The role of epigenetics in the progression of non-alcoholic fatty liver disease

Mini-Reviews in Medicinal Chemistry

Volumn 15, Issue 14, 2015, Pages 1187-1194

  Aguilar Olivos, Nancy Edith ^a   Oria Hernández, Jesús ^b   Ponciano Rodríguez, Guadalupe ^c   Chávez Tapia, Norberto Carlos ^a   Uribe, Misael ^a   Méndez Sánchez, Nahum ^a  

^a LIVER RESEARCH UNIT   (Mexico)

^b INSTITUTO NACIONAL DE PEDIATRÍA   (Mexico)

^c UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

Author keywords

Biological markers; Disease progression; DNA methylation; Histones; Liver; MicroRNAs; One carbon metabolism

Indexed keywords

HISTONE DEACETYLASE 3; METHIONINE; MICRORNA; SIRTUIN 1;

ARTICLE; BARIATRIC SURGERY; CARBON METABOLISM; DEACETYLATION; DISEASE COURSE; DNA METHYLATION; EPIGENETICS; GENOTYPE; HISTONE ACETYLATION; HISTONE MODIFICATION; HUMAN; INFLAMMATION; NONALCOHOLIC FATTY LIVER; NONHUMAN; POLYMERASE CHAIN REACTION; RESTRICTION FRAGMENT LENGTH POLYMORPHISM; ANIMAL; GENETIC EPIGENESIS; GENETICS; PATHOLOGY;

ANIMALS; DISEASE PROGRESSION; DNA METHYLATION; EPIGENESIS, GENETIC; HUMANS; NON-ALCOHOLIC FATTY LIVER DISEASE;

EID: 84945948164     PISSN: 13895575     EISSN: 18755607     Source Type: Journal    
DOI: 10.2174/1389557515666150709115702     Document Type: Article

References (54)

