Chronic Administration of Proanthocyanidins or Docosahexaenoic Acid Reversess the Increase of miR-33a and miR-122 in Dyslipidemic Obese Rats

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Baselga Escudero, Laura ^a   Arola Arnal, Anna ^a   Pascual Serrano, Aïda ^a   Ribas Latre, Aleix ^a   Casanova, Ester ^a   Salvadó, M Josepa ^a   Arola, Lluis ^a   Blade, Cinta ^a  

^a UNIVERSITAT ROVIRA I VIRGILI   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER A1; DOCOSAHEXAENOIC ACID; GRAPE SEED EXTRACT; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; LOW DENSITY LIPOPROTEIN CHOLESTEROL; MESSENGER RNA; MICRORNA; MICRORNA 122; MICRORNA 33A; OMEGA 3 FATTY ACID; PROANTHOCYANIDIN; STEROL REGULATORY ELEMENT BINDING PROTEIN 2; TRIACYLGLYCEROL; UNCLASSIFIED DRUG;

ABCA1 GENE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATHEROGENESIS; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; DIET SUPPLEMENTATION; DYSLIPIDEMIA; GENE; GENE EXPRESSION REGULATION; GENE TARGETING; LIPID COMPOSITION; LIVER LEVEL; LIVER PARENCHYMA; LONG TERM CARE; MALE; NONHUMAN; OBESITY; PERIPHERAL BLOOD MONONUCLEAR CELL; RAT; SREBP2 GENE; THERAPY EFFECT; TREATMENT OUTCOME; TRIACYLGLYCEROL BLOOD LEVEL;

ANIMALS; ATHEROSCLEROSIS; ATP BINDING CASSETTE TRANSPORTER 1; DIET; DOCOSAHEXAENOIC ACIDS; DYSLIPIDEMIAS; GENE EXPRESSION REGULATION; GRAPE SEED EXTRACT; LEUKOCYTES, MONONUCLEAR; LIPIDS; LIVER; MALE; MICRORNAS; OBESITY; ORGAN SIZE; PROANTHOCYANIDINS; RATS; RATS, WISTAR; RNA, MESSENGER; STEROL REGULATORY ELEMENT BINDING PROTEIN 2;

EID: 84880806221     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0069817     Document Type: Article

References (55)

