Activation of ERK1/2 ameliorates liver steatosis in leptin receptor-deficient (db/db) mice via stimulating ATG7-dependent autophagy

Diabetes

Volumn 65, Issue 2, 2016, Pages 393-405

  Xiao, Yuzhong ^a   Liu, Hao ^a   Yu, Junjie ^a   Zhao, Zilong ^a   Xiao, Fei ^a   Xia, Tingting ^a   Wang, Chunxia ^a   Li, Kai ^a   Deng, Jiali ^a   Guo, Yajie ^a   Chen, Shanghai ^a   Chen, Yan ^a   Guo, Feifan ^a  

^a UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

Author keywords

[No Author keywords available]

Indexed keywords

3 HYDROXYBUTYRIC ACID; ACETYL COENZYME A CARBOXYLASE; ACYL COENZYME A DESATURASE; APOLIPOPROTEIN B; AUTOPHAGY RELATED PROTEIN 7; CARBOHYDRATE RESPONSIVE ELEMENT BINDING PROTEIN; CARNITINE PALMITOYLTRANSFERASE I; FATTY ACID BINDING PROTEIN; FATTY ACID SYNTHASE; FATTY ACID TRANSPORTING PROTEIN; GLUCOSE; GLYCEROL 3 PHOSPHATE ACYLTRANSFERASE; INSULIN; LEPTIN RECEPTOR; MALATE DEHYDROGENASE (DECARBOXYLATING); MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PROTEIN; STEROL REGULATORY ELEMENT BINDING PROTEIN 1C; TRIACYLGLYCEROL; UNCLASSIFIED DRUG; ATG7 PROTEIN, MOUSE; MAP2K1 PROTEIN, MOUSE; MICROTUBULE ASSOCIATED PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; BODY WEIGHT; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; FAT MASS; FATTY ACID OXIDATION; FATTY ACID TRANSPORT; FATTY LIVER; FOOD INTAKE; GLUCOSE BLOOD LEVEL; IN VITRO STUDY; INSULIN BLOOD LEVEL; INSULIN TOLERANCE TEST; LIPID LIVER LEVEL; LIPID METABOLISM; LIPID STORAGE; LIPOGENESIS; LIVER CELL; LIVER WEIGHT; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; ANIMAL; C57BL MOUSE; DEFICIENCY; ENZYMOLOGY; KNOCKOUT MOUSE; LIVER; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION;

3-HYDROXYBUTYRIC ACID; ANIMALS; AUTOPHAGY; ENZYME ACTIVATION; FATTY LIVER; HEPATOCYTES; LIPID METABOLISM; LIVER; MALE; MAP KINASE KINASE 1; MAP KINASE SIGNALING SYSTEM; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROTUBULE-ASSOCIATED PROTEINS; RECEPTORS, LEPTIN; TRIGLYCERIDES;

EID: 84962385701     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db15-1024     Document Type: Article

References (50)

