Activation of liver X receptors promotes lipid accumulation but does not alter insulin action in human skeletal muscle cells

Diabetologia

Volumn 49, Issue 5, 2006, Pages 990-999

  Cozzone, D ^a   Debard, C ^a   Dif, N ^a   Ricard, N ^a   Disse, E ^a,b   Vouillarmet, J ^a,b   Rabasa Lhoret, R ^a,b   Laville, M ^a,b   Pruneau, D ^c   Rieusset, J ^a   Lefai, E ^a   Vidal, H ^a,d  

^a UNIVERSITÉ LYON 1   (France)

^b Human Nutrition Research Center   (France)

^c Fournier Pharma ^*  (France)

^d INSERM   (France)

Author keywords

Human muscle cells; Insulin action; Lipogenesis; Liver X receptor; SREBP1c promoter; Type 2 diabetes

Indexed keywords

3 [3 [[2 CHLORO 3 (TRIFLUOROMETHYL)BENZYL](2 DIPHENYLETHYL)AMINO]PROPOXY]PHENYLACETIC ACID; ACYL COENZYME A DESATURASE; ACYL COENZYME A DESATURASE 1; ANTIDIABETIC AGENT; FATTY ACID SYNTHASE; GLUCOSE; GLYCOGEN; INSULIN; LIPID; LIVER X RECEPTOR; LIVER X RECEPTOR ALPHA; LIVER X RECEPTOR BETA; MESSENGER RNA; METFORMIN; N (2,2,2 TRIFLUOROETHYL) N [4 [2,2,2 TRIFLUORO 1 HYDROXY 1 (TRIFLUOROMETHOXY)ETHYL]PHENYL]BENZENESULFONAMIDE; PROTEIN KINASE B; STEROL REGULATORY ELEMENT BINDING PROTEIN 1C; SULFONYLUREA; TRIACYLGLYCEROL; UNCLASSIFIED DRUG;

ADULT; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; FEMALE; GLUCOSE UTILIZATION; GLYCOGEN SYNTHESIS; HORMONE ACTION; HUMAN; HUMAN CELL; LIPID METABOLISM; LIPID STORAGE; MALE; NON INSULIN DEPENDENT DIABETES MELLITUS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RECEPTOR UPREGULATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SKELETAL MUSCLE;

ADULT; BLOOD GLUCOSE; DNA-BINDING PROTEINS; FATTY ACIDS, NONESTERIFIED; FEMALE; GLUCOSE; HUMANS; INSULIN; MALE; MIDDLE AGED; MUSCLE, SKELETAL; RECEPTORS, CYTOPLASMIC AND NUCLEAR;

EID: 33646428390     PISSN: 0012186X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00125-006-0140-8     Document Type: Article

References (40)

