Temporal relationship between diet-induced steatosis and onset of insulin/leptin resistance in male Wistar rats

PLoS ONE

Volumn 10, Issue 2, 2015, Pages

  Zhang, Li ^a   Song, Haiyan ^a   Ge, Yingli ^a   Ji, Guang ^a,b   Yao, Zemin ^c  

^a LONGHUA HOSPITAL AFFILIATED TO SHANGHAI UNIVERSITY OF TRADITIONAL CHINESE MEDICINE   (China)

^b SHANGHAI UNIVERSITY OF TRADITIONAL CHINESE MEDICINE   (China)

^c UNIVERSITY OF OTTAWA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

INSULIN RECEPTOR SUBSTRATE 1; PHOSPHOENOLPYRUVATE CARBOXYKINASE (GTP); PROTEIN KINASE B; STEROL REGULATORY ELEMENT BINDING PROTEIN 1C; SUPPRESSOR OF CYTOKINE SIGNALING 3; GLUCOSE BLOOD LEVEL; INSULIN; LEPTIN; LIPID; LIPOPROTEIN; SUGAR INTAKE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARBOHYDRATE DIET; CONTROLLED STUDY; DYSLIPIDEMIA; GLUCONEOGENESIS; HEPATITIS; HISTOPATHOLOGY; HOMEOSTASIS; HYPERGLYCEMIA; HYPERINSULINEMIA; INSULIN RESISTANCE; INSULIN SENSITIVITY; LIPID DIET; LIPOGENESIS; LIVER METABOLISM; MALE; NONALCOHOLIC FATTY LIVER; NONHUMAN; PROTEIN PHOSPHORYLATION; RAT; SCORING SYSTEM; SIGNAL TRANSDUCTION; UPREGULATION; WISTAR RAT; ADVERSE EFFECTS; ANIMAL; BLOOD; COMPLICATION; FATTY LIVER; GLUCOSE BLOOD LEVEL; HYPERINSULINISM; HYPOTHALAMUS; INFLAMMATION; LIPID METABOLISM; LIVER; METABOLISM; PATHOLOGY; SUGAR INTAKE;

RATTUS; RATTUS NORVEGICUS;

ANIMALS; BLOOD GLUCOSE; DIET, HIGH-FAT; DIETARY SUCROSE; DYSLIPIDEMIAS; FATTY LIVER; HYPERGLYCEMIA; HYPERINSULINISM; HYPOTHALAMUS; INFLAMMATION; INSULIN; INSULIN RESISTANCE; LEPTIN; LIPID METABOLISM; LIPIDS; LIPOPROTEINS; LIVER; MALE; RATS, WISTAR;

EID: 84922631353     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0117008     Document Type: Article

References (49)

