MicroRNA changes, activation of progenitor cells and severity of liver injury in mice induced by choline and folate deficiency

Journal of Nutritional Biochemistry

Volumn 28, Issue , 2016, Pages 83-90

  Tryndyak, Volodymyr P ^a   Marrone, April K ^a   Latendresse, John R ^a   Muskhelishvili, Levan ^a   Beland, Frederick A ^a   Pogribny, Igor P ^a  

^a NATIONAL CENTER FOR TOXICOLOGICAL RESEARCH   (United States)

Author keywords

Liver injury; Methyl donor deficient diet; MicroRNA; Mouse; Progenitor cells

Indexed keywords

CHOLINE; FOLIC ACID; MICRORNA; MICRORNA 134; MICRORNA 409 3P; MICRORNA 410; MICRORNA 495; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CONTROLLED STUDY; DISEASE SEVERITY; FOLIC ACID DEFICIENCY; GENE EXPRESSION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LIVER INJURY; MALE; MOUSE; NONALCOHOLIC FATTY LIVER; NONHUMAN; STEM CELL; VITAMIN DEFICIENCY; ANIMAL; GENETICS; METABOLISM; PATHOLOGY;

ANIMALS; CHOLINE DEFICIENCY; FOLIC ACID DEFICIENCY; MICE; MICRORNAS; NON-ALCOHOLIC FATTY LIVER DISEASE; STEM CELLS;

EID: 84957824116     PISSN: 09552863     EISSN: 18734847     Source Type: Journal    
DOI: 10.1016/j.jnutbio.2015.10.001     Document Type: Article

References (50)

