Commonly used animal models of non-alcoholic steatohepatitis

Hepatobiliary and Pancreatic Diseases International

Volumn 8, Issue 3, 2009, Pages 233-240

  Fan, Jian Gao ^a   Qiao, Liang ^b  

^a SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

Animal models; Non alcoholic fatty liver disease; Non alcoholic steatohepatitis

Indexed keywords

ACYL COENZYME A OXIDASE; CHOLINE; LEPTIN; LEPTIN RECEPTOR; METHIONINE; METHIONINE ADENOSYLTRANSFERASE; METHIONINE ADENOSYLTRANSFERASE 1A; NUCLEAR RESPIRATORY FACTOR 1; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; UNCLASSIFIED DRUG;

ANIMAL MODEL; COMBINATION MODEL; EXPERIMENTAL MODEL; FATTY ACID METABOLISM; FATTY LIVER; GENE DELETION; GENE OVEREXPRESSION; GENETIC MODEL; HEPATITIS; NON ALCOHOLIC STEATOHEPATITIS; NONHUMAN; NUTRITIONAL SUPPORT; REVIEW; VITAMIN DEFICIENCY;

ANIMALS; DIET; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; FATTY LIVER; INFLAMMATION;

EID: 67549113925     PISSN: 14993872     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (70)

1. Angulo P. Nonalcoholic fatty liver disease. N Engl J Med 2002;346:1221-1231.
2. Angulo P. GI epidemiology: nonalcoholic fatty liver disease. Aliment Pharmacol Ther 2007;25:883-889.
3. London RM, George J. Pathogenesis of NASH: animal models. Clin Liver Dis 2007;11:55-74, viii. (Pubitemid 46829974)
4. Williams R. Global challenges in liver disease. Hepatology 2006;44:521-526. (Pubitemid 44433707)
5. Ong JP, Younossi ZM. Epidemiology and natural history of NAFLD and NASH. Clin Liver Dis 2007;11:1-16, vii.
6. Fan JG, Farrell GC. Epidemiology of non-alcoholic fatty liver disease in China. J Hepatol 2009;50:204-210.
7. Weston SR, Leyden W, Murphy R, Bass NM, Bell BP, Manos MM, et al. Racial and ethnic distribution of nonalcoholic fatty liver in persons with newly diagnosed chronic liver disease. Hepatology 2005;41:372-379. (Pubitemid 40165382)
8. McCullough AJ. The epidemiology and risk factors of NASH. In: Farrell GC, George J, Hall P, Mc McCullough AJ, ed. Fatty Liver Disease: NASH and Related Disorders. Oxford: Blackwell Publishing; 2005:23-37.
9. Fan JG, Saibara T, Chitturi S, Kim BI, Sung JJ, Chutaputti A. What are the risk factors and settings for non-alcoholic fatty liver disease in Asia-Pacific? J Gastroenterol Hepatol 2007;22:794-800.
10. Leclercq IA. Pathogenesis of steatohepatitis: insights from the study of animal models. Acta Gastroenterol Belg 2007; 70:25-31. (Pubitemid 46597998)
11. Day CP. Non-alcoholic steatohepatitis (NASH): where are we now and where are we going? Gut 2002;50:585-588.
12. Powell EE, Cooksley WG, Hanson R, Searle J, Halliday JW, Powell LW. The natural history of nonalcoholic steatohepatitis: a follow-up study of forty-two patients for up to 21 years. Hepatology 1990;11:74-80. (Pubitemid 20075105)
13. Harrison SA, Torgerson S, Hayashi PH. The natural history of nonalcoholic fatty liver disease: a clinical histopathological study. Am J Gastroenterol 2003;98:2042-2047. (Pubitemid 37185803)
14. Fan JG, Li F, Cai XB, Peng YD, Ao QH, Gao Y. Effects of nonalcoholic fatty liver disease on the development of metabolic disorders. J Gastroenterol Hepatol 2007;22:1086-1091. (Pubitemid 47019857)
15. Day CP, Saksena S. Non-alcoholic steatohepatitis: definitions and pathogenesis. J Gastroenterol Hepatol 2002;17:S377-384. (Pubitemid 35454314)
16. Ikura Y, Ohsawa M, Suekane T, Fukushima H, Itabe H, Jomura H, et al. Localization of oxidized phosphatidylcholine in nonalcoholic fatty liver disease: impact on disease progression. Hepatology 2006;43:506-514.
17. Choudhury J, Sanyal AJ. Insulin resistance in NASH. Front Biosci 2005;10:1520-1533. (Pubitemid 40529017)