1. Szczepaniak LS, Nurenberg P, Leonard D, Browning JD, Reingold JS, et al. (2005) Magnetic resonance spectroscopy to measure hepatic triglyceride content: prevalence of hepatic steatosis in the general population. Am J Physiol Endocrinol Metab 288: E462-468. PMID: 15339742
2. Chiarelli F, Marcovecchio ML (2008) Insulin resistance and obesity in childhood. Eur J Endocrinol 159 Suppl 1: S67-74. doi: 10.1530/EJE-08-0245 PMID: 18805916
3. de Alwis NM, Day CP (2008) Non-alcoholic fatty liver disease: the mist gradually clears. J Hepatol 48 Suppl 1: S104-112. doi: 10.1016/j.jhep.2008.01.009 PMID: 18304679
4. Tom RZ, Sjogren RJ, Vieira E, Glund S, Iglesias-Gutierrez E, et al. (2011) Increased hepatic insulin sensitivity in mice lacking inhibitory leptin receptor signals. Endocrinology 152: 2237-2246. doi: 10. 1210/en.2010-0040 PMID: 21521753
5. Nobili V, Manco M, Ciampalini P, Diciommo V, Devito R, et al. (2006) Leptin, free leptin index, insulin resistance and liver fibrosis in children with non-alcoholic fatty liver disease. Eur J Endocrinol 155: 735-743. PMID: 17062890
6. Huang XD, Fan Y, Zhang H, Wang P, Yuan JP, et al. (2008) Serum leptin and soluble leptin receptor in non-alcoholic fatty liver disease. World J Gastroenterol 14: 2888-2893. PMID: 18473416
7. Kim IK, Kim J, Kang JH, Song J (2008) Serum leptin as a predictor of fatty liver in 7-year-old Korean children. Ann Nutr Metab 53: 109-116. doi: 10.1159/000165360 PMID: 18946208
8. Medici V, Ali MR, Seo S, Aoki CA, Rossaro L, et al. (2010) Increased soluble leptin receptor levels in morbidly obese patients with insulin resistance and nonalcoholic fatty liver disease. Obesity (Silver Spring) 18: 2268-2273. doi: 10.1038/oby.2010.95 PMID: 20448542
9. Bugianesi E, Moscatiello S, Ciaravella MF, Marchesini G (2010) Insulin resistance in nonalcoholic fatty liver disease. Curr Pharm Des 16: 1941-1951. PMID: 20370677
10. Higuchi T, Shirai N, Saito M, Suzuki H, Kagawa Y (2008) Levels of plasma insulin, leptin and adiponectin, and activities of key enzymes in carbohydrate metabolism in skeletal muscle and liver in fasted ICR mice fed dietary n-3 polyunsaturated fatty acids. J Nutr Biochem 19: 577-586. PMID: 17911005
11. Hajiaghamohammadi AA, Ziaee A, Oveisi S, Masroor H (2012) Effects of metformin, pioglitazone, and silymarin treatment on non-alcoholic Fatty liver disease: a randomized controlled pilot study. Hepat Mon 12: e6099. doi: 10.5812/hepatmon.6099 PMID: 23087748
12. Fraulob JC, Souza-Mello V, Aguila MB, Mandarim-de-Lacerda CA (2012) Beneficial effects of rosuvastatin on insulin resistance, adiposity, inflammatory markers and non-alcoholic fatty liver disease in mice fed on a high-fat diet. Clin Sci (Lond) 123: 259-270. doi: 10.1042/CS20110373 PMID: 22420611
13. Li JM, Li YC, Kong LD, Hu QH (2010) Curcumin inhibits hepatic protein-tyrosine phosphatase 1B and prevents hypertriglyceridemia and hepatic steatosis in fructose-fed rats. Hepatology 51: 1555-1566. doi: 10.1002/hep.23524 PMID: 20222050
14. Bhandari U, Kumar V, Khanna N, Panda BP (2011) The effect of high-fat diet-induced obesity on cardiovascular toxicity in Wistar albino rats. Hum Exp Toxicol 30: 1313-1321. doi: 10.1177/0960327110389499 PMID: 21075806
15. Guo J, Jou W, Gavrilova O, Hall KD (2009) Persistent diet-induced obesity in male C57BL/6 mice resulting from temporary obesigenic diets. PLoS One 4: e5370. doi: 10.1371/journal.pone.0005370 PMID: 19401758
16. Bjorbak C, Lavery HJ, Bates SH, Olson RK, Davis SM, et al. (2000) SOCS3 mediates feedback inhibition of the leptin receptor via Tyr985. J Biol Chem 275: 40649-40657. PMID: 11018044
