High expression of liver histone deacetylase 3 contributes to high-fat-diet-induced metabolic syndrome by suppressing the PPAR-γ and LXR-α-pathways in E3 rats

Molecular and Cellular Endocrinology

Volumn 344, Issue 1-2, 2011, Pages 69-80

  Li, Dongmin ^a,b   Wang, Xuan ^a,b   Ren, Wuchao ^a,b   Ren, Juan ^a,b   Lan, Xi ^a,b   Wang, Feimiao ^a,b   Li, Hongmin ^c   Zhang, Fujun ^a,b   Han, Yan ^a,b   Song, Tianbao ^a,b   Holmdahl, Rikard ^d   Lu, Shemin ^a,b  

^a MEDICAL SCHOOL OF XI AN JIAOTONG UNIVERSITY   (China)

^b XI'AN JIAOTONG UNIVERSITY   (China)

^c NORTHWEST UNIVERSITY   (China)

^d KAROLINSKA INSTITUTE   (Sweden)

Author keywords

DA.1U rat; E3 rat; Histone deacetylase 3; Liver X receptor ; Metabolic syndrome; Peroxisome proliferator activated receptor

Indexed keywords

CELL NUCLEUS RECEPTOR; CHOLESTEROL 7ALPHA MONOOXYGENASE; HISTONE DEACETYLASE 3; LIVER X RECEPTOR ALPHA; LIVER X RECEPTOR BETA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA;

ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; GENETIC DIFFERENCE; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; LIPID DIET; LIVER CELL; METABOLIC SYNDROME X; MOLECULAR MECHANICS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; WESTERN BLOTTING;

ANIMALS; CHOLESTEROL 7-ALPHA-HYDROXYLASE; DIET, HIGH-FAT; FEMALE; GENE EXPRESSION PROFILING; GLUCOSE TRANSPORTER TYPE 2; GLUCOSE TRANSPORTER TYPE 4; HISTONE DEACETYLASES; LIPIDS; LIVER; MALE; METABOLIC SYNDROME X; ORGAN SIZE; ORPHAN NUCLEAR RECEPTORS; PPAR GAMMA; RATS; RECEPTOR, INSULIN; RETINOID X RECEPTORS; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC;

EID: 84860391445     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2011.06.028     Document Type: Article

References (64)

