An improved mouse model that rapidly develops fibrosis in non-alcoholic steatohepatitis

International Journal of Experimental Pathology

Volumn 94, Issue 2, 2013, Pages 93-103

  Matsumoto, Masahiko ^a   Hada, Natsuko ^b   Sakamaki, Yoshiyuki ^a   Uno, Akiko ^a   Shiga, Toshihiko ^a   Tanaka, Chiaki ^a   Ito, Tsuneo ^b   Katsume, Asao ^b   Sudoh, Masayuki ^b  

^a Chugai Research Institute for Medical Science Inc   (Japan)

^b CHUGAI PHARMACEUTICAL CO LTD   (Japan)

Author keywords

Fibrosis; High fat diet; Methionine restricted diet; Mouse model; Non alcoholic steatohepatitis

Indexed keywords

ALANINE AMINOTRANSFERASE; AMINO ACID; CHOLINE; COLLAGEN; HYDROXYPROLINE; MESSENGER RNA; METHIONINE;

ALANINE AMINOTRANSFERASE BLOOD LEVEL; AMINO ACID DEFICIENCY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CONTROLLED STUDY; DISEASE COURSE; FATTY LIVER; HISTOPATHOLOGY; LIPID DIET; LIVER FIBROSIS; MALE; MOUSE; NONALCOHOLIC FATTY LIVER; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; WEIGHT GAIN; WESTERN BLOTTING;

FIBROSIS; HIGH-FAT DIET; METHIONINE-RESTRICTED DIET; MOUSE MODEL; NON-ALCOHOLIC STEATOHEPATITIS;

ALANINE TRANSAMINASE; ANIMALS; ASPARTATE AMINOTRANSFERASES; BIOLOGICAL MARKERS; CHOLINE DEFICIENCY; DIET, FAT-RESTRICTED; DIET, HIGH-FAT; DISEASE MODELS, ANIMAL; FATTY LIVER; HUMANS; LIVER; LIVER CIRRHOSIS; MALE; METHIONINE; MICE; MICE, INBRED A; MICE, INBRED C57BL; OBESITY; SPECIFIC PATHOGEN-FREE ORGANISMS; TIME FACTORS;

EID: 84875056271     PISSN: 09599673     EISSN: 13652613     Source Type: Journal    
DOI: 10.1111/iep.12008     Document Type: Article

References (46)

