Alpha-lipoic acid improves high-fat diet-induced hepatic steatosis by modulating the transcription factors SREBP-1, FoxO1 and Nrf2 via the SIRT1/LKB1/AMPK pathway

Journal of Nutritional Biochemistry

Volumn 25, Issue 11, 2014, Pages 1207-1217

  Yang, Yi ^a,b   Li, Wang ^b   Liu, Yang ^b   Sun, Yuning ^b   Li, Yan ^b   Yao, Qing ^b   Li, Jianning ^b   Zhang, Qian ^b   Gao, Yujing ^b   Gao, Ling ^a   Zhao, Jiajun ^a,c  

^a SHANDONG PROVINCIAL HOSPITAL AFFILIATED TO SHANDONG UNIVERSITY   (China)

^b NINGXIA MEDICAL UNIVERSITY   (China)

^c Shandong Academy of Clinical Medicine   (China)

Author keywords

Alpha lipoic acid; FoxO1; Nonalcoholic fatty liver disease; Nrf2; SIRT1; SREBP 1

Indexed keywords

FATTY ACID SYNTHASE; GLUCOSE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; LIVER TRIACYLGLYCEROL LIPASE; PALMITIC ACID; PROTEIN KINASE LKB1; SIRTUIN 1; STEROL REGULATORY ELEMENT BINDING PROTEIN 1; THIOCTIC ACID; TRANSCRIPTION FACTOR FKHR; TRANSCRIPTION FACTOR NRF2; TRIACYLGLYCEROL; ADENYLATE KINASE; PROTEIN SERINE THREONINE KINASE; SIRT1 PROTEIN, MOUSE; STK11 PROTEIN, MOUSE; TRANSCRIPTION FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; CYTOPLASM; DEACETYLATION; DIET SUPPLEMENTATION; ENDOPLASMIC RETICULUM MEMBRANE; ENZYME PHOSPHORYLATION; EXPERIMENTAL DIGESTIVE SYSTEM DISEASE; GLUCOSE BLOOD LEVEL; HEPG2 CELL LINE; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; LIPID DIET; LIPID METABOLISM; MALE; MOUSE; NONALCOHOLIC FATTY LIVER; NONHUMAN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; TRIACYLGLYCEROL BLOOD LEVEL; WESTERN BLOTTING; ANIMAL; C57BL MOUSE; DRUG EFFECTS; FATTY LIVER; METABOLISM;

ADENYLATE KINASE; ANIMALS; DIET, HIGH-FAT; FATTY LIVER; MALE; MICE; MICE, INBRED C57BL; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION; SIRTUIN 1; THIOCTIC ACID; TRANSCRIPTION FACTORS;

EID: 84908223860     PISSN: 09552863     EISSN: 18734847     Source Type: Journal    
DOI: 10.1016/j.jnutbio.2014.06.001     Document Type: Article

References (42)

