FGF21 ameliorates nonalcoholic fatty liver disease by inducing autophagy

Molecular and Cellular Biochemistry

Volumn 420, Issue 1-2, 2016, Pages 107-119

  Zhu, Shenglong ^a,b   Wu, Yunzhou ^a   Ye, Xianlong ^c   Ma, Lei ^a   Qi, Jianying ^c   Yu, Dan ^a   Wei, Yuquan ^a   Lin, Guangxiao ^b   Ren, Guiping ^a   Li, Deshan ^a  

^a NORTHEAST AGRICULTURAL UNIVERSITY   (China)

^b JIANGNAN UNIVERSITY   (China)

^c HENAN NORMAL UNIVERSITY   (China)

Author keywords

Autophagy; FGF21; Insulin resistance (IR); MSG; NAFLD

Indexed keywords

ACETYL COENZYME A CARBOXYLASE; ACETYL COENZYME A CARBOXYLASE 1; ACETYL COENZYME A CARBOXYLASE 2; ALANINE; ALKALINE PHOSPHATASE; AUTOPHAGY PROTEIN 12; AUTOPHAGY PROTEIN 3; BECLIN 1; CHOLESTEROL; FATTY ACID SYNTHASE; FENOFIBRATE; FIBROBLAST GROWTH FACTOR 21; GLUCOSE; GLUTAMATE SODIUM; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; LEPTIN; LOW DENSITY LIPOPROTEIN CHOLESTEROL; LOW DENSITY LIPOPROTEIN RECEPTOR; MICROTUBULE ASSOCIATED PROTEIN 1; MICROTUBULE ASSOCIATED PROTEIN 1 LIGHT CHAIN 3; PROTEIN; RECOMBINANT FIBROBLAST GROWTH FACTOR 21; RECOMBINANT PROTEIN; TRIACYLGLYCEROL; UNCLASSIFIED DRUG; UNCOUPLING PROTEIN 1; FIBROBLAST GROWTH FACTOR;

ABDOMINAL OBESITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; BODY WEIGHT; CHOLESTEROL BLOOD LEVEL; CONFOCAL LASER SCANNING MICROSCOPY; CONTROLLED STUDY; DRUG MEGADOSE; FOOD INTAKE; GENE EXPRESSION; GLUCOSE BLOOD LEVEL; HEPG2 CELL LINE; HISTOPATHOLOGY; HUMAN; HUMAN CELL; IN VITRO STUDY; INSULIN SENSITIVITY; LEAN BODY WEIGHT; LIPID METABOLISM; LIPID STORAGE; LIVER CELL; LIVER FUNCTION; LOW DRUG DOSE; LYSOSOME; MALE; METABOLIC PARAMETERS; MOUSE; NONALCOHOLIC FATTY LIVER; NONHUMAN; ORAL GLUCOSE TOLERANCE TEST; PROTEIN EXPRESSION; PROTEIN FUNCTION; REAL TIME POLYMERASE CHAIN REACTION; TRANSMISSION ELECTRON MICROSCOPY; TRIACYLGLYCEROL BLOOD LEVEL; WESTERN BLOTTING; ANIMAL; HEP-G2 CELL LINE; INSTITUTE FOR CANCER RESEARCH MOUSE; METABOLISM; MOUSE MUTANT; NON-ALCOHOLIC FATTY LIVER DISEASE; PATHOLOGY;

ANIMALS; AUTOPHAGY; FIBROBLAST GROWTH FACTORS; HEP G2 CELLS; HUMANS; MICE; MICE, INBRED ICR; MICE, OBESE; NON-ALCOHOLIC FATTY LIVER DISEASE;

EID: 84978763095     PISSN: 03008177     EISSN: 15734919     Source Type: Journal    
DOI: 10.1007/s11010-016-2774-2     Document Type: Article

References (41)