1. Vernon G., Baranova A., Younossi Z.M. Systemic review: the epidemiology and natural history of non-alcoholic fatty liver disease and non-alcoholic steatohepatitis in adults. Aliment Pharmacol Ther 2011, 34:274-285.
2. Masarone M., Federico A., Abenavoli L., Loguercio C., Persico M. Non alcoholic fatty liver: epidemiology and natural history. Rev Recent Clin Trials 2014, 9:126-133.
3. Cohen J.C., Horton J.D., Hobbs H.H. Human fatty liver disease: old questions and new insights. Science 2011, 332:1519-1523.
4. Bhala N., Jouness R.I.K., Bugianesi E. Epidemiology and natural history of patients with NAFLD. Curr Pharm Des 2013, 19:5169-5176.
5. White D.L., Kanwal F., El-Serag H.B. Association between nonalcoholic fatty liver disease and risk for hepatocellular cancer, based on systematic review. Clin Gastroenterol Hepatol 2012, 10:1342-1359.
6. 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.
7. 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.
8. Corbin K.D., Abdelmalek M.F., Spencer M.D., da Costa K.-A., Galanko J.A., Sha W., et al. Genetic signatures in choline and 1-carbon metabolism are associated with the severity of hepatic steatosis. FASEB J 2013, 27:1674-1689.
9. Shpyleva S., Pogribna M., Cozart C., Bryant M.S., Muskhelishvili L., Tryndyak V.P., et al. Interstrain differences in the progression of nonalcoholic steatohepatitis to fibrosis in mice are associated with altered hepatic iron metabolism. J Nutr Biochem 2014, 25:1235-1242.
10. 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 by a choline- and folate-deficient diet. Toxicol Appl Pharmacol 2012, 262:52-59.
11. Alisi A., Da Sacco L., Bruscalupi G., Piemonte F., Panera N., De Vito R., et al. Mirnome analysis reveals novel molecular determinants in the pathogenesis of diet-induced nonalcoholic fatty liver disease. Lab Invest 2011, 91:283-293.
12. Cheung O., Puri P., Eicken C., Contos M.J., Mirshahi F., Maher J.W., et al. Nonalcoholic steatohepatitis is associated with altered hepatic microRNA expression. Hepatology 2008, 48:1810-1820.
13. Ferreira D.M.S., Simão A.L., Rodrigues C.M.P., Castro R.E. Revisiting the metabolic syndrome and paving the way for microRNAs in non-alcoholic fatty liver disease. FEBS J 2014, 281:2503-2524.
14. Pogribny I.P., Muskhelishvili L., Tryndyak V.P., Beland F.A. The tumor-promoting activity of 2-acetylaminofluorene is associated with disruption of the p53 signaling pathway and the balance between apoptosis and cell proliferation. Toxicol Appl Pharmacol 2009, 235:305-311.
15. Schmittgen T.D., Livak K.J. Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 2008, 3:1101-1108.
16. Hagan J.P., O'Neill B.L., Stewart C.L., Kozlov S.V., Croce C.M. At least ten genes define the imprinted Dlk-Dio3 cluster on mouse chromosome 12qF1. PLoS One 2009, 4:e4352.
17. Labialle S., Marty V., Bortolin-Cavaillé M.-L., Hoareau-Osman M., Pradère J.P., Valet P., et al. The miR-379/miR-410 cluster at the imprinted Dlk-Dio3 domain controls neonatal metabolic adaptation. EMBO J 2014, 33:2216-2230.
18. Liu L., Luo G.-Z., Yang W., Zhao X., Zheng Q., Lv Z., et al. Activation of the imprinted Dlk-Dio3 region correlates with pluripotency levels of mouse stem cells. J Biol Chem 2010, 285:19483-19490.
19. Benetatos L., Vartholomatos G., Hatzimichael E. DLK1-DIO3 imprinted cluster in induced pluripotency: landscape in the mist. Cell Mol Life Sci 2014, 71:4421-4430.
20. Luk J.M., Burchard J., Zhang C., Liu A.M., Wong K.F., Shek F.H., et al. DLK1-DIO3 genomic imprinted microRNA cluster at 14q32.2 defines a stemlike subtype of hepatocellular carcinoma associated with poor survival. J Biol Chem 2011, 286:30706-30713.
21. Bird T.G., Lorenzini S., Forbes S.J. Activation of stem cells in hepatic diseases. Cell Tissue Res 2008, 331:283-300.
22. Oishi N., Wang X.W. Novel therapeutic strategies for targeting liver cancer stem cells. Int J Biol Sci 2011, 7:517-535.
23. Williams M.J., Clouston A.D., Forbes S.J. Links between hepatic fibrosis, ductular reaction, and progenitor cell expansion. Gastroenterology 2014, 146:349-356.
24. Cerec V., Glaise D., Garnier D., Morosan S., Turlin B., Drenou B., et al. Transdifferentiation of hepatocyte-like cells from the human hepatoma HepaRG cell line through bipotent progenitor. Hepatology 2007, 45:957-967.
25. Gatti D.M., Lu L., Williams R.W., Sun W., Wright F.A., Threadgill D.W., et al. MicroRNA expression in the livers of inbred mice. Mutat Res 2011, 714:126-133.
26. DeLaForest A., Nagaoka M., Si-Tayeb K., Noto F.K., Konopka G., Battle M.A., et al. HNF4A is essential for specification of hepatic progenitors from human pluripotent stem cells. Development 2011, 138:4143-4153.