1. Anderson N. & Borlak J. (2008) Molecular mechanisms and therapeutic targets in steatosis and steatohepatitis. Pharmacol. Rev. 60, 311-357.
2. Anstee Q.M. & Goldin R.D. (2006) Mouse models in non-alcoholic fatty liver disease and steatohepatitis research. Int. J. Exp. Pathol. 87, 1-16.
3. Bellentani S. & Marino M. (2009) Epidemiology and natural history of non-alcoholic fatty liver disease (NAFLD). Ann. Hepatol. 8(Suppl 1), S4-S8.
4. Boyd J.N., Graham E.S., Graham T.C., Tennant B.C. (1985) A comparison of the response of woodchucks and rats to variations in dietary lipotrope and lipid content. J. Nutr. 115, 1136-1146.
5. Burrage L.C., Baskin-Hill A.E., Sinasac D.S. et al. (2010) Genetic resistance to diet-induced obesity in chromosome substitution strains of mice. Mamm. Genome 21, 115-129.
6. Caballero F., Fernandez A., Matias N. et al. (2010) Specific contribution of methionine and choline in nutritional nonalcoholic steatohepatitis: impact on mitochondrial S-adenosyl-l-methionine and glutathione. J. Biol. Chem. 285, 18528-18536.
7. Chahl J.S. & Kratzing C.C. (1966) Environmental temperature and choline requirements in rats. II. Choline and methionine requirements for lipotropic activity. J. Lipid Res. 7, 22-26.
8. Day C.P. (2002) Pathogenesis of steatohepatitis. Best Pract. Res. Clin. Gastroenterol. 16, 663-678.
9. Day C.P. & James O.F.W. (1998) Steatohepatitis: a tale of two "hits"? Gastroenterology 114, 842-845.
10. Denda A., Kitayama W., Kishida H. et al. (2002) Development of hepatocellular adenomas and carcinomas associated with fibrosis in C57BL/6J male mice given a choline-deficient, l-amino acid-defined diet. Jpn. J. Cancer Res. 93, 125-132.
11. Denda A., Kitayama W., Kishida H. et al. (2007) Expression of inducible nitric oxide (NO) synthase but not prevention by its gene ablation of hepatocarcinogenesis with fibrosis caused by a choline-deficient, l-amino acid-defined diet in rats and mice. Nitric Oxide 16, 164-176.
12. Folch J., Lees M., Sloane-Stanley G.H. (1957) A simple method for the isolation and purification of total lipides from animal tissues. J. Biol. Chem. 226, 497-509.
13. Fujita K., Nozaki Y., Wada K. et al. (2008) Effectiveness of antiplatelet drugs against experimental non-alcoholic fatty liver disease. Gut 57, 1583-1591.
14. Gambino R., Cassader M., Pagano G., Durazzo M., Musso G. (2007) Polymorphism in microsomal triglyceride transfer protein: a link between liver disease and atherogenic postprandial lipid profile in NASH? Hepatology 45, 1097-1107.
15. Guilherme A., Virbasius J.V., Puri V., Czech M.P. (2008) Adipocyte dysfunctions linking obesity to insulin resistance and type 2 diabetes. Nat. Rev. Mol. Cell Biol. 9, 367-377.
16. György P., Cardi E., Rose C.S., Hirooka M., Langer B.W. Jr (1967) Lipid transport in experimental dietary hepatic injury in rats. J. Nutr. 93, 568-578.
17. Hill-Baskin A.E., Markiewski M.M., Buchner D.A. et al. (2009) Diet-induced hepatocellular carcinoma in genetically predisposed mice. Hum. Mol. Genet. 18, 2975-2988.
18. Hironaka K., Sakaida I., Uchida K., Okita K. (2000) Correlation between stellate cell activation and serum fibrosis markers in choline-deficient l-amino acid-defined diet-induced rat liver fibrosis. Dig. Dis. Sci. 45, 1935-1943.
19. Inayama S., Shibata T., Ohtsuki J., Saito S. (1978) A new microanalytical method for determination of hydroxyproline in connective tissue. Keio J. Med. 27, 43-46.
20. John A.M. & Bell J.M. (1976) Amino acid requirements of the growing mouse. J. Nutr. 106, 1361-1367.
21. Kamada Y., Matsumoto H., Tamura S. et al. (2007) Hypoadiponectinemia accelerates hepatic tumor formation in a nonalcoholic steatohepatitis mouse model. J. Hepatol. 47, 556-564.
22. Kashireddy P.V. & Rao M.S. (2004) Lack of peroxisome proliferator-activated receptor alpha in mice enhances methionine and choline deficient diet-induced steatohepatitis. Hepatol. Res. 30, 104-110.
23. Kivirikko K.I., Laitinen O., Prockop D.J. (1967) Modifications of a specific assay for hydroxyproline in urine. Anal. Biochem. 19, 249-255.
24. Kleiner D.E., Brunt E.M., Van Natta M. et al. (2005) Design and validation of a histological scoring system for nonalcoholic fatty liver disease. Hepatology 41, 1313-1321.