1. Bedogni G, Miglioli L, Masutti F, Tiribelli C, Marchesini G, Bellentani S (2005) Prevalence of and risk factors for nonalcoholic fatty liver disease: the Dionysos nutrition and liver study. Hepatology 42(1):44–52
2. Cohen JC, Horton JD, Hobbs HH (2011) Human fatty liver disease: old questions and new insights. Science 332(6037):1519–1523
3. Stickel F, Hellerbrand C (2010) Non-alcoholic fatty liver disease as a risk factor for hepatocellular carcinoma: mechanisms and implications. Gut 59(10):1303–1307
4. Serfaty L, Lemoine M (2008) Definition and natural history of metabolic steatosis: clinical aspects of NAFLD, NASH and cirrhosis. Diabetes Metab 34(6 Pt 2):634–637
5. García-Villafranca J, Guillén A, Castro J (2008) Ethanol consumption impairs regulation of fatty acid metabolism by decreasing the activity of AMP-activated protein kinase in rat liver. Biochimie 90(3):460–466
6. Angelico F, Del Ben M, Conti R, Francioso S, Feole K, Fiorello S, Cavallo MG, Zalunardo B, Lirussi F, Alessandri C, Violi F (2005) Insulin resistance, the metabolic syndrome, and nonalcoholic fatty liver disease. J Clin Endocrinol Metab 90(3):1578–1582
7. Marchesini G, Bugianesi E, Forlani G, Cerrelli F, Lenzi M, Manini R, Natale S, Vanni E, Villanova N, Melchionda N, Rizzetto M (2003) Nonalcoholic fatty liver, steatohepatitis, and the metabolic syndrome. Hepatology 37(4):917–923
8. Kharitonenkov A, Shiyanova TL, Koester A, Ford AM, Micanovic R, Galbreath EJ, Sandusky GE, Hammond LJ, Moyers JS, Owens RA, Gromada J, Brozinick JT, Hawkins ED, Wroblewski VJ, Li DS, Mehrbod F, Jaskunas SR, Shanafelt AB (2005) FGF-21 as a novel metabolic regulator. J Clin Invest 115(6):1627–1635
9. Gälman C, Lundåsen T, Kharitonenkov A, Bina HA, Eriksson M, Hafström I, Dahlin M, Amark P, Angelin B, Rudling M (2008) The circulating metabolic regulator FGF21 is induced by prolonged fasting and PPAR-α activation in man. Cell Metab 8(2):169–174
10. Kharitonenkov A, Wroblewski VJ, Koester A, Chen YF, Clutinger CK, Tigno XT, Hansen BC, Shanafelt AB, Etgen GJ (2007) The metabolic state of diabetic monkeys is regulated by fibroblast growth factor-21. Endocrinology 148(2):774–781
11. Nakanishi Y, Tsuneyama K, Fujimoto M, Salunga TL, Nomoto K, An JL, Takano Y, Iizuka S, Nagata M, Suzuki W, Shimada T, Aburada M, Nakano M, Selmi C, Gershwin ME (2008) Monosodium glutamate (MSG): a villain and promoter of liver inflammation and dysplasia. J Autoimmun 30(1–2):42–50
12. Cahová M, Daňková H, Páleníčková E, Papáčková Z, Kazdová L (2010) The autophagy-lysosomal pathway is involved in TAG degradation in the liver: the effect of high-sucrose and high-fat diet. Folia Biol (Praha) 56(4):173–182
13. Ding WX, Li M, Yin XM (2011) Selective taste of ethanol-induced autophagy for mitochondria and lipid droplets. Autophagy 7(2):248–249
14. Yang L, Li P, Fu S, Calay ES, Hotamisligil GS (2010) Defective hepatic autophagy in obesity promotes ER stress and causes insulin resistance. Cell Metab 11(6):467–478
15. Amir M, Czaja MJ (2011) Autophagy in nonalcoholic steatohepatitis. Expert Rev Gastroenterol Hepatol 5(2):159–166
16. Singh R, Kaushik S, Wang Y, Xiang Y, Novak I, Komatsu M, Tanaka K, Cuervo AM, Czaja MJ (2009) Autophagy regulates lipid metabolism. Nature 458(7242):1131–1135
17. Jiang P, Huang Z, Zhao H, Wei T (2013) Hydrogen peroxide impairs autophagic flux in a cellmodel of nonalcoholic fatty liver disease. Biochem Biophys Res Commun 433(4):408–414
18. Ye X, Zhao J, Ren G, Yu D, Liu M, Yu Y, Li D (2013) The hypoglycemic effect of the PEGylated FGF-21. Prog Biochem Biophys 40(4):374–385
19. Sun SJ, Shen ZF, Chen YT, Tang L, Ding SY, Xie MZ (2003) Effects of conjugated linoleic acid on obese MSG mice with insulin resistance. Yao Xue Xue Bao 38(12):904–907
20. Liu SN, Liu Q, Shen ZF (2008) A preliminary study on the mechanism of impaired beta cell function in monosodium glutamate obese rat with insulin resistance. Yao Xue Xue Bao 43(11):1106–1111
21. Ramírez-Zacarías JL, Castro-Muñozledo F, Kuri-Harcuch W (1992) Quantitation of adipose conversion and triglycerides by staining intracytoplasmic lipids with Oil red O. Histochemistry 97(6):493–497