17. Hubschle T, Thom E, Watson A, Roth J, Klaus S, et al. (2001) Leptin-induced nuclear translocation of STAT3 immunoreactivity in hypothalamic nuclei involved in body weight regulation. J Neurosci 21: 2413-2424. PMID: 11264315
18. Banks AS, Davis SM, Bates SH, Myers MG Jr (2000) Activation of downstream signals by the long form of the leptin receptor. J Biol Chem 275: 14563-14572. PMID: 10799542
19. Bates SH, Stearns WH, Dundon TA, Schubert M, Tso AW, et al. (2003) STAT3 signalling is required for leptin regulation of energy balance but not reproduction. Nature 421: 856-859. PMID: 12594516
20. Morris DL, Rui L (2009) Recent advances in understanding leptin signaling and leptin resistance. Am J Physiol Endocrinol Metab 297: E1247-1259. doi: 10.1152/ajpendo.00274.2009 PMID: 19724019
21. Huynh FK, Levi J, Denroche HC, Gray SL, Voshol PJ, et al. (2010) Disruption of hepatic leptin signaling protects mice from age- and diet-related glucose intolerance. Diabetes 59: 3032-3040. doi: 10.2337/db10-0074 PMID: 20876720
22. Huynh FK, Neumann UH, Wang Y, Rodrigues B, Kieffer TJ, et al. (2013) A role for hepatic leptin signaling in lipid metabolism via altered very low density lipoprotein composition and liver lipase activity in mice. Hepatology 57: 543-554. doi: 10.1002/hep.26043 PMID: 22941940
23. Tartaglia LA, Dembski M, Weng X, Deng N, Culpepper J, et al. (1995) Identification and expression cloning of a leptin receptor, OB-R. Cell 83: 1263-1271. PMID: 8548812
24. Huang W, Dedousis N, Bandi A, Lopaschuk GD, O'Doherty RM (2006) Liver triglyceride secretion and lipid oxidative metabolism are rapidly altered by leptin in vivo. Endocrinology 147: 1480-1487. PMID: 16339207
25. Fishman S, Muzumdar RH, Atzmon G, Ma X, Yang X, et al. (2007) Resistance to leptin action is the major determinant of hepatic triglyceride accumulation in vivo. FASEB J 21: 53-60. PMID: 17099068
26. Yue JT, Lam TK (2012) Lipid sensing and insulin resistance in the brain. Cell Metab 15: 646-655. doi: 10.1016/j.cmet.2012.01.013 PMID: 22560217
27. Kanu A, Fain JN, Bahouth SW, Cowan GS Jr (2003) Regulation of leptin release by insulin, glucocorticoids, G(i)-coupled receptor agonists, and pertussis toxin in adipocytes and adipose tissue explants from obese humans in primary culture. Metabolism 52: 60-66. PMID: 12524663
28. Sachithanandan N, Fam BC, Fynch S, Dzamko N, Watt MJ, et al. (2010) Liver-specific suppressor of cytokine signaling-3 deletion in mice enhances hepatic insulin sensitivity and lipogenesis resulting in fatty liver and obesity. Hepatology 52: 1632-1642. doi: 10.1002/hep.23861 PMID: 20799351
29. Inoue H, OgawaW, Ozaki M, Haga S, Matsumoto M, et al. (2004) Role of STAT-3 in regulation of hepatic gluconeogenic genes and carbohydrate metabolism in vivo. Nat Med 10: 168-174. PMID: 14716305
30. Biddinger SB, Hernandez-Ono A, Rask-Madsen C, Haas JT, Aleman JO, et al. (2008) Hepatic insulin resistance is sufficient to produce dyslipidemia and susceptibility to atherosclerosis. Cell Metab 7: 125-134. doi: 10.1016/j.cmet.2007.11.013 PMID: 18249172
31. Villanueva CJ, Monetti M, Shih M, Zhou P, Watkins SM, et al. (2009) Specific role for acyl CoA:Diacylglycerol acyltransferase 1 (Dgat1) in hepatic steatosis due to exogenous fatty acids. Hepatology 50: 434-442. doi: 10.1002/hep.22980 PMID: 19472314
32. Kleiner DE, Brunt EM, Van Natta M, Behling C, Contos MJ, et al. (2005) Design and validation of a histological scoring system for nonalcoholic fatty liver disease. Hepatology 41: 1313-1321. PMID: 15915461
33. Xing LJ, Zhang L, Liu T, Hua YQ, Zheng PY, et al. (2011) Berberine reducing insulin resistance by upregulating IRS-2 mRNA expression in nonalcoholic fatty liver disease (NAFLD) rat liver. Eur J Pharmacol 668: 467-471. doi: 10.1016/j.ejphar.2011.07.036 PMID: 21839075
