Liraglutide ameliorates non-alcoholic fatty liver disease by enhancing mitochondrial architecture and promoting autophagy through the SIRT1/SIRT3–FOXO3a pathway

Hepatology Research

Volumn 46, Issue 9, 2016, Pages 933-943

  Tong, Wenxin ^a   Ju, Liping ^a   Qiu, Miaoyan ^a   Xie, Qihai ^a   Chen, Ying ^a   Shen, Weili ^a   Sun, Weihong ^a   Wang, Weiqing ^a   Tian, Jingyan ^a  

^a SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

autophagy; liraglutide; mitochondrial architecture; oxidative stress

Indexed keywords

BECLIN 1; CATALASE; COMPLEX1 ENZYME; DRP1 ENZYME; GUANOSINE TRIPHOSPHATASE; LIRAGLUTIDE; MALONALDEHYDE; MANGANESE SUPEROXIDE DISMUTASE; MICROTUBULE ASSOCIATED PROTEIN 2; OPA1 ENZYME; PROTEIN P62; REACTIVE OXYGEN METABOLITE; SIRTUIN 1; SIRTUIN 3; TRANSCRIPTION FACTOR FKHRL1; TRIACYLGLYCEROL; UNCLASSIFIED DRUG; UNCOUPLING PROTEIN 2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOPHAGY; CONTROLLED STUDY; CYTOARCHITECTURE; DRUG MECHANISM; ENZYME INDUCTION; FOOD INTAKE; GENE EXPRESSION REGULATION; GLUCOSE TOLERANCE; LIPID COMPOSITION; LIPID LIVER LEVEL; MALE; MITOCHONDRION; MOUSE; NONALCOHOLIC FATTY LIVER; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TREATMENT DURATION; UPREGULATION; WEIGHT REDUCTION;

EID: 84982823017     PISSN: 13866346     EISSN: 1872034X     Source Type: Journal    
DOI: 10.1111/hepr.12634     Document Type: Article

References (38)