1. Mendez-Sanchez, N.; Arrese, M.; Zamora-Valdes, D.; Uribe, M. Current concepts in the pathogenesis of nonalcoholic fatty liver disease. Liver. Int., 2007, 27(4), 423-433.
2. Chalasani, N.; Younossi, Z.; Lavine, J. E.; Diehl, A. M.; Brunt, E. M.; Cusi, K.; Charlton, M.; Sanyal, A. J. The diagnosis and management of non-alcoholic fatty liver disease: practice Guideline by the American Association for the Study of Liver Diseases, American College of Gastroenterology, and the American Gastroenterological Association. Hepatology, 2012, 55(6), 2005- 2023.
3. Michelotti, G. A.; Machado, M. V.; Diehl, A. M. NAFLD, NASH and liver cancer. Nat. Rev. Gastroenterol. Hepatol., 2013, 10(11), 656-665.
4. Clark, J. M.; Brancati, F. L.; Diehl, A. M. The prevalence and etiology of elevated aminotransferase levels in the United States. Am. J. Gastroenterol., 2003, 98(5), 960-967.
5. Cohen, J. C.; Horton, J. D.; Hobbs, H. H. Human fatty liver disease: old questions and new insights. Science, 2011, 332(6037), 1519-23.
6. Vernon, G.; Baranova, A.; Younossi, Z. M. Systematic review: the epidemiology and natural history of non-alcoholic fatty liver disease and non-alcoholic steatohepatitis in adults. Aliment. Pharmacol. Ther., 2011, 34(3), 274-85.
7. Lopez-Velazquez, J. A.; Silva-Vidal, K. V.; Ponciano-Rodriguez, G.; Chavez-Tapia, N. C.; Arrese, M.; Uribe, M.; Mendez-Sanchez, N., The prevalence of nonalcoholic fatty liver disease in the Americas. Ann. Hepatol., 2014, 13(2), 166-78.
8. Campion, J.; Milagro, F.; Martinez, J. A. Epigenetics and obesity. Prog. Mol. Biol. Transl. Sci., 2010, 94, 291-347.
9. Li, Y. Y. Genetic and epigenetic variants influencing the development of nonalcoholic fatty liver disease. World. J. Gastroenterol., 2012, 18(45), 6546-51.
10. Riddihough, G.; Zahn, L. M. Epigenetics. What is epigenetics? Introduction. Science, 2010, 330(6004), 611.
11. Martinez, J. A.; Milagro, F. I.; Claycombe, K. J.; Schalinske, K. L. Epigenetics in adipose tissue, obesity, weight loss, and diabetes. Adv. Nutr., 2014, 5(1), 71-81.
12. Kaelin, W. G., Jr.; McKnight, S. L. Influence of metabolism on epigenetics and disease. Cell, 2013, 153(1), 56-69.
13. Liyanage, V.R.; Jarmasz, J.S.; Murugeshan, N.; Del Bigio, M.R.; Rastegar, M.; Davie, J. R. DNA modifications: function and applications in normal and disease States. Biology, 2014, 3(4), 670- 723.
14. Thurman, R. E.; Rynes, E.; Humbert, R.; Vierstra, J.; Maurano, M. T.; Haugen, E.; Sheffield, N. C.; Stergachis, A. B.; Wang, H.; Vernot, B.; Garg, K.; John, S.; Sandstrom, R.; Bates, D.; Boatman, L.; Canfield, T. K.; Diegel, M.; Dunn, D.; Ebersol, A. K.; Frum, T.; Giste, E.; Johnson, A. K.; Johnson, E. M.; Kutyavin, T.; Lajoie, B.; Lee, B. K.; Lee, K.; London, D.; Lotakis, D.; Neph, S.; Neri, F.; Nguyen, E. D.; Qu, H.; Reynolds, A. P.; Roach, V.; Safi, A.; Sanchez, M. E.; Sanyal, A.; Shafer, A.; Simon, J. M.; Song, L.; Vong, S.; Weaver, M.; Yan, Y.; Zhang, Z.; Zhang, Z.; Lenhard, B.; Tewari, M.; Dorschner, M. O.; Hansen, R. S.; Navas, P. A.; Stamatoyannopoulos, G.; Iyer, V. R.; Lieb, J. D.; Sunyaev, S. R.; Akey, J. M.; Sabo, P. J.; Kaul, R.; Furey, T. S.; Dekker, J.; Crawford, G. E.; Stamatoyannopoulos, J. A. The accessible chromatin landscape of the human genome. Nature, 2012, 489(7414), 75-82.