18. Baskol G, Baskol M, Kocer D. Oxidative stress and antioxidant defenses in serum of patients with non-alcoholic steatohepatitis. Clin Biochem 2007;40:776-780. (Pubitemid 46961959)
19. Fan JG. Expression of mitochondrial uncoupling protein 2 and relationship to the content of adenosine triphosphate in liver of rats with nonalcoholic fatty liver disease. Gastroenterology 2004;126:A710.
20. Fan JG. Overexpression of peroxisome proliferator-activated receptors gamma and uncoupling protein-2 in liver of rats with nonalcoholic steatohepatitis. Hepatology 2003;36:A693.
21. Fan JG. Preventive effects of metformin on rats with nonalcoholic steatohepatitis. Hepatology 2003;36:A711.
22. Wanless IR, Shiota K. The pathogenesis of nonalcoholic steatohepatitis and other fatty liver diseases: a four-step model including the role of lipid release and hepatic venular obstruction in the progression to cirrhosis. Semin Liver Dis 2004;24:99-106. (Pubitemid 38496052)
23. Farrell GC, Larter CZ. Nonalcoholic fatty liver disease: from steatosis to cirrhosis. Hepatology 2006;43:S99-S112. (Pubitemid 43303974)
24. Larter CZ. Not all models of fatty liver are created equal: understanding mechanisms of steatosis development is important. J Gastroenterol Hepatol 2007;22:1353-1354. (Pubitemid 47274583)
25. Uno M, Kurita S, Misu H, Ando H, Ota T, Matsuzawa-Nagata N, et al. Tranilast, an antifibrogenic agent, ameliorates a dietary rat model of nonalcoholic steatohepatitis. Hepatology 2008;48:109-118. (Pubitemid 351975536)
26. Fan JG, Xu ZJ, Wang GL. Effect of lactulose on establishment of a rat non-alcoholic steatohepatitis model. World J Gastroenterol 2005;11:5053-5056. (Pubitemid 41227211)
27. Fan JG. Protective of pentoxifylline in nonalcoholic steatohepatitis in rats induced by fat-rich diet. Hepatology 2003;36:A696
28. Fan JG, Zhong L, Tia LY, Xu ZJ, Li MS, Wang GL. Effects of ursodeoxycholic acid and/or low-calorie diet on steatohepatitis in rats with obesity and hyperlipidemia. World J Gastroenterol 2005;11:2346-2350. (Pubitemid 40691349)
29. Fan JG, Chen LH, Xu ZJ, Zeng MD. Overexpression of hepatic plasminogen activator inhibitor type 1 mRNA in rabbits with fatty liver. World J Gastroenterol 2001;7:710-712.
30. Nakayama H, Otabe S, Ueno T, Hirota N, Yuan X, Fukutani T, et al. Transgenic mice expressing nuclear sterol regulatory element-binding protein 1c in adipose tissue exhibit liver histology similar to nonalcoholic steatohepatitis. Metabolism 2007;56:470-475. (Pubitemid 46427843)
31. Kitade M, Yoshiji H, Kojima H, Ikenaka Y, Noguchi R, Kaji K, et al. Leptin-mediated neovascularization is a prerequisite for progression of nonalcoholic steatohepatitis in rats. Hepatology 2006;44:983-991. (Pubitemid 46489563)
32. Sundaram SS, Whitington PF, Green RM. Steatohepatitis develops rapidly in transgenic mice overexpressing Abcb11 and fed a methionine-choline-deficient diet. Am J Physiol Gastrointest Liver Physiol 2005;288:G1321-1327. (Pubitemid 40741087)
33. Kashireddy PV, Rao MS. Lack of peroxisome proliferator-activated receptor alpha in mice enhances methionine and choline deficient diet-induced steatohepatitis. Hepatol Res 2004;30:104-110. (Pubitemid 41115272)
34. Baffy G, Zhang CY, Glickman JN, Lowell BB. Obesity-related fatty liver is unchanged in mice deficient for mitochondrial uncoupling protein 2. Hepatology 2002;35: 753-761. (Pubitemid 34258368)
35. Sahai A, Malladi P, Pan X, Paul R, Melin-Aldana H, Green RM, et al. Obese and diabetic db/db mice develop marked liver fibrosis in a model of nonalcoholic steatohepatitis: role of short-form leptin receptors and osteopontin. Am J Physiol Gastrointest Liver Physiol 2004;287:G1035-1043. (Pubitemid 39423696)
