Interstrain differences in the progression of nonalcoholic steatohepatitis to fibrosis in mice are associated with altered hepatic iron metabolism

Journal of Nutritional Biochemistry

Volumn 25, Issue 12, 2014, Pages 1235-1242

  Shpyleva, Svitlana ^a   Pogribna, Marta ^a   Cozart, Christy ^a   Bryant, Matthew S ^a   Muskhelishvili, Levan ^a   Tryndyak, Volodymyr P ^a   Ross, Sharon A ^b   Beland, Frederick A ^a   Pogribny, Igor P ^a  

^a NATIONAL CENTER FOR TOXICOLOGICAL RESEARCH   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

Author keywords

Iron metabolism; IRP1; Liver fibrogenesis; Methyl deficient diet; MiR 200a; NAFLD

Indexed keywords

CHOLINE; COLLAGEN TYPE 1; FERRITIN; FOLIC ACID; IRON; IRON REGULATORY PROTEIN 1; MICRORNA 200A; MICRORNA 223; PROTEIN; PROTEIN ACTA2; SMAD3 PROTEIN; TRANSFERRIN RECEPTOR; TRIACYLGLYCEROL; UNCLASSIFIED DRUG; APOFERRITIN; CATION TRANSPORT PROTEIN; METAL TRANSPORTING PROTEIN 1; MICRORNA; MIRN200 MICRORNA, MOUSE; MIRN223 MICRORNA, MOUSE; TFRC PROTEIN, MOUSE;

129S1/SVIMJ MOUSE; A J MOUSE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIETARY INTAKE; DISEASE SEVERITY; DOWN REGULATION; FERRITIN HEAVY CHAIN GENE; FIBROGENESIS; GENE EXPRESSION REGULATION; IRON METABOLISM; IRON REGULATORY PROTEIN 1 GENE; LIVER FIBROSIS; LIVER INJURY; LIVER LEVEL; LIVER METABOLISM; MALE; MOUSE; MOUSE MODEL; MOUSE STRAIN; NONALCOHOLIC FATTY LIVER; NONHUMAN; RECEPTOR GENE; SLC40A1 GENE; STRAIN DIFFERENCE; TRANSFERRIN RECEPTOR GENE; WSB/EIJ MOUSE; ANIMAL; C57BL MOUSE; COMPLICATION; CYTOLOGY; DISEASE COURSE; FOLIC ACID DEFICIENCY; GENETICS; INBRED MOUSE STRAIN; LIVER; LIVER CELL; LIVER CIRRHOSIS; METABOLISM; PATHOLOGY; VITAMIN DEFICIENCY;

MUS;

ANIMALS; APOFERRITINS; CATION TRANSPORT PROTEINS; CHOLINE DEFICIENCY; DISEASE PROGRESSION; DOWN-REGULATION; FOLIC ACID DEFICIENCY; HEPATOCYTES; IRON; IRON REGULATORY PROTEIN 1; LIVER; LIVER CIRRHOSIS; MALE; MICE; MICE, INBRED C57BL; MICE, INBRED STRAINS; MICRORNAS; NON-ALCOHOLIC FATTY LIVER DISEASE; RECEPTORS, TRANSFERRIN;

EID: 84922816405     PISSN: 09552863     EISSN: 18734847     Source Type: Journal    
DOI: 10.1016/j.jnutbio.2014.06.012     Document Type: Article

References (39)