25. Kodama Y., Kisseleva T., Iwaisako K. et al. (2009) c-Jun N-terminal kinase-1 from hematopoietic cells mediates progression from hepatic steatosis to steatohepatitis and fibrosis in mice. Gastroenterology 137, 1467-1477.
26. Maina V., Sutti S., Locatelli I. et al. (2012) Bias in macrophage activation pattern influences non-alcoholic steatohepatitis (NASH) in mice. Clin. Sci. 122, 545-553.
27. McAnulty R.J. (2005) Methods for measuring hydroxyproline and estimating in vivo rates of collagen synthesis and degradation. Methods Mol. Med. 117, 189-207.
28. Minehira K., Young S.G., Villanueva C.J. et al. (2008) Blocking VLDL secretion causes hepatic steatosis but does not affect peripheral lipid stores or insulin sensitivity in mice. J. Lipid Res. 49, 2038-2044.
29. Nagatani Y., Muto Y., Sato H., Iijima M. (1986) An improved method for the determination of hydroxyproline. Yakugaku Zasshi 106, 41-46 (in Japanese).
30. Nakae D., Yoshiji H., Maruyama H., Kinugasa T., Denda A., Konishi Y. (1990) Production of both 8-hydroxydeoxyguanosine in liver DNA and gamma-glutamyltransferase-positive hepatocellular lesions in rats given a choline-deficient, l-amino acid-defined diet. Jpn. J. Cancer Res. 81, 1081-1084.
31. Nakae D., Yoshiji H., Mizumoto Y. et al. (1992) High incidence of hepatocellular carcinomas induced by a choline deficient l-amino acid defined diet in rats. Cancer Res. 52, 5042-5045.
32. Namikawa C., Shun-Ping Z., Vyselaar J.R. et al. (2004) Polymorphisms of microsomal triglyceride transfer protein gene and manganese superoxide dismutase gene in non-alcoholic steatohepatitis. J. Hepatol. 40, 781-786.
33. National Research Council (NRC) (1995) Nutrient requirements of the laboratory mouse. In: Nutrient Requirements of Laboratory Animals, 4th edn, pp. 80-102 (ed. N.J. Benevenga ), Washington, D.C.: National Academy Press.
34. Noga A.A. & Vance D.E. (2003) Insights into the requirement of phosphatidylcholine synthesis for liver function in mice. J. Lipid Res. 44, 1998-2005.
35. Rangnekar A.S., Lammert F., Igolnikov A., Green R.M. (2006) Quantitative trait loci analysis of mice administered the methionine-choline deficient dietary model of experimental steatohepatitis. Liver Int. 26, 1000-1005.
36. Raubenheimer P.J., Nyirenda M.J., Walker B.R. (2006) A choline-deficient diet exacerbates fatty liver but attenuates insulin resistance and glucose intolerance in mice fed a high-fat diet. Diabetes 55, 2015-2020.
37. Rinella M.E., Elias M.S., Smolak R.R., Fu T., Borensztajn J., Green R.M. (2008) Mechanisms of hepatic steatosis in mice fed a lipogenic methionine choline-deficient diet. J. Lipid Res. 49, 1068-1076.
38. Rizki G., Arnaboldi L., Gabrielli B. et al. (2006) Mice fed a lipogenic methionine-choline-deficient diet develop hypermetabolism coincident with hepatic suppression of SCD-1. J. Lipid Res. 47, 2280-2290.
39. Sakaida I., Kubota M., Kayano K., Takenaka K., Mori K., Okita K. (1994) Prevention of fibrosis reduces enzyme-altered lesions in the rat liver. Carcinogenesis 15, 2201-2206.
40. Samuel V.T., Liu Z.X., Qu X. et al. (2004) Mechanism of hepatic insulin resistance in non-alcoholic fatty liver disease. J. Biol. Chem. 279, 32345-323453.
41. Schattenberg J.M., Wang Y., Singh R., Rigoli R.M., Czaja M.J. (2005) Hepatocyte CYP2E1 overexpression and steatohepatitis lead to impaired hepatic insulin signaling. J. Biol. Chem. 280, 9887-9894.
42. Sha W., da Costa K.A., Fischer L.M. et al. (2010) Metabolomic profiling can predict which humans will develop liver dysfunction when deprived of dietary choline. FASEB J. 24, 2962-2975.
43. Song L., da Costa K.A., Fischer L.M. et al. (2005) Polymorphism of the PEMT gene and susceptibility to nonalcoholic fatty liver disease (NAFLD). FASEB J. 19, 1266-1271.
44. Tilg H. & Moschen A.R. (2010) Evolution of inflammation in nonalcoholic fatty liver disease: the multiple parallel hits hypothesis. Hepatology 52, 1836-1846.
45. Tsujimoto T., Kawaratani H., Kitazawa T. et al. (2009) Immunotherapy for nonalcoholic steatohepatitis using the multiple cytokine production modulator Y-40138. World J. Gasteroenterol. 15, 5533-5540.
46. Yamazaki Y., Kakizaki S., Takizawa D. et al. (2008) Interstrain differences in susceptibility to non-alcoholic steatohepatitis. J. Gastroenterol. Hepatol. 23, 276-282.