1. Liu W, Cao H, Yan J, Huang R, Ying H. 'Micro-managers' of hepatic lipid metabolism and NAFLD. Wiley Interdiscip Rev RNA 2015; 6: 581-593
2. Kerr TA, Davidson NO. Cholesterol and nonalcoholic fatty liver disease: renewed focus on an old villain. Hepatology 2012; 56: 1995-1998
3. Neuschwander-Tetri BA, Caldwell SH. Nonalcoholic steatohepatitis: summary of an AASLD Single Topic Conference. Hepatology 2003; 37: 1202-1219
4. Postic C, Girard J. Contribution of de novo fatty acid synthesis to hepatic steatosis and insulin resistance: lessons from genetically engineered mice. J Clin Invest 2008; 118: 829-838
5. Mizushima N. Physiological functions of autophagy. Curr Top Microbiol Immunol 2009; 335: 71-84
6. Singh R, Cuervo AM: Lipophagy: connecting autophagy and lipid metabolism. Int J Cell Biol 2012; 2012: 282041
7. Singh R, Kaushik S, Wang Y, et al. Autophagy regulates lipid metabolism. Nature 2009; 458: 1131-1135
8. Shen HM, Mizushima N. At the end of the autophagic road: an emerging understanding of lysosomal functions in autophagy. Trends Biochem Sci 2014; 39: 61-71
9. Dong H, Czaja MJ. Regulation of lipid droplets by autophagy. Trends Endocrinol Metab 2011; 22: 234-240
10. Jaber N, Dou Z, Chen JS, et al. Class III PI3K Vps34 plays an essential role in autophagy and in heart and liver function. Proc Natl Acad Sci U S A 2012; 109: 2003-2008
11. Sinha RA, Farah BL, Singh BK, et al. Caffeine stimulates hepatic lipid metabolism by the autophagy-lysosomal pathway in mice. Hepatology 2014; 59: 1366-1380
12. Lin C-W, Zhang H, Li M, et al. Pharmacological promotion of autophagy alleviates steatosis and injury in alcoholic and non-alcoholic fatty liver conditions in mice. J Hepatol 2013; 58: 993-999
13. 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
14. Bost F, Aouadi M, Caron L, et al. The extracellular signal-regulated kinase isoform ERK1 is specifically required for in vitro and in vivo adipogenesis. Diabetes 2005; 54: 402-411
15. Wiesenauer CA, Yip-Schneider MT, Wang Y, Schmidt CM. Multiple anticancer effects of blocking MEK-ERK signaling in hepatocellular carcinoma. J Am Coll Surg 2004; 198: 410-421
16. Liu H, Yu J, Xia T, et al. Hepatic serum- and glucocorticoid-regulated protein kinase 1 (SGK1) regulates insulin sensitivity in mice via extracellular-signal-regulated kinase 1/2 (ERK1/2). Biochem J 2014; 464: 281-289
17. Jiao P, Feng B, Li Y, He Q, Xu H. Hepatic ERK activity plays a role in energy metabolism. Mol Cell Endocrinol 2013; 375: 157-166
18. Tsai J, Qiu W, Kohen-Avramoglu R, Adeli K. MEK-ERK inhibition corrects the defect in VLDL assembly in HepG2 cells: potential role of ERK in VLDL-ApoB100 particle assembly. Arterioscler Thromb Vasc Biol 2007; 27: 211-218
19. Mauvoisin D, Prévost M, Ducheix S, Arnaud MP, Mounier C. Key role of the ERK1/2 MAPK pathway in the transcriptional regulation of the Stearoyl-CoA Desaturase (SCD1) gene expression in response to leptin. Mol Cell Endocrinol 2010; 319: 116-128
20. Yousefi B, Darabi M, Baradaran B, et al. Inhibition of MEK/ERK1/2 signaling affects the fatty acid composition of HepG2 human hepatic cell line. Bioimpacts 2012; 2: 145-150
21. Wang J, Whiteman MW, Lian H, et al. A non-canonical MEK/ERK signaling pathway regulates autophagy via regulating Beclin 1. J Biol Chem 2009; 284: 21412-21424
22. Gong K, Chen C, Zhan Y, Chen Y, Huang Z, Li W. Autophagy-related gene 7 (ATG7) and reactive oxygen species/extracellular signal-regulated kinase regulate tetrandrine-induced autophagy in human hepatocellular carcinoma. J Biol Chem 2012; 287: 35576-35588
23. Keil E, Höcker R, Schuster M, et al. Phosphorylation of Atg5 by the Gadd45β-MEKK4-p38 pathway inhibits autophagy. Cell Death Differ 2013; 20: 321-332
24. Wang Q, Jiang L, Wang J, et al. Abrogation of hepatic ATP-citrate lyase protects against fatty liver and ameliorates hyperglycemia in leptin receptor-deficient mice. Hepatology 2009; 49: 1166-1175
25. Ding WX, Li M, Chen X, et al. Autophagy reduces acute ethanol-induced hepatotoxicity and steatosis in mice. Gastroenterology 2010; 139: 1740-1752
26. Palmer WK, Emeson EE, Johnston TP. Poloxamer 407-induced atherogenesis in the C57BL/6 mouse. Atherosclerosis 1998; 136: 115-123