36. Honda H, Ikejima K, Hirose M, Yoshikawa M, Lang T, Enomoto N, et al. Leptin is required for fibrogenic responses induced by thioacetamide in the murine liver. Hepatology 2002;36:12-21. (Pubitemid 34700757)
37. Leclercq IA, Farrell GC, Schriemer R, Robertson GR. Leptin is essential for the hepatic fibrogenic response to chronic liver injury. J Hepatol 2002;37:206-213. (Pubitemid 34833082)
38. Romestaing C, Piquet MA, Bedu E, Rouleau V, Dautresme M, Hourmand-Ollivier I, et al. Long term highly saturated fat diet does not induce NASH in Wistar rats. Nutr Metab (Lond) 2007;4:4. (Pubitemid 46328647)
39. Baumgardner JN, Shankar K, Hennings L, Badger TM, Ronis MJ. A new model for nonalcoholic steatohepatitis in the rat utilizing total enteral nutrition to overfeed a high-polyunsaturated fat diet. Am J Physiol Gastrointest Liver Physiol 2008;294:G27-38.
40. Deng QG, She H, Cheng JH, French SW, Koop DR, Xiong S, et al. Steatohepatitis induced by intragastric overfeeding in mice. Hepatology 2005;42:905-914. (Pubitemid 41401129)
41. Svegliati-Baroni G, Candelaresi C, Saccomanno S, Ferretti G, Bachetti T, Marzioni M, et al. A model of insulin resistance and nonalcoholic steatohepatitis in rats: role of peroxisome proliferator-activated receptor-alpha and n-3 polyunsaturated fatty acid treatment on liver injury. Am J Pathol 2006;169:846-860. (Pubitemid 44411952)
42. Zou Y, Li J, Lu C, Wang J, Ge J, Huang Y, et al. High-fat emulsion-induced rat model of nonalcoholic steatohepatitis. Life Sci 2006;79:1100-1107. (Pubitemid 44102717)
43. Carmiel-Haggai M, Cederbaum AI, Nieto N. A high-fat diet leads to the progression of non-alcoholic fatty liver disease in obese rats. FASEB J 2005;19:136-138. (Pubitemid 40069943)
44. Musso G, Gambino R, De Michieli F, Cassader M, Rizzetto M, Durazzo M, et al. Dietary habits and their relations to insulin resistance and postprandial lipemia in nonalcoholic steatohepatitis. Hepatology 2003;37:909-916. (Pubitemid 36397404)
45. Rinella ME, Elias MS, Smolak RR, Fu T, Borensztajn J, Green RM. Mechanisms of hepatic steatosis in mice fed a lipogenic methionine choline-deficient diet. J Lipid Res 2008;49:1068-1076.
46. de Oliveira CP, de Lima VM, Simplicio FI, Soriano FG, de Mello ES, de Souza HP, et al. Prevention and reversion of nonalcoholic steatohepatitis in OB/OB mice by S-nitroso-N-acetylcysteine treatment. J Am Coll Nutr 2008;27:299-305.
47. Ito M, Suzuki J, Sasaki M, Watanabe K, Tsujioka S, Takahashi Y, et al. Development of nonalcoholic steatohepatitis model through combination of high-fat diet and tetracycline with morbid obesity in mice. Hepatol Res 2006;34:92-98. (Pubitemid 43137557)
48. Arsov T, Larter CZ, Nolan CJ, Petrovsky N, Goodnow CC, Teoh NC, et al. Adaptive failure to high-fat diet characterizes steatohepatitis in Almsl mutant mice. Biochem Biophys Res Commun 2006;342:1152-1159.
49. Brix AE, Elgavish A, Nagy TR, Gower BA, Rhead WJ, Wood PA. Evaluation of liver fatty acid oxidation in the leptin-deficient obese mouse. Mol Genet Metab 2002;75: 219-226. (Pubitemid 34971591)
50. Matsuzawa N, Takamura T, Kurita S, Misu H, Ota T, Ando H, et al. Lipid-induced oxidative stress causes steatohepatitis in mice fed an atherogenic diet. Hepatology 2007;46:1392-1403. (Pubitemid 350155521)
51. Savransky V, Bevans S, Nanayakkara A, Li J, Smith PL, Torbenson MS, et al. Chronic intermittent hypoxia causes hepatitis in a mouse model of diet-induced fatty liver. Am J Physiol Gastrointest Liver Physiol 2007;293:G871-877. (Pubitemid 47605939)