34. Yang Z, Hulver M, McMillan RP, Cai L, Kershaw EE, et al. (2012) Regulation of insulin and leptin signaling by muscle suppressor of cytokine signaling 3 (SOCS3). PLoS One 7: e47493. doi: 10.1371/journal. pone.0047493 PMID: 23115649
35. El-Haschimi K, Pierroz DD, Hileman SM, Bjorbaek C, Flier JS (2000) Two defects contribute to hypothalamic leptin resistance in mice with diet-induced obesity. J Clin Invest 105: 1827-1832. PMID: 10862798
36. Yang G, Lim CY, Li C, Xiao X, Radda GK, et al. (2009) FoxO1 inhibits leptin regulation of pro-opiomelanocortin promoter activity by blocking STAT3 interaction with specificity protein 1. J Biol Chem 284: 3719-3727. doi: 10.1074/jbc.M804965200 PMID: 19049975
37. Ueki K, Kondo T, Kahn CR (2004) Suppressor of cytokine signaling 1 (SOCS-1) and SOCS-3 cause insulin resistance through inhibition of tyrosine phosphorylation of insulin receptor substrate proteins by discrete mechanisms. Mol Cell Biol 24: 5434-5446. PMID: 15169905
38. Rui L, Yuan M, Frantz D, Shoelson S, White MF (2002) SOCS-1 and SOCS-3 block insulin signaling by ubiquitin-mediated degradation of IRS1 and IRS2. J Biol Chem 277: 42394-42398. PMID: 12228220
39. Metlakunta AS, Sahu M, Sahu A (2008) Hypothalamic phosphatidylinositol 3-kinase pathway of leptin signaling is impaired during the development of diet-induced obesity in FVB/N mice. Endocrinology 149: 1121-1128. PMID: 18048492
40. Barthel A, Schmoll D, Unterman TG (2005) FoxO proteins in insulin action and metabolism. Trends Endocrinol Metab 16: 183-189. PMID: 15860415
41. Kim MS, Pak YK, Jang PG, Namkoong C, Choi YS, et al. (2006) Role of hypothalamic Foxo1 in the regulation of food intake and energy homeostasis. Nat Neurosci 9: 901-906. PMID: 16783365
42. Fabbrini E, Sullivan S, Klein S (2010) Obesity and nonalcoholic fatty liver disease: biochemical, metabolic, and clinical implications. Hepatology 51: 679-689. doi: 10.1002/hep.23280 PMID: 20041406
43. Cline GW, Johnson K, RegittnigW, Perret P, Tozzo E, et al. (2002) Effects of a novel glycogen synthase kinase-3 inhibitor on insulin-stimulated glucose metabolism in Zucker diabetic fatty (fa/fa) rats. Diabetes 51: 2903-2910. PMID: 12351425
44. Lacombe VA (2014) Expression and regulation of facilitative glucose transporters in equine insulin-sensitive tissue: from physiology to pathology. ISRN Vet Sci 2014: 409547. doi: 10.1155/2014/409547 PMID: 24977043
45. Horiguchi N, Wang L, Mukhopadhyay P, Park O, Jeong WI, et al. (2008) Cell type-dependent pro- and anti-inflammatory role of signal transducer and activator of transcription 3 in alcoholic liver injury. Gastroenterology 134: 1148-1158. doi: 10.1053/j.gastro.2008.01.016 PMID: 18395093
46. Wang H, Lafdil F, Kong X, Gao B (2011) Signal transducer and activator of transcription 3 in liver diseases: a novel therapeutic target. Int J Biol Sci 7: 536-550. PMID: 21552420
47. Ueki K, Kondo T, Tseng YH, Kahn CR (2004) Central role of suppressors of cytokine signaling proteins in hepatic steatosis, insulin resistance, and the metabolic syndrome in the mouse. Proc Natl Acad Sci U S A 101: 10422-10427. PMID: 15240880
48. Martin TL, Alquier T, Asakura K, Furukawa N, Preitner F, et al. (2006) Diet-induced obesity alters AMP kinase activity in hypothalamus and skeletal muscle. J Biol Chem 281: 18933-18941. PMID: 16687413
49. Ramadoss P, Unger-Smith NE, Lam FS, Hollenberg AN (2009) STAT3 targets the regulatory regions of gluconeogenic genes in vivo. Mol Endocrinol 23: 827-837. doi: 10.1210/me.2008-0264 PMID: 19264844