22. Shen Z, Liang X, Rogers CQ, Rideout D, You M (2010) Involvement of adiponectin-SIRT1-AMPK signaling in the protective action of rosiglitazone against alcoholic fatty liver in mice. Am J Physiol Gastrointest Liver Physiol 298(3):G364–G374
23. Cusi K (2009) Role of insulin resistance and lipotoxicity in non-alcoholic steatohepatitis. Clin Liver Dis 13(4):545–563
24. Angelico F1, Del Ben M, Conti R, Francioso S, Feole K, Fiorello S, Cavallo MG, Zalunardo B, Lirussi F, Alessandri C, Violi F (2005) Insulin resistance, the metabolic syndrome, and nonalcoholic fatty liver disease. J Clin Endocrinol Metab 90(3):1578–1582
25. Marchesini G, Bugianesi E, Forlani G, Cerrelli F, Lenzi M, Manini R, Natale S, Vanni E, Villanova N, Melchionda N, Rizzetto M (2003) Nonalcoholic fatty liver, steatohepatitis, and the metabolic syndrome. Hepatology 37(4):917–923
26. Ye X, Qi J, Wu Y, Yu D, Xu P, Li S, Zhu S, Wu Q, Ren G, Li D (2015) Comparison of PEGylated FGF-21 with insulin glargine for long-lasting hypoglycaemic effect in db/db mice. Diabetes Metab. 41(1):82–90
27. Xu J, Lloyd DJ, Hale C, Stanislaus S, Chen M, Sivits G, Vonderfecht S, Hecht R, Li YS, Lindberg RA, Chen JL, Jung DY, Zhang Z, Ko HJ, Kim JK, Véniant MMX, X J, JL D, H C, Hale C (2008) Fibroblast growth factor 21 reverses hepatic steatosis, increases energy expenditure, and improves insulin sensitivity in diet-induced obese mice. Diabetes 58(1):250–259
28. Coskun T, Bina HA, Schneider MA, Dunbar JD, Hu CC, Chen Y, Moller DE, Kharitonenkov A (2008) Fibroblast growth factor 21 corrects obesity in mice. Endocrinology 149(12):6018–6027
29. Ye X, Qi J, Ren G, Xu P, Wu Y, Zhu S, Yu D, Li S, Wu Q, Muhi RL, Li D (2015) Long-lasting anti-diabetic efficacy of PEGylated FGF-21 and liraglutide in treatment of type 2 diabetic mice. Endocrine 49(3):683–692
30. Feng X, Jiang Y, Meltzer P, Yen PM (2000) Thyroid hormone regulation of hepatic genes in vivo detected by complementary DNA microarray. Mol Endocrinol 14(7):947–955
31. Xu J, Stanislaus S, Chinookoswong N, Lau YY, Hager T, Patel J, Ge H, Weiszmann J, Lu SC, Graham M, Busby J, Hecht R, Li YS, Li Y, Lindberg R, Véniant MM (2009) Acute glucose-lowering and insulin-sensitizing action of FGF21 in insulin-resistant mouse models–association with liver and adipose tissue effects. Am J Physiol Endocrinol Metab 297(5):E1105–E1114
32. Huett A, Goel G, Xavier RJ (2010) A systems biology viewpoint on autophagy in health and disease. Curr Opin Gastroenterol 26(4):302–309
33. Czaja MJ (2010) Regulation of lipid metabolism and storage by autophagy: pathophysiological implications. Am J Physiol Cell Physiol 298(5):973–978
34. Kaushik S, Singh R, Cuervo AM (2010) Autophagic pathways and metabolic stress. Diabetes Obes Metab 12(Suppl 2):4–14
35. Rautou PE, Mansouri A, Lebrec D, Durand F, Valla D, Moreau R (2010) Autophagy in liver diseases. J Hepatol 53(6):1123–1134
36. Tacke F, Trautwein C (2011) Controlling autophagy: a new concept for clearing liver disease. Hepatology 53(1):356–358
37. Kim KH, Jeong YT, Oh H, Kim SH, Cho JM, Kim YN, Kim SS, Kim do H, Hur KY, Kim HK, Ko T, Han J, Kim HL, Kim J, Back SH, Komatsu M, Chen H, Chan DC, Konishi M, Itoh N, Choi CS, Lee MS (2013) Autophagy deficiency leads to protection from obesity and insulin resistance by inducing Fgf21 as a mitokine. Nat Med 19(1):83–92
38. Gurusamy N, Lekli I, Mukherjee S, Ray D, Ahsan MK, Gherghiceanu M, Popescu LM, Das DK (2010) Cardioprotection by resveratrol: a novel mechanism via autophagy involving the mTORC2 pathway. Cardiovasc Res 86(1):103–112
39. Kimura S, Fujita N, Noda T, Yoshimori T (2009) Monitoring autophagy in mammalian cultured cells through the dynamics of LC3. Methods Enzymol 452:1–12
40. Rubinsztein DC, Cuervo AM, Ravikumar B, Sarkar S, Korolchuk V, Kaushik S, Klionsky DJ (2009) In search of an “autophagomometer”. Autophagy 5(5):585–589
41. Oosterveer MH, Grefhorst A, van Dijk TH, Havinga R, Staels B, Kuipers F, Groen AK, Reijngoud DJ (2009) Fenofibrate simultaneously induces hepatic fatty acid oxidation, synthesis, and elongation in mice. J Biol Chem 284(49):34036–34044