1. Sonsuz A, Basaranoglu M, Ozbay G. Relationship between aminotransferase levels and histopathological findings in patients with nonalcoholic steatohepatitis. Am J Gastroenterol 2000 (May); 95: 1370–1.
2. Ratziu V, Goodman Z, Sanyal A. Current efforts and trends in the treatment of NASH. J Hepatol 2015 (Apr)62: S65–s75.
3. Eng C, Kramer CK, Zinman B, Retnakaran R. Glucagon-like peptide-1 receptor agonist and basal insulin combination treatment for the management of type 2 diabetes: a systematic review and meta-analysis. Lancet 2014 (Dec 20) 384: 2228–34.
4. Eguchi Y, Kitajima Y, Hyogo H et al. Pilot study of liraglutide effects in non-alcoholic steatohepatitis and non-alcoholic fatty liver disease with glucose intolerance in Japanese patients (LEAN-J). Hepatol Res: the official journal of the Japan Society of Hepatology 2015 (Mar); 45: 269–78.
5. Kahal H, Abouda G, Rigby AS, Coady AM, Kilpatrick ES, Atkin SL. Glucagon-like peptide-1 analogue, liraglutide, improves liver fibrosis markers in obese women with polycystic ovary syndrome and nonalcoholic fatty liver disease. Clin Endocrinol 2014 (Oct); 81: 523–8.
6. Sharma S, Mells JE, Fu PP, Saxena NK, Anania FA. GLP-1 analogs reduce hepatocyte steatosis and improve survival by enhancing the unfolded protein response and promoting macroautophagy. PLoS One 2011; 6: e25269.
7. Gao H, Xu L, Li D, Guang L, Deng W. [Effects of glucagon-like peptide-1 on liver oxidative stress, TNF-alpha and TGF-beta1 in rats with non-alcoholic fatty liver disease]. Nan fang yi ke da xue xue bao = Journal of Southern Medical University 2013 (Nov); 33: 1661–4.
8. Jing Yin J, Bo Li Y, Ming Cao M, Wang Y. Liraglutide Improves the Survival of INS-1 Cells by Promoting Macroautophagy. Int J Endocrinol Metab 2013 (Summer); 11: 184–90.
9. Krasner NM, Ido Y, Ruderman NB, Cacicedo JM. Glucagon-like peptide-1 (GLP-1) analog liraglutide inhibits endothelial cell inflammation through a calcium and AMPK dependent mechanism. PLoS One 2014; 9: e97554.
10. Wang L, Liu X, Nie J et al. ALCAT1 controls mitochondrial etiology of fatty liver diseases, linking defective mitophagy to steatosis. Hepatology 2015 (Feb); 61: 486–96.
11. Gambino R, Musso G, Cassader M. Redox balance in the pathogenesis of nonalcoholic fatty liver disease: mechanisms and therapeutic opportunities. Antioxid Redox Signal 2011 (Sep 1); 15: 1325–65.
12. Ganji SH, Kashyap ML, Kamanna VS. Niacin inhibits fat accumulation, oxidative stress, and inflammatory cytokine IL-8 in cultured hepatocytes: Impact on non-alcoholic fatty liver disease. Metab Clin Exp 2015 (Sep); 64: 982–90.
13. Cahova M, Palenickova E, Dankova H et al. Metformin prevents ischemia reperfusion-induced oxidative stress in the fatty liver by attenuation of reactive oxygen species formation. Am J Physiol Gastrointest Liver Physiol 2015 (Jun 4): ajpgi.00329.2014.
14. Nakatsu Y, Seno Y, Kushiyama A et al. The xanthine oxidase inhibitor febuxostat suppresses development of nonalcoholic steatohepatitis in a rodent model. Am J Physiol Gastrointest Liver Physiol 2015 (May 21): ajpgi.00443.2014.
15. Shabalina IG, Nedergaard J. Mitochondrial (‘mild’) uncoupling and ROS production: physiologically relevant or not? Biochem Soc Trans 2011 (Oct); 39: 1305–9.
16. Ortiz-Avila O, Gallegos-Corona MA, Sanchez-Briones LA et al. Protective effects of dietary avocado oil on impaired electron transport chain function and exacerbated oxidative stress in liver mitochondria from diabetic rats. J Bioenerg Biomembr 2015; (Aug);47: 337–53.
17. Adjeitey CN, Mailloux RJ, Dekemp RA, Harper ME. Mitochondrial uncoupling in skeletal muscle by UCP1 augments energy expenditure and glutathione content while mitigating ROS production. Am J Physiol Endocrinol Metab 2013 (Aug 1); 305: E405–15.
18. Biala AK, Dhingra R, Kirshenbaum LA. Mitochondrial dynamics: Orchestrating the journey to advanced age. J Mole Cell Cardiol 2015 (Jun); 83: 37–43.
19. Scherz-Shouval R, Elazar Z. Regulation of autophagy by ROS: physiology and pathology. Trends Biochem Sci 2011 (Jan); 36: 30–8.
20. Ney PA. Mitochondrial autophagy: Origins, significance, and role of BNIP3 and NIX. Biochim Biophys Acta 2015 (Oct); 1853: 2775–83.
21. van der Bliek AM, Shen Q, Kawajiri S. Mechanisms of mitochondrial fission and fusion. Cold Spring Harb Perspect Biol 2013 (Jun); 5: a011072.
22. Lee IH, Cao L, Mostoslavsky R et al. A role for the NAD-dependent deacetylase Sirt1 in the regulation of autophagy. Proceedings of the National Academy of Sciences of the United States of America. 2008 (Mar 4); 105: 3374–9.
23. Guarente L. Mitochondria--a nexus for aging, calorie restriction, and sirtuins? Cell 2008 (Jan 25); 132: 171–6.
24. Pinkston-Gosse J, Kenyon C. DAF-16/FOXO targets genes that regulate tumor growth in Caenorhabditis elegans. Nat Genet 2007 (Nov); 39: 1403–9.
25. Das S, Mitrovsky G, Vasanthi HR, Das DK. Antiaging properties of a grape-derived antioxidant are regulated by mitochondrial balance of fusion and fission leading to mitophagy triggered by a signaling network of Sirt1-Sirt3-Foxo3-PINK1-PARKIN. Oxid Med Cell Longev 2014; 2014: 345105.
26. Jacobs KM, Pennington JD, Bisht KS et al. SIRT3 interacts with the daf-16 homolog FOXO3a in the mitochondria, as well as increases FOXO3a dependent gene expression. Int J Biol Sci 2008; 4: 291–9.
27. Liesa M, Shirihai OS. Mitochondrial dynamics in the regulation of nutrient utilization and energy expenditure. Cell Metab 2013 (Apr 2); 17: 491–506.
28. Sebastian D, Hernandez-Alvarez MI, Segales J et al. Mitofusin 2 (Mfn2) links mitochondrial and endoplasmic reticulum function with insulin signaling and is essential for normal glucose homeostasis. Proceedings of the National Academy of Sciences of the United States of America. 2012 (Apr 3); 109: 5523-8.
29. Nadal-Casellas A, Amengual-Cladera E, Proenza AM, Llado I, Gianotti M. Long-term high-fat-diet feeding impairs mitochondrial biogenesis in liver of male and female rats. Cell Physiol Biochem: international journal of experimental cellular physiology, biochemistry, and pharmacology 2010; 26: 291–302.
30. Franko A, von Kleist-Retzow JC, Neschen S et al. Liver adapts mitochondrial function to insulin resistant and diabetic states in mice. J Hepatol 2014 (Apr); 60: 816–23.
31. Flamment M, Rieusset J, Vidal H, et al. Regulation of hepatic mitochondrial metabolism in response to a high fat diet: a longitudinal study in rats. J Physiol Biochem 2012 (Sep); 68: 335–44.
32. Held NM, Houtkooper RH. Mitochondrial quality control pathways as determinants of metabolic health. BioEssays: news and reviews in molecular, cellular and developmental biology 2015 (Aug); 37: 867–76.
33. Zhou SW, Zhang M, Zhu M. Liraglutide reduces lipid accumulation in steatotic L02 cells by enhancing autophagy. Mol Med Rep 2014 (Nov); 10: 2351–7.
34. Pallauf K, Rimbach G. Autophagy, polyphenols and healthy ageing. Ageing Res Rev 2013 (Jan); 12: 237–52.
35. Caton PW, Nayuni NK, Kieswich J, Khan NQ, Yaqoob MM, Corder R. Metformin suppresses hepatic gluconeogenesis through induction of SIRT1 and GCN5. J Endocrinol 2010 (Apr); 205: 97–106.
36. Song YM, Lee YH, Kim JW et al. Metformin alleviates hepatosteatosis by restoring SIRT1-mediated autophagy induction via an AMP-activated protein kinase-independent pathway. Autophagy 2015; 11: 46–59.
37. Aucello M, Dobrowolny G, Musaro A. Localized accumulation of oxidative stress causes muscle atrophy through activation of an autophagic pathway. Autophagy 2009 (May); 5: 527–9.
38. Li L, Tan J, Miao Y, Lei P, Zhang Q. ROS and Autophagy: Interactions and Molecular Regulatory Mechanisms. Cell Mol Neurobiol 2015 (Jul); 35: 615–21.