1. Ambros V, (2004) The functions of animal microRNAs. Nature 431: 350-355.
2. Bartel DP, (2009) MicroRNAs: target recognition and regulatory functions. Cell 136: 215-233.
3. Breving K, Esquela-Kerscher A, (2010) The complexities of microRNA regulation: mirandering around the rules. Int J Biochem Cell Biol 42: 1316-1329.
4. Friedman RC, Farh KK, Burge CB, Bartel DP, (2009) Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 19: 92-105.
5. Rottiers V, Näär AM, (2012) MicroRNAs in metabolism and metabolic disorders. Nature Reviews Molecular Cell Biology 13: 239-250.
6. Ramírez CM, Goedeke L, Fernández-Hernando C, (2011) "Micromanaging" metabolic syndrome. Cell Cycle 10: 3249-3252.
7. Tsai WC, Hsu SD, Hsu CS, Lai TC, Chen SJ, et al. (2012) MicroRNA-122 plays a critical role in liver homeostasis and hepatocarcinogenesis. J Clin Invest 122: 2884-2897.
8. Hsu S, Wang B, Kota J, Yu J, Costinean S, et al. (2012) Essential metabolic, anti-inflammatory, and anti-tumorigenic functions of miR-122 in liver. J Clin Invest 122: 2871-2883.
9. Krutzfeldt J, Rajewsky N, Braich R, Rajeev KG, Tuschl T, et al. (2005) Silencing of microRNAs in vivo with 'antagomirs'. Nature 438: 685-689.
10. Esau C, Davis S, Murray SF, Yu XX, Pandey SK, et al. (2006) miR-122 regulation of lipid metabolism revealed by in vivo antisense targeting. Cell Metab 3: 87-98.
11. Elmén J, Lindow M, Schütz S, Lawrence M, Petri A, et al. (2008) LNA-mediated microRNA silencing in non-human primates. Nature 452: 896-899.
12. Lanford RE, Hildebrandt-Eriksen ES, Petri A, Persson R, Lindow M, et al. (2010) Therapeutic silencing of microRNA-122 in primates with chronic hepatitis C virus infection. Science 327: 198-201.
13. Moore KJ, Rayner KJ, Suarez Y, Fernandez-Hernando C, (2011) The role of microRNAs in cholesterol efflux and hepatic lipid metabolism. Annu Rev Nutr 31: 49-63.
14. Fernandez-Hernando C, Suarez Y, Rayner KJ, Moore KJ, (2011) MicroRNAs in lipid metabolism. Curr Opin Lipidol 22: 86-92.
15. Horie T, Ono K, Horiguchi M, Nishi H, Nakamura T, et al. (2010) MicroRNA-33 encoded by an intron of sterol regulatory element-binding protein 2 (Srebp2) regulates HDL in vivo. Proc Natl Acad Sci U S A 107: 17321-17326.
16. Raghow R, Yellaturu C, Deng X, Park EA, Elam MB, (2008) SREBPs: the crossroads of physiological and pathological lipid homeostasis. Trends Endocrinol Metab 19: 65-73.
17. Rayner KJ, Sheedy FJ, Esau CC, Hussain FN, Temel RE, et al. (2011) Antagonism of miR-33 in mice promotes reverse cholesterol transport and regression of atherosclerosis. J Clin Invest 121: 2921-2931.
18. Najafi-Shoushtari SH, Kristo F, Li Y, Shioda T, Cohen DE, et al. (2010) MicroRNA-33 and the SREBP host genes cooperate to control cholesterol homeostasis. Science 328: 1566-1569.
19. Rayner KJ, Esau CC, Hussain FN, McDaniel AL, Marshall SM, et al. (2011) Inhibition of miR-33a/b in non-human primates raises plasma HDL and lowers VLDL triglycerides. Nature 478: 404-407.
20. Cannon CP, (2008) Mixed dyslipidemia, metabolic syndrome, diabetes mellitus, and cardiovascular disease: clinical implications. Am J Cardiol 102: 5L-9L.
21. Popkin BM, Adair LS, Ng SW, (2012) Global nutrition transition and the pandemic of obesity in developing countries. Nutr Rev 70: 3-21.
22. Gerber PA, Gouni-Berthold I, Berneis K, (2013) Omega-3 Fatty Acids: Role on Metabolism and Cardiovascular Disease. Curr Pharm (Epub ahead of print).
23. Blade C, Arola L, Salvado MJ, (2010) Hypolipidemic effects of proanthocyanidins and their underlying biochemical and molecular mechanisms. Mol Nutr Food Res 54: 37-59.
24. Del Bas JM, Fernandez-Larrea J, Blay M, Ardevol A, Salvado MJ, et al. (2005) Grape seed procyanidins improve atherosclerotic risk index and induce liver CYP7A1 and SHP expression in healthy rats. FASEB J 19: 479-481.
25. Quesada H, del Bas JM, Pajuelo D, Diaz S, Fernandez-Larrea J, et al. (2009) Grape seed proanthocyanidins correct dyslipidemia associated with a high-fat diet in rats and repress genes controlling lipogenesis and VLDL assembling in liver. Int J Obes (Lond) 33: 1007-1012.
26. Danaei G, Ding EL, Mozaffarian D, Taylor B, Rehm J, et al. (2009) The preventable causes of death in the United States: comparative risk assessment of dietary, lifestyle, and metabolic risk factors. PLoS Med 6: e1000058.
27. Bays HE, (2007) Safety considerations with omega-3 fatty acid therapy. Am J Cardiol 99: S35-S43.
28. Rustan AC, Christiansen EN, Drevon CA, (1992) Serum lipids, hepatic glycerolipid metabolism and peroxisomal fatty acid oxidation in rats fed omega-3 and omega-6 fatty acids. Biochem J 283: 333-339.
29. Ruzickova J, Rossmeisl M, Prazak T, Flachs P, Sponarova J, et al. (2004) Omega-3 PUFA of marine origin limit diet-induced obesity in mice by reducing cellularity of adipose tissue. Lipids 39: 1177-1185.
30. Davidson LA, Wang N, Shah MS, Lupton JR, Ivanov I, et al. (2009) n-3 Polyunsaturated fatty acids modulate carcinogen-directed non-coding microRNA signatures in rat colon. Carcinogenesis 30: 2077-2084.