27. Willaime S, Vanhoutte P, Caboche J, Lemaigre-Dubreuil Y, Mariani J, Brugg B. Ceramide-induced apoptosis in cortical neurons is mediated by an increase in p38 phosphorylation and not by the decrease in ERK phosphorylation. Eur J Neurosci 2001; 13: 2037-2046
28. Folch J, Lees M, Sloane Stanley GH A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 1957; 226: 497-509
29. Shao M, Shan B, Liu Y, et al. Hepatic IRE1α regulates fasting-induced metabolic adaptive programs through the XBP1s-PPARα axis signalling. Nat Commun 2014; 5: 3528
30. Yuan L, Xiao Y, Zhou Q, et al. Proteomic analysis reveals that MAEL, a component of nuage, interacts with stress granule proteins in cancer cells. Oncol Rep 2014; 31: 342-350
31. Anstee QM, Goldin RD. Mouse models in non-alcoholic fatty liver disease and steatohepatitis research. Int J Exp Pathol 2006; 87: 1-16
32. Horton JD, Shimomura I. Sterol regulatory element-binding proteins: activators of cholesterol and fatty acid biosynthesis. Curr Opin Lipidol 1999; 10: 143-150
33. Yang L, Li P, Fu S, Calay ES, Hotamisligil GS. Defective hepatic autophagy in obesity promotes ER stress and causes insulin resistance. Cell Metab 2010; 11: 467-478
34. Mizushima N, Yoshimori T, Ohsumi Y. The role of Atg proteins in auto-phagosome formation. Annu Rev Cell Dev Biol 2011; 27: 107-132
35. Berra E, Diaz-Meco MT, Moscat J. The activation of p38 and apoptosis by the inhibition of Erk is antagonized by the phosphoinositide 3-kinase/Akt pathway. J Biol Chem 1998; 273: 10792-10797
36. Häussinger D, Schliess F, Dombrowski F, Vom Dahl S. Involvement of p38MAPK in the regulation of proteolysis by liver cell hydration. Gastroenterology 1999; 116: 921-935
37. Rahmouni K, Sigmund CD, Haynes WG, Mark AL. Hypothalamic ERK mediates the anorectic and thermogenic sympathetic effects of leptin. Diabetes 2009; 58: 536-542
38. Weng L-P, Smith WM, Brown JL, Eng C. PTEN inhibits insulin-stimulated MEK/MAPK activation and cell growth by blocking IRS-1 phosphorylation and IRS-1/Grb-2/Sos complex formation in a breast cancer model. Hum Mol Genet 2001; 10: 605-616
39. Li XC, Carretero OA, Shao Y, Zhuo JL. Glucagon receptor-mediated extracellular signal-regulated kinase 1/2 phosphorylation in rat mesangial cells: role of protein kinase A and phospholipase C. Hypertension 2006; 47: 580-585
40. Gan L, Xiang W, Xie B, Yu L. Molecular mechanisms of fatty liver in obesity. Front Med 2015; 9: 275-287
41. Feng B, Jiao P, Yang Z, Xu H. MEK/ERK pathway mediates insulin-promoted degradation of MKP-3 protein in liver cells. Mol Cell Endocrinol 2012; 361: 116-123
42. Wang B, Chandrasekera PC, Pippin JJ. Leptin- and leptin receptor-deficient rodent models: relevance for human type 2 diabetes. Curr Diabetes Rev 2014; 10: 131-145
43. Sekiya S, Suzuki A. Glycogen synthase kinase 3 β-dependent Snail degradation directs hepatocyte proliferation in normal liver regeneration. Proc Natl Acad Sci U S A 2011; 108: 11175-11180
44. Liu Y, Shao M, Wu Y, et al. Role for the endoplasmic reticulum stress sensor IRE1α in liver regenerative responses. J Hepatol 2015; 62: 590-598
45. Jager J, Corcelle V, Grémeaux T, et al. Deficiency in the extracellular signalregulated kinase 1 (ERK1) protects leptin-deficient mice from insulin resistance without affecting obesity. Diabetologia 2011; 54: 180-189
46. Bouzakri K, Roques M, Gual P, et al. Reduced activation of phosphatidylinositol-3 kinase and increased serine 636 phosphorylation of insulin receptor substrate-1 in primary culture of skeletal muscle cells from patients with type 2 diabetes. Diabetes 2003; 52: 1319-1325
47. Yamaguchi K, Yang L, McCall S, et al. Inhibiting triglyceride synthesis improves hepatic steatosis but exacerbates liver damage and fibrosis in obese mice with nonalcoholic steatohepatitis. Hepatology 2007; 45: 1366-1374
48. Li ZZ, Berk M, McIntyre TM, Feldstein AE. Hepatic lipid partitioning and liver damage in nonalcoholic fatty liver disease: role of stearoyl-CoA desaturase. J Biol Chem 2009; 284: 5637-5644
49. Wu M, Lao Y, Xu N, et al. Guttiferone K induces autophagy and sensitizes cancer cells to nutrient stress-induced cell death. Phytomedicine 2015; 22: 902-910
50. Verschuren WM, Jacobs DR, Bloemberg BP, et al. Serum total cholesterol and long-term coronary heart disease mortality in different cultures. Twenty-five-year follow-up of the seven countries study. JAMA 1995; 274: 131-136