1. Chitturi S, Farrell GC, Hashimoto E, Saibara T, Lau GK, Sollano JD, et al. Non-alcoholic fatty liver disease in the Asia-Pacific region: definitions and overview of proposed guidelines. J Gastroenterol Hepatol 2007, 22:778-787.
2. Petta S., Muratore C., Craxi A. Non-alcoholic fatty liver disease pathogenesis: the present and the future. Dig Liver Dis 2009, 41:615-625.
3. Hou X, Xu S, Maitland-Toolan KA, Sato K, Jiang B, Ido Y, et al. SIRT1 regulates hepatocyte lipid metabolism through activating AMP-activated protein kinase. J Biol Chem 2008, 283:20015-20026.
4. Xie M, Zhang D, Dyck JR, Li Y, Zhang H, Morishima M, et al. A pivotal role for endogenous TGF-β-activated kinase-1 in the LKB1/AMP-activated protein kinase energy-sensor pathway. Proc Natl Acad Sci U S A 2006, 103:17378-17383.
5. Canto C., Auwerx J. PGC-1alpha, SIRT1 and AMPK, an energy sensing network that controls energy expenditure. Curr Opin Lipidol 2009, 20:98-105.
6. 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, 9:327-338.
7. + metabolism and SIRT1 activity. Nature 2009, 458:1056-1060.
8. Daemen S., Kutmon M., Evelo C.T. A pathway approach to investigate the function and regulation of SREBPs. Genes Nutr 2013, 8:289-300.
9. Sumida Y., Niki E., Naito Y., Yoshikawa T. Involvement of free radicals and oxidative stress in NAFLD/NASH. Free Radic Res 2013, 47:869-880.
10. Oliveira C.P., Da Costa Gayotto L.C., Tatai C., Della Bina BI., Janiszewski M., Lima ES., et al. Oxidative stress in the pathogenesis of nonalcoholic fatty liver disease, in rats fed with a choline deficient diet. J Cell Mol Med 2002, 6:399-406.
11. Kensler T.W., Wakabayashi N., Biswal S. Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway. Annu Rev Pharmacol Toxicol 2007, 47:89-116.
12. Xu W., Shao L., Zhou C., Wang H., Guo J. Upregulation of Nrf2 expression in non-alcoholic fatty liver and steatohepatitis. Hepato-Gastroenterology 2011, 58:2077-2080.
13. Li Y., Xu W., McBurney MW, Longo VD SIRT1 inhibition reduces IGF-I/IRS-2/Ras/ERK1/2 signaling and protects neurons. Cell Metab 2008, 8:38-48.
14. Huang K., Huang J., Xie X., Wang S., Chen C., Shen X., et al. Sirt1 resists advanced glycation end product-induced expressions of fibronectin and TGF-β1 by activating the Nrf2/ARE pathway in glomerular mesangial cells. Free Radic Biol Med 2013, 65:528-540.
15. Valdecantos M.P., Pérez-Matute P., González-Muniesa P., Prieto-Hontoria PL., Moreno-Aliaga MJ., Martínez JA. Lipoic acid improves mitochondrial function in nonalcoholic steatosis through the stimulation of sirtuin 1 and sirtuin 3. Obesity 2012, 20:1974-1983.
16. Castro M.C., Massa M.L., Schinella G., Gagliardino JJ., Francini F. Lipoic acid prevents liver metabolic changes induced by administration of a fructose-rich diet. Biochim Biophys Acta 1830, 2013:2226-2232.
17. Chen W.L., Kang C.H., Wang SG., Lee HM. α-Lipoic acid regulates lipid metabolism through induction of sirtuin 1 (SIRT1) and activation of AMP-activated protein kinase. Diabetologia 2012, 55:1824-1835.
18. Golbidi S., Badran M., Laher I. Diabetes and alpha lipoic Acid. Front Pharmacol 2011, 2:1-15.
19. Park K.G., Min A.K., Koh EH., Kim HS., Kim MO., Park HS., et al. Alpha-lipoic acid decreases hepatic lipogenesis through adenosine monophosphate-activated protein kinase (AMPK)-dependent and AMPK-independent pathways. Hepatology 2008, 48:1477-1486.
20. Kaya-Dagistanli F., Tanriverdi G., Altinok A., Ozyazgan S., Ozturk M. The effects of alpha lipoic acid on liver cells damages and apoptosis induced by polyunsaturated fatty acids. Food Chem Toxicol 2013, 53:84-93.
21. Kuo Y.T., Lin T.H., Chen WL., Lee HM. Alpha-lipoic acid induces adipose triglyceride lipase expression and decreases intracellular lipid accumulation in HepG2 cells. Eur J Pharmacol 2012, 692:10-18.
22. Serviddio G., Bellanti F., Vendemiale G. Free radical biology for medicine: learning from nonalcoholic fatty liver disease. Free Radic Biol Med 2013, 65:952-968.