1. Alberti K.G., et al. Metabolic syndrome - a new world-wide definition. A Consensus Statement from the International Diabetes Federation. Diabet. Med. 2006, 23:469-480.
2. Berger J., Moller D.E. The mechanisms of action of PPARs. Annu. Rev. Med. 2002, 53:409-435.
3. Bruning J.C., et al. Development of a novel polygenic model of NIDDM in mice heterozygous for IR and IRS-1 null alleles. Cell 1997, 88:561-572.
4. Canto C., Auwerx J. PGC-1alpha, SIRT1 and AMPK, an energy sensing network that controls energy expenditure. Curr. Opin. Lipidol. 2009, 20:98-105.
5. Carvalho E., et al. Adipose-specific overexpression of GLUT4 reverses insulin resistance and diabetes in mice lacking GLUT4 selectively in muscle. Am. J. Physiol. Endocrinol. Metab. 2005, 289:E551-E561.
6. Chawla A., et al. A PPAR gamma-LXR-ABCA1 pathway in macrophages is involved in cholesterol efflux and atherogenesis. Mol. Cell. 2001, 7:161-171.
7. Chiang J.Y., et al. Regulation of cholesterol 7alpha-hydroxylase gene (CYP7A1) transcription by the liver orphan receptor (LXRalpha). Gene 2001, 262:257-265.
8. de Ruijter A.J., et al. Histone deacetylases (HDACs): characterization of the classical HDAC family. Biochem. J. 2003, 370:737-749.
9. Dominici F.P., et al. Increased insulin sensitivity and upregulation of insulin receptor, insulin receptor substrate (IRS)-1 and IRS-2 in liver of Ames dwarf mice. J. Endocrinol. 2002, 173:81-94.
10. Duncan R.E., Archer M.C. Farnesol decreases serum triglycerides in rats: identification of mechanisms including up-regulation of PPARalpha and down-regulation of fatty acid synthase in hepatocytes. Lipids 2008, 43:619-627.
11. Efendic S., et al. Increased activity of the glucose cycle in the liver: early characteristic of type 2 diabetes. Proc. Natl. Acad. Sci. USA 1985, 82:2965-2969.
12. Etienne J., Brault D. Lipoprotein lipase deficiencies. Ann. Biol. Clin. (Paris) 1992, 50:299-309.
13. Expert Panel on Detection, E., Treatment of High Blood Cholesterol in Adults, 2001. Executive Summary of The Third Report of The National Cholesterol Education Program (NCEP) Expert Panel on Detection, Evaluation, And Treatment of High Blood Cholesterol In Adults (Adult Treatment Panel III). JAMA 285, 2486-2497.
14. Fiorucci S., Baldelli F. Farnesoid X receptor agonists in biliary tract disease. Curr. Opin. Gastroenterol. 2009, 25:252-259.
15. Gao Z., et al. Butyrate improves insulin sensitivity and increases energy expenditure in mice. Diabetes 2009, 58:1509-1517.
16. Gong F.Y., et al. Fatty acid synthase and hormone-sensitive lipase expression in liver are involved in zinc-alpha2-glycoprotein-induced body fat loss in obese mice. Chin. Med. Sci. J. 2010, 25:169-175.
17. Gupta S., et al. LXR alpha is the dominant regulator of CYP7A1 transcription. Biochem. Biophys. Res. Commun. 2002, 293:338-343.
18. Hamm J.K., et al. Role of PPAR gamma in regulating adipocyte differentiation and insulin-responsive glucose uptake. Ann. NY Acad. Sci. 1999, 892:134-145.
19. Holmdahl R., et al. Arthritis induced in rats with adjuvant oil is a genetically restricted, alpha beta T-cell dependent autoimmune disease. Immunology 1992, 76:197-202.
20. Inagaki T., et al. Fibroblast growth factor 15 functions as an enterohepatic signal to regulate bile acid homeostasis. Cell. Metab. 2005, 2:217-225.
21. Iwata M., et al. Pioglitazone ameliorates tumor necrosis factor-alpha-induced insulin resistance by a mechanism independent of adipogenic activity of peroxisome proliferator - activated receptor-gamma. Diabetes 2001, 50:1083-1092.
22. Jin L., et al. Crystal structures of human SIRT3 displaying substrate-induced conformational changes. J. Biol. Chem. 2009, 284:24394-24405.
23. Joseph S.B., et al. Direct and indirect mechanisms for regulation of fatty acid synthase gene expression by liver X receptors. J. Biol. Chem. 2002, 277:11019-11025.
24. Kast H.R., et al. Farnesoid X-activated receptor induces apolipoprotein C-II transcription: a molecular mechanism linking plasma triglyceride levels to bile acids. Mol. Endocrinol. 2001, 15:1720-1728.
25. Kelly T., et al. Global burden of obesity in 2005 and projections to 2030. Int. J. Obes. (Lond.) 2008, 32:1431-1437.
26. Kim J.B., Spiegelman B.M. ADD1/SREBP1 promotes adipocyte differentiation and gene expression linked to fatty acid metabolism. Genes Dev. 1996, 10:1096-1107.
27. Kloting I., et al. Mapping of novel genes predisposing or protecting diabetes development in the BB/OK rat. Biochem. Biophys. Res. Commun. 1998, 245:483-486.
28. Knutson S.K., et al. Liver-specific deletion of histone deacetylase 3 disrupts metabolic transcriptional networks. EMBO J. 2008, 27:1017-1028.
29. Laffitte B.A., et al. Activation of liver X receptor improves glucose tolerance through coordinate regulation of glucose metabolism in liver and adipose tissue. Proc. Natl. Acad. Sci. USA 2003, 100:5419-5424.
30. Lai P.H., et al. HDAC1/HDAC3 modulates PPARG2 transcription through the sumoylated CEBPD in hepatic lipogenesis. Biochim. Biophys. Acta 2008, 1783:1803-1814.