52. Wortham M, He L, Gyamfi M, Copple BL, Wan YJ. The transition from fatty liver to NASH associates with SAMe depletion in db/db mice fed a methionine choline-deficient diet. Dig Dis Sci 2008;53:2761-2774.
53. Wouters K, van Gorp PJ, Bieghs V, Gijbels MJ, Duimel H, Lütjohann D, et al. Dietary cholesterol, rather than liver steatosis, leads to hepatic inflammation in hyperlipidemic mouse models of nonalcoholic steatohepatitis. Hepatology 2008;48:474-486.
54. Cook WS, Jain S, Jia Y, Cao WQ, Yeldandi AV, Reddy JK, et al. Peroxisome proliferator-activated receptor alpha-responsive genes induced in the newborn but not prenatal liver of peroxisomal fatty acyl-CoA oxidase null mice. Exp Cell Res 2001;268:70-76. (Pubitemid 32678861)
55. Fan CY, Pan J, Chu R, Lee D, Kluckman KD, Usuda N, et al. Hepatocellular and hepatic peroxisomal alterations in mice with a disrupted peroxisomal fatty acyl-coenzyme A oxidase gene. J Biol Chem 1996;271:24698-24710. (Pubitemid 26333214)
56. Lu SC, Alvarez L, Huang ZZ, Chen L, An W, Corrales FJ, et al. Methionine adenosyltransferase 1A knockout mice are predisposed to liver injury and exhibit increased expression of genes involved in proliferation. Proc Natl Acad Sci U S A 2001;98:5560-5565.
57. Xu Z, Chen L, Leung L, Yen TS, Lee C, Chan JY. Liver-specific inactivation of the Nrf1 gene in adult mouse leads to nonalcoholic steatohepatitis and hepatic neoplasia. Proc Natl Acad Sci U S A 2005;102:4120-4125. (Pubitemid 40388565)
58. Stiles B, Wang Y, Stahl A, Bassilian S, Lee WP, Kim YJ, et al. Liver-specific deletion of'negative regulator Pten results in fatty liver and insulin hypersensitivity [corrected]. Proc Natl Acad Sci U S A 2004;101:2082-2087.
59. Sato W, Horie Y, Kataoka E, Ohshima S, Dohmen T, Iizuka M, et al. Hepatic gene expression in hepatocyte-specific Pten deficient mice showing steatohepatitis without ethanol challenge. Hepatol Res 2006;34:256-265.
60. Diehl AM. Lessons from animal models of NASH. Hepatol Res 2005;33:138-144. (Pubitemid 41799792)
61. Anstee QM, Goldin RD. Mouse models in non-alcoholic fatty liver disease and steatohepatitis research. Int J Exp Pathol 2006;87:1-16.
62. DeIa Pena A, Leclercq I, Field J, George J, Jones B, Farrell G. NF-kappaB activation, rather than TNF, mediates hepatic inflammation in a murine dietary model of steatohepatitis. Gastroenterology 2005;129:1663-1674. (Pubitemid 41597405)
63. Lieber CS, Leo MA, Mak KM, Xu Y, Cao Q, Ren C, et al. Model of nonalcoholic steatohepatitis. Am J Clin Nutr 2004;79:502-509. (Pubitemid 41115597)
64. Koteish A, Diehl AM. Animal models of steatosis. Semin Liver Dis 2001;21:89-104. (Pubitemid 32240489)
65. den Boer M, Voshol PJ, Kuipers F, Havekes LM, Romijn JA. Hepatic steatosis: a mediator of the metabolic syndrome. Lessons from animal models. Arterioscler Thromb Vasc Biol 2004;24:644-649.
66. Fan JG. Changes of Kupffer cell activity in the process of inducing the rat model of nonalcoholic steatohepatitis. Hepatology 2003;36:A705.
67. Fan JG. Relationship between hepatic SCD-1 expression and ATP content in rats with nonalcoholic fatty liver caused by fat-rich diet. J Hepatol 2007;46:A342
68. Nanji AA. Animal models of nonalcoholic fatty liver disease and steatohepatitis. Clin Liver Dis 2004;8:559-574, ix. (Pubitemid 39141143)
69. Farrell GC. Animal models of steatohepatitis. In: Farrell GC, George J, de la M. Hall P, McCullough AJ, eds. Fatty Liver Disease: NASH and Related Disorders. Malden, MA: Blackwell Publishing; 2005:91-108.
70. Yamazaki Y, Kakizaki S, Takizawa D, Ichikawa T, Sato K, Takagi H, et al. Interstrain differences in susceptibility to non-alcoholic steatohepatitis. J Gastroenterol Hepatol 2008;23:276-282. (Pubitemid 351257673)