15. Sookoian, S.; Rosselli, M. S.; Gemma, C.; Burgueno, A. L.; Fernandez Gianotti, T.; Castano, G. O.; Pirola, C. J. Epigenetic regulation of insulin resistance in nonalcoholic fatty liver disease: impact of liver methylation of the peroxisome proliferator-activated receptor gamma coactivator 1alpha promoter. Hepatology, 2010, 52(6), 1992-2000.
16. Pirola, C. J.; Gianotti, T. F.; Burgueno, A. L.; Rey-Funes, M.; Loidl, C. F.; Mallardi, P.; Martino, J. S.; Castano, G. O.; Sookoian, S. Epigenetic modification of liver mitochondrial DNA is associated with histological severity of nonalcoholic fatty liver disease. Gut, 2013, 62(9), 1356-63.
17. Fosslien, E. Mitochondrial medicine--molecular pathology of defective oxidative phosphorylation. Ann. Clin. Lab. Sci., 2001, 31(1), 25-67.
18. Murphy, S. K.; Yang, H.; Moylan, C. A.; Pang, H.; Dellinger, A.; Abdelmalek, M. F.; Garrett, M. E.; Ashley-Koch, A.; Suzuki, A.; Tillmann, H. L.; Hauser, M. A.; Diehl, A. M. Relationship between methylome and transcriptome in patients with nonalcoholic fatty liver disease. Gastroenterology, 2013, 145(5), 1076-87.
19. Ahrens, M.; Ammerpohl, O.; von Schonfels, W.; Kolarova, J.; Bens, S.; Itzel, T.; Teufel, A.; Herrmann, A.; Brosch, M.; Hinrichsen, H.; Erhart, W.; Egberts, J.; Sipos, B.; Schreiber, S.; Hasler, R.; Stickel, F.; Becker, T.; Krawczak, M.; Rocken, C.; Siebert, R.; Schafmayer, C.; Hampe, J. DNA methylation analysis in nonalcoholic fatty liver disease suggests distinct disease-specific and remodeling signatures after bariatric surgery. Cell. Metab., 2013, 18(2), 296-302.
20. Chypre, M.I; Zaidi, N.; Smans K. ATP-citrate lyase: a minireview. Biochem. Biophys. Res. Commun., 2012, 422(1), 1-4.
21. Wang, Q.I.; Jiang, L.; Wang, J.; Li, S.; Yu, Y.; You, J.; Zeng, R.; Gao, X.; Rui, L.; Li, W.; Liu, Y. Abrogation of hepatic ATP-citrate lyase protects against fatty liver and ameliorates hyperglycemia in leptin receptor-deficient mice. Hepatology, 2009, 49(4), 1166-75.
22. Heald, A.H.I.; Kaushal, K.; Siddals, K.W.; Rudenski, A.S.; Anderson, S.G.; Gibson, J.M. Insulin-like growth factor binding protein-2 (IGFBP-2) is a marker for the metabolic syndrome. Exp. Clin. Endocrinol. Diabetes, 2006, 114(7), 371-6.
23. Sumida, Y.I.; Yonei, Y.; Tanaka, S.; Mori, K.; Kanemasa, K.; Imai, S.; Taketani, H,; Hara, T.; Seko, Y.; Ishiba, H.; Okajima, A.; Yamaguchi, K.; Moriguchi, M.; Mitsuyoshi, H.; Yasui, K.; Minami, M.; Itoh, Y. Lower levels of insulin-like growth factor-1 standard deviation score are associated with histological severity of non-alcoholic fatty liver disease. Hepatol. Res., 2014, DOI: 10.1111/hepr.12408
24. Jornayvaz, F.R.I.; Shulman, G.I. Diacylglycerol activation of protein kinase Cε and hepatic insulin resistance. Cell Metab., 2012, 15(5), 574-84.
25. Sazci, A.I.; Ozel, M.D.; Ergul, E.; Aygun, C. Association of nicotinamide-N-methyltransferase gene rs694539 variant with patients with nonalcoholic steatohepatitis. Genet. Test. Mol. Biomarkers, 2013, 17(11), 849-53.
26. Sazci, A.I.; Ergul, E.; Aygun, C.; Akpinar, G.; Senturk, O.; Hulagu, S. Methylenetetrahydrofolate reductase gene polymorphisms in patients with nonalcoholic steatohepatitis (NASH). Cell Biochem. Funct., 2008, 26(3), 291-6.