27. Pirola C.J., Fernández Gianotti T., Castaño G.O., Mallardi P., San Martino J., Mora Gonzalez Lopez Ledesma M., et al. Circulating microRNA signature in non-alcoholic fatty liver disease: from serum non-coding RNAs to liver histology and disease pathogenesis. Gut 2015, 64:800-812.
28. Tan Y., Ge G., Pan T., Wen D., Gan J. A pilot study of serum microRNAs panel as potential biomarkers for diagnosis of nonalcoholic fatty liver disease. PLoS One 2014, 9:e105192.
29. Machado M.V., Michelotti G.A., Xie G., de Almeida T.P., Boursier J., Bohnic B., et al. Mouse models of diet-induced nonalcoholic steatohepatitis reproduce the heterogeneity of the human disease. PLoS One 2015, 10:e0127991.
30. Hebbard L., George J. Animal models of nonalcoholic fatty liver disease. Nat Rev Gastroenterol Hepatol 2011, 8:35-44.
31. Maher J.J. New insights from rodent models of fatty liver disease. Antioxid Redox Signal 2011, 15:535-550.
32. Glen C.D., McVeigh L.E., Voutounou M., Dubrova Y.E. The effects of methyl-donor deficiency on the pattern of gene expression in mice. Mol Nutr Food Res 2015, 59:501-506.
33. Yeh M.M., Brunt E.M. Pathological features of fatty liver disease. Gastroenterology 2014, 147:754-764.
34. 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.
35. Dong X., Liu H., Chen F., Li D., Zhao Y. MiR-214 promotes the alcohol-induced oxidative stress via down-regulation of glutathione reductase and cytochrome P450 oxidoreductase in liver cells. Alcohol Clin Exp Res 2014, 38:68-77.
36. Takahashi K., Oda Y., Toyoda Y., Fukami T., Yokoi T., Nakajima M. Regulation of cytochrome b5 expression by miR-223 in human liver: effects on cytochrome P450 activities. Pharm Res 2014, 31:780-794.
37. Wang B., Majumder S., Nuovo G., Kutay H., Volinia S., Patel T., et al. Role of microRNA-155 at early stages of hepatocarcinogenesis induced by choline-deficient and amino acid-defined diet in C57BL/6 mice. Hepatology 2009, 50:1152-1161.
38. Shi C., Zhu L., Chen X., Gu N., Chen L., Zhu L., et al. IL-and TNF-α induced obesity-related inflammatory response through transcriptional regulation of miR-146b. J Interferon Cytokine Res 2014, 35:342-348.
39. Castro R.E., Ferreira D.M.S., Afonso M.B., Borralho P.M., Machado M.V., 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.
40. Takagi S., Nakajima M., Kida K., Yamaura Y., Fukami T., Yokoi T. MicroRNAs regulate human hepatocyte nuclear factor 4alpha, modulating the expression of metabolic enzymes and cell cycle. J Biol Chem 2010, 285:4415-4422.
41. Yue H.-Y., Yin C., Hou J.-L., Zeng X., Chen Y.-X., Zhong W., et al. Hepatocyte nuclear factor 4alpha attenuates hepatic fibrosis in rats. Gut 2010, 59:236-246.
42. Huang P., He Z., Ji S., Sun H., Xiang D., Liu C., et al. Induction of functional hepatocyte-like cells from mouse fibroblasts by defined factors. Nature 2011, 475:386-389.
43. Sekiya S., Suzuki A. Direct conversion of mouse fibroblasts to hepatocyte-like cells by defined factors. Nature 2011, 475:390-393.
44. Kim N., Kim H., Jung I., Kim Y., Kim D., Han Y.-M. Expression profiles of miRNAs in human embryonic stem cells during hepatocyte differentiation. Hepatol Res 2011, 41:170-183.
45. Deng X.-G., Qiu R.-L., Wu Y.-H., Li Z.-X., Xie P., Zhang J., et al. Overexpression of miR-122 promotes the hepatic differentiation and maturation of mouse ESCs through a miR-122/FoxA1/HNF4a-positive feedback loop. Liver Int 2014, 34:281-295.
46. Takayama K., Inamura M., Kawabata K., Katayama K., Higuchi M., Tashiro K., et al. Efficient generation of functional hepatocytes from human embryonic stem cells and induced pluripotent stem cells by HNF4α transduction. Mol Ther 2012, 20:127-137.
47. Richardson M.M., Jonsson J.R., Powell E.E., Brunt E.M., Neuschwander-Tetri B.A., Bhathal P.S., et al. Progressive fibrosis in nonalcoholic steatohepatitis: association with altered regeneration and a ductular reaction. Gastroenterology 2007, 133:80-90.
48. Nobili V., Carpino G., Alisi A., Franchitto A., Alpini G., De Vito R., et al. Hepatic progenitor cells activation, fibrosis, and adipokines production in pediatric nonalcoholic fatty liver disease. Hepatology 2012, 56:2142-2153.
49. Mavila N., James D., Shivakumar P., Nguyen M.V., Utley S., Mak K., et al. Expansion of prominin-1-expressing cells in association with fibrosis of biliary atresia. Hepatology 2014, 60:941-953.
50. Milosevic J., Pandit K., Magister M., Rabinovich E., Ellwanger D.C., Yu G., et al. Profibrotic role of miR-154 in pulmonary fibrosis. Am J Respir Cell Mol Biol 2012, 47:879-887.