31. Lawless M.W., et al. Histone deacetylase inhibitors target diabetes via chromatin remodeling or as chemical chaperones?. Curr. Diabetes Rev. 2009, 5:201-209.
32. Li D., et al. A modified method using TRIzol reagent and liquid nitrogen produces high-quality RNA from rat pancreas. Appl. Biochem. Biotechnol. 2009, 158:253-261.
33. Li J., et al. Both corepressor proteins SMRT and N-CoR exist in large protein complexes containing HDAC3. EMBO J. 2000, 19:4342-4350.
34. Mak P.A., et al. Identification of PLTP as an LXR target gene and apoE as an FXR target gene reveals overlapping targets for the two nuclear receptors. J. Lipid. Res. 2002, 43:2037-2041.
35. McGee S.L., Hargreaves M. Histone modifications and skeletal muscle metabolic gene expression. Clin. Exp. Pharmacol. Physiol. 2010, 37(3):392-396.
36. Mlinar B., et al. Molecular mechanisms of insulin resistance and associated diseases. Clin. Chim. Acta 2007, 375:20-35.
37. Montgomery R.L., et al. Maintenance of cardiac energy metabolism by histone deacetylase 3 in mice. J. Clin. Invest. 2008, 118:3588-3597.
38. Noh H., et al. Histone deacetylase-2 is a key regulator of diabetes- and transforming growth factor-beta1-induced renal injury. Am. J. Physiol. Renal. Physiol. 2009, 297:F729-F739.
39. Obici S., et al. Decreasing hypothalamic insulin receptors causes hyperphagia and insulin resistance in rats. Nat. Neurosci. 2002, 5:566-572.
40. Ohashi R., et al. Reverse cholesterol transport and cholesterol efflux in atherosclerosis. Qjm 2005, 98:845-856.
41. Parthasarathy C., et al. Sex steroids enhance insulin receptors and glucose oxidation in Chang liver cells. Clin. Chim. Acta 2009, 399:49-53.
42. Peet D.J., et al. Cholesterol and bile acid metabolism are impaired in mice lacking the nuclear oxysterol receptor LXR alpha. Cell 1998, 93:693-704.
43. Petruzzelli M., et al. Targeting the liver in the metabolic syndrome: evidence from animal models. Curr. Pharm. Des. 2007, 13:2199-2207.
44. Raymond S.L., Dodds W.J. Characterization of the fawn-hooded rat as a model for hemostatic studies. Thromb. Diath. Haemorrh. 1975, 33:361-369.
45. Razidlo D.F., et al. Histone deacetylase 3 depletion in osteo/chondroprogenitor cells decreases bone density and increases marrow fat. PLoS One 2010, 5:e11492.
46. Reeves P.G., et al. AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. J. Nutr. 1993, 123:1939-1951.
47. Repa J.J., et al. Regulation of mouse sterol regulatory element-binding protein-1c gene (SREBP-1c) by oxysterol receptors, LXRalpha and LXRbeta. Genes Dev. 2000, 14:2819-2830.
48. Rodgers J.T., Puigserver P. Fasting-dependent glucose and lipid metabolic response through hepatic sirtuin 1. Proc. Natl. Acad. Sci. USA 2007, 104:12861-12866.
49. Schoonjans K., et al. PPARalpha and PPARgamma activators direct a distinct tissue-specific transcriptional response via a PPRE in the lipoprotein lipase gene. EMBO J. 1996, 15:5336-5348.
50. Seo J.B., et al. Activated liver X receptors stimulate adipocyte differentiation through induction of peroxisome proliferator-activated receptor gamma expression. Mol. Cell Biol. 2004, 24:3430-3444.
51. Shulman A.I., Mangelsdorf D.J. Retinoid X receptor heterodimers in the metabolic syndrome. N. Engl. J. Med. 2005, 353:604-615.
52. Sonoda J., et al. Nuclear receptors: decoding metabolic disease. FEBS Lett. 2008, 582:2-9.
53. Spiegelman B.M. PPAR-gamma: adipogenic regulator and thiazolidinedione receptor. Diabetes 1998, 47:507-514.
54. Stenbit A.E., et al. GLUT4 heterozygous knockout mice develop muscle insulin resistance and diabetes. Nat. Med. 1997, 3:1096-1101.
55. Sun C., Zhang, et al. SIRT1 improves insulin sensitivity under insulin-resistant conditions by repressing PTP1B. Cell Metab. 2007, 6:307-319.
56. Swift L.L., Farkas M.H., Major A.S., et al. A recycling pathway for resecretion of internalized apolipoprotein E in liver cells. J. Biol. Chem. 2001, 276:22965-22970.
57. Tontonoz P., et al. Stimulation of adipogenesis in fibroblasts by PPAR gamma 2, a lipid-activated transcription factor. Cell 1994, 79:1147-1156.
58. Ulven S.M., et al. LXR is crucial in lipid metabolism. Prostaglandins Leukot Essent Fatty Acids 2005, 73:59-63.
59. Watson R.T., et al. Regulated membrane trafficking of the insulin-responsive glucose transporter 4 in adipocytes. Endocr. Rev. 2004, 25:177-204.
60. Yamamoto H., et al. Sirtuin functions in health and disease. Mol. Endocrinol. 2007, 21:1745-1755.
61. Yang X.J., Gregoire S. Metabolism, cytoskeleton and cellular signalling in the grip of protein Nepsilon- and O-acetylation. EMBO Rep. 2007, 8:556-562.
62. Zhang Y., et al. Peroxisome proliferator-activated receptor-gamma coactivator 1alpha (PGC-1alpha) regulates triglyceride metabolism by activation of the nuclear receptor FXR. Genes Dev. 2004, 18:157-169.
63. Zhang Y., et al. Activation of the nuclear receptor FXR improves hyperglycemia and hyperlipidemia in diabetic mice. Proc. Natl. Acad. Sci. USA 2006, 103:1006-1011.
64. Zhu Y., Li Y. Liver X receptors as potential therapeutic targets in atherosclerosis. Clin. Invest. Med. 2009, 32:E383-E394.