27. Cuomo, R.I.; Dattilo, M.; Pumpo, R.; Capuano, G.; Boselli, L.; Budillon, G. Nicotinamide methylation in patients with cirrhosis. J. Hepatol., 1994, 20(1), 138-42.
28. Kim, J.I.; Hong, S.J.; Lim, E.K.; Yu, Y.S.; Kim, S.W.; Roh, J.H.; Do, I.G.; Joh, J.W.; Kim, D.S. Expression of nicotinamide Nmethyltransferase in hepatocellular carcinoma is associated with poor prognosis. J. Exp. Clin. Cancer Res., 2009, 28,20.
29. Sazci, A.I.; Ozel, M.D.; Ergul, E.; Aygun, C. Association of nicotinamide-N-methyltransferase gene rs694539 variant with patients with nonalcoholic steatohepatitis. Genet. Test. Mol. Biomarkers, 2013, 17(11), 849-53.
30. Chen, G.I.; Broseus, J.; Hergalant, S.; Donnart, A.; Chevalier, C.; Bolanos-Jimenez, F.; Gueant, J.L.; Houlgatte, R. Identification of master genes involved in liver key functions through transcriptomics and epigenomics of methyl donor deficiency in rat: relevance to nonalcoholic liver disease. Mol. Nutr. Food Res., 2015, 59(2), 293-302.
31. Dahlhoff, C.; Worsch, S.; Sailer, M.; Hummel, B.A.; Fiamoncini, J.; Uebel, K.; Obeid, R.; Scherling, C; Geisel, J.; Bader, B.L.; Daniel, H. Methyl-donor supplementation in obese mice prevents the progression of NAFLD, activates AMPK and decreases acylcarnitine levels. Mol. Metab., 2014, 3(5), 565-80.
32. Turner, B. M. Histone acetylation as an epigenetic determinant of long-term transcriptional competence. Cell. Mol. Life Sci., 1998, 54(1), 21-31.
33. Berger, S. L. The complex language of chromatin regulation during transcription. Nature, 2007, 447(7143), 407-12.
34. Purushotham, A.; Schug, T. T.; Xu, Q.; Surapureddi, S.; Guo, X.; Li, X. Hepatocyte-specific deletion of SIRT1 alters fatty acid metabolism and results in hepatic steatosis and inflammation. Cell. Metab., 2009, 9(4), 327-38.
35. Blander, G.; Guarente, L. The Sir2 family of protein deacetylases. Annu. Rev. Biochem., 2004, 73, 417-35.
36. Pfluger, P. T.; Herranz, D.; Velasco-Miguel, S.; Serrano, M.; Tschop, M. H. Sirt1 protects against high-fat diet-induced metabolic damage. Proc. Natl. Acad. Sci. U. S. A., 2008, 105(28), 9793-8.
37. Cao, Y.; Xue, Y.; Xue, L.; Jiang, X.; Wang, X.; Zhang, Z.; Yang, J.; Lu, J.; Zhang, C.; Wang, W.; Ning, G. Hepatic menin recruits SIRT1 to control liver steatosis through histone deacetylation. J. hepatol., 2013, 59(6), 1299-306.
38. Escande, C.; Chini, C. C.; Nin, V.; Dykhouse, K. M.; Novak, C. M.; Levine, J.; van Deursen, J.; Gores, G. J.; Chen, J.; Lou, Z.; Chini, E. N. Deleted in breast cancer-1 regulates SIRT1 activity and contributes to high-fat diet-induced liver steatosis in mice. J. Clin. Invest., 2010, 120(2), 545-58.
39. Kim, H. S.; Xiao, C.; Wang, R. H.; Lahusen, T.; Xu, X.; Vassilopoulos, A.; Vazquez-Ortiz, G.; Jeong, W. I.; Park, O.; Ki, S. H.; Gao, B.; Deng, C. X. Hepatic-specific disruption of SIRT6 in mice results in fatty liver formation due to enhanced glycolysis and triglyceride synthesis. Cell. Metab., 2010, 12(3), 224-36.
40. Colak, Y.; Ozturk, O.; Senates, E.; Tuncer, I.; Yorulmaz, E.; Adali, G.; Doganay, L.; Enc, F. Y. SIRT1 as a potential therapeutic target for treatment of nonalcoholic fatty liver disease. Med. Sci. Monit., 2011, 17(5), HY5-9.
