absence of interleukin-5 in liver and peripheral blood. Liver Int 2009, 29:544-51.
95. Liu M, Chan C W, Mcgilvray I, Ning Q, Levy GA. Fulminant viral hepatitis: molecular and cellular basis, and clinical implications. Expert Rev Mol Med 2001, 2001:1-19.
96. Senzolo M, Agarwal S, Zappoli P. Heparin-like effect contributes to the coagulopathy in patients with acute liver failure undergoing liver transplantation. Liver Int 2009, 29:754-9.
97. Kuriyama N, Isaji S, Hamada T. Activated protein C prevents hepatic ischaemia-reperfusion injury in rats. Liver Int 2009, 29:299-307.
98. Iannacone M, Sitia G, Isogawa M. Platelets mediate cytotoxic T lymphocyte-induced liver damage. Nat Med 2005, 11:1167-9.
99. Sindram D, Porte RJ, Hoffman MR, Bentley RC, Clavien PA. Platelets induce sinusoidal endothelial cell apoptosis upon reperfusion of the cold ischemic rat liver. Gastroenterology 2000, 118:183-91.
100. Marsden PA, Ning Q, Fung LS. The Fgl2/fibroleukin prothrombinase contributes to immunologically mediated thrombosis in experimental and human viral hepatitis. J Clin Invest 2003, 112:58-66.
101. Zhu C, Sun Y, Luo X. Novel mfgl2 antisense plasmid inhibits murine fgl2 expression and ameliorates murine hepatitis virus type 3-induced fulminant hepatitis in BALB/cJ mice. Hum Gene Ther 2006, 17:589-600.
102. Zhu CL, Yan WM, Zhu F. Fibrinogen-like protein 2 fibroleukin expression and its correlation with disease progression in murine hepatitis virus type 3-induced fulminant hepatitis and in patients with severe viral hepatitis B. World J Gastroenterol 2005, 11:6936-40.
103. Han M, Yan W, Guo W. Hepatitis B virus-induced hFGL2 transcription is dependent on c-Ets-2 and MAPK signal pathway. J Biol Chem 2008, 283:32715-29.
104. Armbrust T, Kreissig M, Tron K, Ramadori G. Modulation of fibronectin gene expression in inflammatory mononuclear phagocytes of rat liver after acute liver injury. J Hepatol 2004, 40:638-45.
105. Beier JI, Luyendyk JP, Guo L. Fibrin accumulation plays a critical role in the sensitization to lipopolysaccharide-induced liver injury caused by ethanol in mice. Hepatology 2009, 49:1545-53.
106. Neuhuber WL, Tiegs G. Innervation of immune cells: evidence for neuroimmunomodulation in the liver. Anat Rec A Discov Mol Cell Evol Biol 2004, 280:884-92.
107. Oben JA, Roskams T, Yang S. Sympathetic nervous system inhibition increases hepatic progenitors and reduces liver injury. Hepatology 2003, 38:664-73.
108. Chida Y, Sudo N, Takaki A, Kubo C. The hepatic sympathetic nerve plays a critical role in preventing Fas induced liver injury in mice. Gut 2005, 54:994-1002.
109. Borovikova LV, Ivanova S, Zhang M. Vagus nerve stimulation attenuates the systemic inflammatory response to endotoxin. Nature 2000, 405:458-62.
110. Sanchez-Osorio M, Duarte-Rojo A, Martinez-Benitez B, Torre A, Uribe M. Anabolic-androgenic steroids and liver injury. Liver Int 2008, 28:278-82.
111. Sanchez O, Almagro A, Viladrich M, Ramirez I, Soley M. Sialoadenectomy enhances hepatic injury induced by lipopolysaccharide/galactosamine in mice. Liver Int 2008, 28:878-88.
112. Baghdasaryan A, Fickert P, Fuchsbichler A. Role of hepatic phospholipids in development of liver injury in Mdr2 (Abcb4) knockout mice. Liver Int 2008, 28:948-58.
113. Kerem M, Bedirli A, Pasaoglu H. Effect of adrenomedullin on hepatic damage in hepatic ischaemia/reperfusion injury in rats. Liver Int 2008, 28:972-81.
114. Yin M, Ikejima K, Wheeler MD. Estrogen is involved in early alcohol-induced liver injury in a rat enteral feeding model. Hepatology 2000, 31:117-23.
115. Fernandez V, Castillo I, Tapia G. Thyroid hormone preconditioning: protection against ischemia-reperfusion liver injury in the rat. Hepatology 2007, 45:170-7.
116. Kostopanagiotou G, Kalimeris K, Mourouzis I. Thyroid hormones alterations during acute liver failure: possible underlying mechanisms and consequences. Endocrine 2009, 36:198-204.
117. Belanger M, Butterworth RF. Acute liver failure: a critical appraisal of available animal models. Metab Brain Dis 2005, 20:409-23.
118. Tunon MJ, Alvarez M, Culebras JM, Gonzalez-Gallego J. An overview of animal models for investigating the pathogenesis and therapeutic strategies in acute hepatic failure. World J Gastroenterol 2009, 15:3086-98.
119. Wu ZG, Yan WM, Guo W. Telbivudine preserves T-helper 1 cytokine production and down regulates PD-L1 in a mouse model of viral hepatitis. J Viral Hepat 2010, 17((Suppl. 1)):24-33.
120. Ando K, Moriyama T, Guidotti LG. Mechanisms of class I restricted immunopathology. A transgenic mouse model of fulminant hepatitis. J Exp Med 1993, 178:1541-54.
121. Moriyama T, Guilhot S, Klopchin K. Immunobiology and pathogenesis of hepatocellular injury in hepatitis B virus transgenic mice. Science 1990, 248:361-4.
122. Tunon MJ, Sanchez-Campos S, Garcia-Ferreras J. Rabbit hemorrhagic viral disease: characterization of a new animal model of fulminant liver failure. J Lab Clin Med 2003, 141:272-8.
123. Prieto JM, Fernandez F, Alvarez V. Immunohistochemical localisation of rabbit haemorrhagic disease virus VP-60 antigen in early infection of young and adult rabbits. Res Vet Sci 2000, 68:181-7.
124. Sanchez-Campos S, Alvarez M, Culebras JM, Gonzalez-Gallego J, Tunon MJ. Pathogenic molecular mechanisms in an animal model of fulminant hepatic failure: rabbit hemorrhagic viral disease. J Lab Clin Med 2004, 144:215-22.