1. Smith B.W., Adams L.A. Non-alcoholic fatty liver disease. Crit Rev Clin Lab Sci 2011, 48:97-113.
2. Cohen J.C., Horton J.D., Hobbs H.H. Human fatty liver disease: old questions and new insights. Science 2011, 332:1519-1523.
3. Chalasani N., Younossi Z., Lavine J.E., Diehl A.M., Brunt E.M., Cusi K., et al. The diagnosis and management of non-alcoholic fatty liver disease: practice guideline by the American Association for the Study Liver Diseases, American College of Gastroenterology, and the American Gastroenterological Association. Hepatology 2012, 55:2005-2023.
4. Bhala N., Jouness R.I., Bugianesi E. Epidemiology and natural history of patients with NAFLD. Curr Pharm Des 2013, 19:5169-5176.
5. Siegel A.B., Zhu A.X. Metabolic syndrome and hepatocellular carcinoma: two growing epidemics with a potential link. Cancer 2009, 115:5651-5661.
6. Tilg H., Moschen A.R. Evolution of inflammation in nonalcoholic fatty liver disease: the multiple parallel hits hypothesis. Hepatology 2010, 52:1836-1846.
7. Tessari P., Coracina A., Cosma A., Tiengo A. Hepatic lipid metabolism and non-alcoholic fatty liver disease. Nutr Metab Cardiovasc Dis 2009, 19:291-302.
8. Rolo A.P., Teodoro J.S., Palmeira C.M. Role of oxidative stress in the pathogenesis of nonalcoholic steatohepatitis. Free Radic Biol Med 2012, 52:59-69.
9. Farrell G.C., van Rooyen D., Gan L., Chitturi S. NASH is an inflammatory disorder: pathogenic, prognostic and therapeutic implications. Gut Liver 2012, 6:149-171.
10. Pagliassotti M.J. Endoplasmic reticulum stress in nonalcoholic fatty liver disease. Annu Rev Nutr 2012, 32:17-33.
11. Nelson J.E., Wilson L., Brunt E.M., Yeh M.M., Kleiner D.E., Unalp-Arida A., et al. Nonalcoholic Steatohepatitis Clinical Research Network. Relationship between the pattern of hepatic iron deposition and histological severity in nonalcoholic fatty liver disease. Hepatology 2011, 53:448-457.
12. Dongiovanni P., Fracanzani A.L., Fargion S., Valenti L. Iron in fatty liver and in the metabolic syndrome: a promising therapeutic target. J Hepatol 2011, 55:920-932.
13. Corradini E., Pitrangelo A. Iron and steatohepatitis. J Gastroenterol Hepatol 2012, 27:42-46.
14. Tryndyak V., de Conti A., Kobets T., Kutanzi K., Koturbash I., Han T., et al. Interstrain differences in the severity of liver injury induced by a choline- and folate-deficient diet in mice are associated with dysregulation of genes involved in lipid metabolism. FASEB J 2012, 26:4592-4602.
15. Pogribny I.P., Kutanzi K., Melnyk S., de Conti A., Tryndyak V., Montgomery B., et al. Strain-dependent dysregulation of one-carbon metabolism in male mice is associated with choline- and folate-deficient diet-induced liver injury. FASEB J 2013, 27:2233-2243.
16. Oppenheim E.W., Adelman C., Liu X., Stover P.J. Heavy chain ferritin enhances serine hydroxymethyltransferase expression and de novo thymidine biosynthesis. J Biol Chem 2001, 276:19855-19861.
17. Oliveira S.J., de Sousa M., Pinto J.P. ER stress and iron homeostasis: a new frontier for the UPR. Biochem Res Int 2011, 2011:896474.
18. Ahmed U., Latham P.S., Oates P.S. Interactions between hepatic iron and lipid metabolism with possible relevance to steatohepatitis. World J Gastroenterol 2012, 18:4651-4658.
19. Tan T.C., Crawford D.H., Jaskowski L.A., Subramaniam V.N., Clouston A.D., Crane D.I., et al. Excess iron modulates endoplasmic reticulum stress-associated pathways in a mouse model of alcohol and high-fat diet-induced liver injury. Lab Invest 2013, 93:1295-1312.
20. Takeuchi-Yorimoti A., Noto T., Yamada A., Miyamae Y., Oishi Y., Matsumoto M. Persistent fibrosis in the liver of choline-deficient and iron-supplemented L-amino acid-defined diet-induced nonalcoholic steatohepatitis rat due to continuing oxidative stress after choline supplementation. Toxicol Appl Pharmacol 2013, 268:264-277.