41. Colak, Y.; Yesil, A.; Mutlu, H. H.; Caklili, O. T.; Ulasoglu, C.; Senates, E.; Takir, M.; Kostek, O.; Yilmaz, Y.; Yilmaz Enc, F.; Tasan, G.; Tuncer, I. A potential treatment of non-alcoholic fatty liver disease with SIRT1 activators. J. Gastrointestin. Liver. Dis., 2014, 23(3), 311-9.
42. Feng, D.; Liu, T.; Sun, Z.; Bugge, A.; Mullican, S. E.; Alenghat, T.; Liu, X. S.; Lazar, M. A. A circadian rhythm orchestrated by histone deacetylase 3 controls hepatic lipid metabolism. Science, 2011, 331(6022), 1315-9.
43. Sun, Z.; Miller, R. A.; Patel, R. T.; Chen, J.; Dhir, R.; Wang, H.; Zhang, D.; Graham, M. J.; Unterman, T. G.; Shulman, G. I.; Sztalryd, C.; Bennett, M. J.; Ahima, R. S.; Birnbaum, M. J.; Lazar, M. A. Hepatic Hdac3 promotes gluconeogenesis by repressing lipid synthesis and sequestration. Nat. Med., 2012, 18(6), 934-42.
44. Bricambert, J.; Miranda, J.; Benhamed, F.; Girard, J.; Postic, C.; Dentin, R. Salt-inducible kinase 2 links transcriptional coactivator p300 phosphorylation to the prevention of ChREBP-dependent hepatic steatosis in mice. J. Clin. Invest., 2010, 120(12), 4316-31.
45. Dentin, R.; Benhamed, F.; Hainault, I.; Fauveau, V.; Foufelle, F.; Dyck, J. R.; Girard, J.; Postic, C. Liver-specific inhibition of ChREBP improves hepatic steatosis and insulin resistance in ob/ob mice. Diabetes, 2006, 55(8), 2159-70.
46. Rottiers, V.; Naar, A. M. MicroRNAs in metabolism and metabolic disorders. Nat. Rev. Mol. Cell. Biol., 2012, 13(4), 239-50.
47. Lewis, B. P.; Shih, I. H.; Jones-Rhoades, M. W.; Bartel, D. P.; Burge, C. B. Prediction of mammalian microRNA targets. Cell, 2003, 115(7), 787-98.
48. Lynn, F. C. Meta-regulation: microRNA regulation of glucose and lipid metabolism. Trends. Endocrinol. Metab., 2009, 20(9), 452-9.
49. Pirola, C. J.; Fernandez Gianotti, T.; Castano, G. O.; Mallardi, P.; San Martino, J.; Mora Gonzalez Lopez Ledesma, M.; Flichman, D.; Mirshahi, F.; Sanyal, A. J.; Sookoian, S. Circulating microRNA signature in non-alcoholic fatty liver disease: from serum noncoding RNAs to liver histology and disease pathogenesis. Gut, 2014, doi: 10.1136/gutjnl-2014-306996.
50. Celikbilek, M.; Baskol, M.; Taheri, S.; Deniz, K.; Dogan, S.; Zararsiz, G.; Gursoy, S.; Guven, K.; Ozbakir, O.; Dundar, M.; Yucesoy, M. Circulating microRNAs in patients with non-alcoholic fatty liver disease. World J. Hepatol., 2014, 6(8), 613-20.
51. Ortega, F. J.; Mercader, J. M.; Moreno-Navarrete, J. M.; Rovira, O.; Guerra, E.; Esteve, E.; Xifra, G.; Martinez, C.; Ricart, W.; Rieusset, J.; Rome, S.; Karczewska-Kupczewska, M.; Straczkowski, M.; Fernandez-Real, J. M. Profiling of circulating microRNAs reveals common microRNAs linked to type 2 diabetes that change with insulin sensitization. Diabetes Care, 2014, 37(5), 1375-83.
52. Lee, J. H.; Friso, S.; Choi, S. W. Epigenetic mechanisms underlying the link between non- alcoholic fatty liver diseases and nutrition. Nutrients, 2014, 6(8), 3303-25.
53. Lakner, A. M.; Bonkovsky, H. L.; Schrum, L. W., microRNAs: fad or future of liver disease. World J. Gastroenterol., 2011, 17(20), 2536-42.
54. Cheung, O.; Puri, P.; Eicken, C.; Contos, M. J.; Mirshahi, F.; Maher, J. W.; Kellum, J. M.; Min, H.; Luketic, V. A.; Sanyal, A. J. Nonalcoholic steatohepatitis is associated with altered hepatic MicroRNA expression. Hepatology, 2008, 48(6), 1810-20.