31. Vinciguerra M, Sgroi A, Veyrat Durebex C, Rubbia Brandt L, Buhler LH, et al. (2009) Unsaturated fatty acids inhibit the expression of tumor suppressor phosphatase and tensin homolog (PTEN) via microRNA- 21 up- regulation in hepatocytes. Hepatology 49: 1176-1184.
32. Faragó N, Fehér LZ, Kitajka K, Das UN, Puskás LG, (2011) MicroRNA profile of polyunsaturated fatty acid treated glioma cells reveal apoptosis-specific expression changes. Lipids Health Dis 10: 173.
33. Bladé C, Baselga-Escudero L, Salvadó MJ, Arola-Arnal A, (2012) miRNAs, polyphenols, and chronic disease. Mol Nutr Food Res 57: 58-70.
34. Baselga-Escudero L, Blade C, Ribas-Latre A, Casanova E, Salvado MJ, et al. (2012) Grape seed proanthocyanidins repress the hepatic lipid regulators miR-33 and miR-122 in rats. Mol Nutr Food Res 56: 1636-1646.
35. Bouwens M, Afman LA, Muller M, (2008) Activation of peroxisome proliferator-activated receptor alpha in human peripheral blood mononuclear cells reveals an individual gene expression profile response. BMC Genomics 9: 262-2164-9-262.
36. Bouwens M, Afman LA, Muller M, (2007) Fasting induces changes in peripheral blood mononuclear cell gene expression profiles related to increases in fatty acid beta-oxidation: functional role of peroxisome proliferator activated receptor alpha in human peripheral blood mononuclear cells. Am J Clin Nutr 86: 1515-1523.
37. Serra A, Macià A, Romero MP, Valls J, Bladé C, et al. (2010) Bioavailability of procyanidin dimers and trimers and matrix food effects in in vitro and in vivo models. Br J Nutr 103: 944-52.
38. Rayner KJ, Suarez Y, Davalos A, Parathath S, Fitzgerald ML, et al. (2010) MiR-33 contributes to the regulation of cholesterol homeostasis. Science 328: 1570-1573.
39. Gerin I, Clerbaux LA, Haumont O, Lanthier N, Das AK, et al. (2010) Expression of miR-33 from an SREBP2 intron inhibits cholesterol export and fatty acid oxidation. J Biol Chem 285: 33652-33661.
40. Horie T, Ono K, Horiguchi M, Nishi H, Nakamura T, et al. (2010) MicroRNA-33 encoded by an intron of sterol regulatory element-binding protein 2 (Srebp2) regulates HDL in vivo. Proc Natl Acad Sci U S A 107: 17321-17326.
41. Sampey BP, Vanhoose AM, Winfield HM, Freemerman AJ, Muehlbauer MJ, et al. (2011) Cafeteria diet is a robust model of human metabolic syndrome with liver and adipose inflammation: comparison to high-fat diet. Obesity 9: 1109-1117.
42. Wu N, Sarna LK, Hwang SY, Zhu Q, Wang P, et al. (2013) Activation of 3-hydroxy-3-methylglutaryl coenzyme A (HMG-CoA) reductase during high fat diet feeding. Biochim Biophys Acta. doi: 10.1016/j.bbadis.2013.04.024. [In press].
43. Caballero F, Fernandez A, De Lacy AM, Fernandez-Checa JC, Caballeria J, et al. (2009) Enhanced free cholesterol, SREBP-2 and StAR expression in human NASH. J Hepatol 50: 789-796.
44. Gao W, He HW, Wang ZM, Zhao H, Lian XQ, et al. (2012) Plasma levels of lipometabolism-related miR-122 and miR-370 are increased in patients with hyperlipidemia and associated with coronary artery disease. Lipids Health Dis 11: 55-511X-11-55.
45. Yang YM, Seo SY, Kim TH, Kim SG, (2012) Decrease of microRNA-122 causes hepatic insulin resistance by inducing protein tyrosine phosphatase 1B, which is reversed by licorice flavonoid. Hepatology 56: 2209-2220.
46. Alisi A, Da Sacco L, Bruscalupi G, Piemonte F, Panera N, et al. (2011) Mirnome analysis reveals novel molecular determinants in the pathogenesis of diet-induced nonalcoholic fatty liver disease. Lab Invest 91: 283-293.
47. Li S, Chen X, Zhang H, Liang X, Xiang Y, et al. (2009) Differential expression of microRNAs in mouse liver under aberrant energy metabolic status. J Lipid Res 50: 1756-1765.
48. Joven J, Espinel E, Rull A, Aragonès G, Rodríguez-Gallego E, et al. (2012) Plant-derived polyphenols regulate expression of miRNA paralogs miR-103/107 and miR-122 and prevent diet-induced fatty liver disease in hyperlipidemic mice. Biochim Biophys Acta 1820: 894-9.
49. Gatfield D, Le Martelot G, Vejnar CE, Gerlach D, Schaad O, et al. (2009) Integration of microRNA miR-122 in hepatic circadian gene expression. Genes Dev 23: 1313-1326.
50. Pallares V, Calay D, Cedo L, Castell-Auvi A, Raes M, et al. (2012) Additive, antagonistic, and synergistic effects of procyanidins and polyunsaturated fatty acids over inflammation in RAW 264.7 macrophages activated by lipopolysaccharide. Nutrition 28: 447-457.
51. Millan J, Pinto X, Munoz A, Zuniga M, Rubies-Prat J, et al. (2009) Lipoprotein ratios: Physiological significance and clinical usefulness in cardiovascular prevention. Vasc Health Risk Manag 5: 757-765.
52. Oliveira C, Coelho A, Barbeiro H, Lima V, Soriano F, et al. (2006) Liver mitochondrial dysfunction and oxidative stress in the pathogenesis of experimental nonalcoholic fatty liver disease. Braz J Med Biol Res 39: 189-194.
53. Fernández-Hernando C, Moore KJ, (2011) MicroRNA modulation of cholesterol homeostasis. Arterioscler Thromb Vasc Biol 31: 2378-2382.
54. Lewis AP, opling CL, (2010) Regulation and biological function of the liver-specific miR-122. Biochem Soc Trans 38: 1553-1557.
55. Horton JD, Goldstein JL, Brown MS, (2002) SREBPs: activators of the complete program of cholesterol and fatty acid synthesis in the liver. J Clin Invest 109: 1125-1132.