21. Mitsuyoshi H., Yasui K., Harano Y., Endo M., Tsuji K., Minami M., et al. Analysis of hepatic genes involved in the metabolism of fatty acids and iron in nonalcoholic fatty liver disease. Hepatol Res 2009, 39:366-373.
22. Tryndyak V.P., Latendresse J.R., Montgomery B., Ross S.A., Beland F.A., Rusyn I., et al. Plasma microRNAs are sensitive indicators of inter-strain differences in the severity of liver injury induced in mice by a choline- and folate-deficient diet. Toxicol Appl Pharmacol 2012, 262:52-59.
23. Meguro R., Asano Y., Odagiri S., Iwatsuki H., Shoumura K. Nonheme-iron histochemistry for light and electron microscopy: a historical, theoretical and technical review. Arch Histol Cytol 2007, 70:1-19.
24. Shpyleva S.I., Muskhelishvili L., Tryndyak V.P., Koturbash I., Tokar E.J., Waalkes M.P., et al. Chronic administration of 2-acetylaminofluorene alters the cellular iron metabolism in rat liver. Toxicol Sci 2011, 123:433-440.
25. Tacke F., Weiskirchen R. Update on hepatic stellate cells: pathogenic role in liver fibrosis and novel isolation techniques. Expert Rev Gastroenterol Hepatol 2012, 6:67-80.
26. Rouault T.A. The role of iron regulatory proteins in mammalian iron homeostasis and disease. Nat Chem Biol 2006, 2:406-4114.
27. Anderson C.P., Shen M., Eisenstein R.S., Leibold E.A. Mammalian iron metabolism and its control by iron regulatory proteins. Biochim Biophys Acta 1823, 2012:1468-1483.
28. Hevi S., Chuck S.L. Ferritins can regulate the secretion of apolipoprotein B. J Biol Chem 2003, 278:31924-31929.
29. Chitturi S., George J. Interaction of iron, insulin resistance, and nonalcoholic steatohepatitis. Curr Gastroenterol Rep 2003, 5:18-25.
30. Ruddell R.G., Hoang-Le D., Barwood J.M., Rutherford P.S., Piva T.J., Watters D.J., et al. Ferritin functions as a proinflamatory cytokine via iron-independent protein kinase C zeta/nuclear factor kappaB-regulated signaling in rat hepatic stellate cells. Hepatology 2009, 49:887-900.
31. George D.K., Goldwurm S., MacDonald G.A., Cowley L.L., Walker N.I., Ward P.J., et al. Increased hepatic iron concentration in nonalcoholic steatohepatitis associated with increased fibrosis. Gastroenterology 1998, 114:311-318.
32. Valenti L., Fracanzani A.L., Bugianesi E., Dongiovanni P., Calmozzi E., Vanni E., et al. HFE genotype, parenchymal iron accumulation, and liver fibrosis in patients with nonalcoholic fatty liver disease. Gastroenterology 2010, 138:905-912.
33. Tsuchiya A., Ashla A.A., Hoshikawa Y., Matsumi Y., Kanki K., Enjoji M., et al. Iron state in association with retinoid metabolism in non-alcoholic fatty liver disease. Hepatol Res 2010, 40:1227-1238.
34. Kowdley K.V., Belt P., Wilson L.A., Yeh M.M., Neuschwander-Tetri B.A., Chalasani N., et al. Serum ferritin is an independent predictor of histologic severity and advanced fibrosis in patients with nonalcoholic fatty liver disease. Hepatology 2012, 55:77-85.
35. Bridle K.R., Crawford D.H.G., Ramm G.A. Identification and characterization of the hepatic stellate cell transferrin receptor. Am J Pathol 2003, 162:1661-1667.
36. Ramm G.A., Britton R.S., O'Neil R., Bacon B.R. Identification and characterization of a receptor for tissue ferritin on activated rat lipocytes. J Clin Invest 1994, 94:9-15.
37. Feng Q., Migas M.C., Waheed A., Britton R.S., Fleming R.E. Ferritin upregulates hepatic expression of bone morphogenic protein 6 and hepcidin in mice. Am J Physiol Gastrointest Liver Physiol 2012, 302:G-1397-G-1404.
38. Eisenstein R.S. Iron regulatory proteins and the molecular control of mammalian iron metabolism. Annu Rev Nutr 2000, 20:627-662.
39. Smith S.R., Cooperman S., Lavaute T., Tresser N., Ghosh M., Meyron-Holtz E., et al. Severity of neurodegeneration correlates with compromise of iron metabolism in mice with iron regulatory protein deficiencies. Ann N Y Acad Sci 2004, 1012:65-83.