23. Sekiya M., Yahagi N., Matsuzaka T., Takeuchi Y., Nakagawa Y., Takahashi H., et al. SREBP-1-independent regulation of lipogenic gene expression in adipocytes. J Lipid Res 2007, 48:1581-1591.
24. Choi Y., Yanagawa Y., Kim S., Park T. Involvement of SIRT1-AMPK signaling in the protective action of indole-3-carbinol against hepatic steatosis in mice fed a high-fat diet. J Nutr Biochem 2013, 24:1393-1400.
25. Burnett C., Valentini S., Cabreiro F., Goss M., Somogyvári M., Piper MD., et al. Absence of effects of Sirt2 overexpression on lifespan in C. elegans and Drosophila. Nature 2011, 477:482-485.
26. Shackelford D.B., Shaw R.J. The LKB1-AMPK pathway: metabolism and growth control in tumour suppression. Nat Rev Cancer 2009, 9:563-575.
27. Zheng Z., Chen H., Li J., Li T., Zheng B., Zheng Y., et al. Sirtuin 1-mediated cellular metabolic memory of high glucose via the LKB1/AMPK/ROS pathway and therapeutic effects of metformin. Diabetes 2012, 61:217-228.
28. Feige J.N., Lagouge M., Canto C., Strehle A., Houten SM., Milne JC., et al. Specific SIRT1 activation mimics low energy levels and protects against diet-induced metabolic disorders by enhancing fat oxidation. Cell Metab 2008, 8:347-358.
29. Chakrabarti P., English T., Karki S., Qiang L., Tao R., Kim J., et al. SIRT1 controls lipolysis in adipocytes via FoxO1-mediated expression of ATGL. J Lipid Res 2011, 52:1693-1701.
30. Wang H., Kouri G., Wollheim C.B. ER stress and SREBP-1 activation are implicated in beta-cell glucolipotoxicity. J Cell Sci 2005, 118:3905-3915.
31. Zhang D.D., Hannink M. Distinct cysteine residues in Keap1 are required for Keap1-dependent ubiquitination on Nrf2 and for stabilizationof Nrf2 by chemopreventive agents and oxidative stress. Mol Cell Biol 2003, 23:8137-8151.
32. Angulo P. Treatment of nonalcoholic fatty liver disease. Ann Hepatol 2002, 1:12-19.
33. Bordone L., Cohen D., Robinson A., Motta MC., van Veen E., Czopik A., et al. SIRT1 transgenic mice show phenotypes resembling calorie restriction. Aging Cell 2007, 6:759-767.
34. Escande C., Chini C.C., Nin V., Dykhouse KM., Novak CM., Levine J., et al. Deleted in breast cancer-1 regulates SIRT1 activity and contributes to high-fat diet-induced liver steatosis in mice. J Clin Invest 2010, 120:545-558.
35. Wang X., Sato R., Brown MS., Hua X, Goldstein JL. SREBP-1, a membrane-bound transcription factor released by sterol-regulated proteolysis. Cell 1994, 77:53-62.
36. Sheng Z., Otani H., Brown MS, Goldstein JL. Independent regulation of sterol regulatory element-binding proteins 1 and 2 in hamster liver. Proc Natl Acad Sci U S A 1995, 92:935-938.
37. Surh Y.J., Kundu J.K., Li MH., Na HK., Cha YN. Role of Nrf2-mediated heme oxygenase-1 upregulation in adaptive survival response to nitrosative stress. Arch Pharm Res 2009, 32:1163-1176.
38. Huerta-Olvera S.G., Macías-Barragán J., Ramos-Márquez ME., Armendáriz-Borunda J., Díaz-Barriga F., Siller-López F. Alpha-lipoic acid regulates heme oxygenase gene expression and nuclear Nrf2 activation as a mechanism of protection against arsenic exposure in HepG2 cells. Environ Toxicol Pharmacol 2010, 29:144-149.
39. Kawai Y., Garduño L., Theodore M., Yang J., Arinze IJ. Acetylation-deacetylation of the transcription factor Nrf2 regulates its transcriptional activity and nucleocytoplasmic localization. J Biol Chem 2011, 286:7629-7640.
40. Zheng H.T., Whitman S.A., Wu W., Wondrak GT., Wong PK., Fang D., et al. Therapeutic potential of Nrf2 activators in streptozotocin-induced diabetic nephropathy. Diabetes 2011, 60:3055-3066.
41. Liu X.M., Peyton K.J., Shebib AR., Wang H., Korthuis RJ., Durante W. Activation of AMPK stimulates heme oxygenase-1 gene expression and human endothelial cell survival. Am J Physiol Heart Circ Physiol 2011, 300:H84-H93.
42. Lin Y.C., Lai Y.S., Chou TC. The protective effect of alpha-lipoic acid in lipopolysaccharide-induced acute lung injury is mediated by heme oxygenase-1. Evid Based Complement Alternat Med 2013, 2013:590363.