1. Kelley DE, Mandarino LJ (2000) Fuel selection in human skeletal muscle in insulin resistance: a reexamination. Diabetes 49:677-683
2. Kelley DE, Simoneau JA (1994) Impaired free fatty acid utilization by skeletal muscle in non-insulin-dependent diabetes mellitus. J Clin Invest 94:2349-2356
3. McGarry JD (2002) Banting lecture 2001: dysregulation of fatty acid metabolism in the etiology of type 2 diabetes. Diabetes 51:7-18
4. Shulman GI (2000) Cellular mechanisms of insulin resistance. J Clin Invest 106:171-176
5. Hegarty BD, Furler SM, Ye J, Cooney GJ, Kraegen EW (2003) The role of intramuscular lipid in insulin resistance. Acta Physiol Scand 178:373-383
6. Schultz JR, Tu H, Luk A et al (2000) Role of LXRs in control of lipogenesis. Genes Dev 14:2831-2838
7. Laffitte BA, Chao LC, Li J et al (2003) Activation of liver X receptor improves glucose tolerance through coordinate regulation of glucose metabolism in liver and adipose tissue. Proc Natl Acad Sci USA 100:5419-5424
8. Muscat GE, Wagner BL, Hou J et al (2002) Regulation of cholesterol homeostasis and lipid metabolism in skeletal muscle by liver X receptors. J Biol Chem 277:40722-40728
9. Auboeuf D, Rieusset J, Fajas L et al (1997) Tissue distribution and quantification of the expression of mRNAs of peroxisome proliferator-activated receptors and liver X receptor-alpha in humans: no alteration in adipose tissue of obese and NIDDM patients. Diabetes 46:1319-1327
10. Repa JJ, Liang G, Ou J et al (2000) Regulation of mouse sterol regulatory element-binding protein-1c gene (SREBP-1c) by oxysterol receptors, LXRalpha and LXRbeta. Genes Dev 14:2819-2830
11. Foretz M, Guichard C, Ferre P, Foufelle F (1999) Sterol regulatory element binding protein-1c is a major mediator of insulin action on the hepatic expression of glucokinase and lipogenesis-related genes. Proc Natl Acad Sci USA 96:12737-12742
12. Foufelle F, Ferre P (2002) New perspectives in the regulation of hepatic glycolytic and lipogenic genes by insulin and glucose: a role for the transcription factor sterol regulatory element binding protein-1c. Biochem J 366:377-391
13. Osborne TF (2000) Sterol regulatory element-binding proteins (SREBPs): key regulators of nutritional homeostasis and insulin action. J Biol Chem 275:32379-32382
14. Yoshikawa T, Shimano H, Amemiya-Kudo M et al (2001) Identification of liver X receptor-retinoid X receptor as an activator of the sterol regulatory element-binding protein 1c gene promoter. Mol Cell Biol 21:2991-3000
15. DeBose-Boyd RA, Ou J, Goldstein JL, Brown MS (2001) Expression of sterol regulatory element-binding protein 1c (SREBP-1c) mRNA in rat hepatoma cells requires endogenous LXR ligands. Proc Natl Acad Sci USA 98:1477-1482
16. Ducluzeau PH, Perretti N, Laville M et al (2001) Regulation by insulin of gene expression in human skeletal muscle and adipose tissue. Evidence for specific defects in type 2 diabetes. Diabetes 50:1134-1142
17. Becard D, Hainault I, Azzout-Marniche D, Bertry-Coussot L, Ferre P, Foufelle F (2001) Adenovirus-mediated overexpression of sterol regulatory element binding protein-1c mimics insulin effects on hepatic gene expression and glucose homeostasis in diabetic mice. Diabetes 50:2425-2430
18. Guillet-Deniau I, Mieulet V, Le Lay S et al (2002) Sterol regulatory element binding protein-1c expression and action in rat muscles: insulin-like effects on the control of glycolytic and lipogenic enzymes and UCP3 gene expression. Diabetes 51:1722-1728
19. Kase ET, Wensaas AJ, Aas V (2005) Skeletal muscle lipid accumulation in type 2 diabetes may involve the liver X receptor pathway. Diabetes 54:1108-1115
20. Chisholm JW, Hong J, Mills SA, Lawn RM (2003) The LXR ligand T0901317 induces severe lipogenesis in the db/db diabetic mouse. J Lipid Res 44:2039-2048
21. Chavez JA, Summers SA (2003) Characterizing the effects of saturated fatty acids on insulin signaling and ceramide and diacylglycerol accumulation in 3T3-L1 adipocytes and C2C12 myotubes. Arch Biochem Biophys 419:101-109
22. Laville M, Auboeuf D, Khalfallah Y et al (1996) Acute regulation by insulin of phosphatidylinositol-3-kinase, Rad, Glut 4, and lipoprotein lipase mRNA levels in human muscle. J Clin Invest 98:43-49
23. Bouzakri K, Roques M, Gual P et al (2003) 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 52:1319-1325
24. Rieusset J, Bouzakri K, Chevillotte E et al (2004) Suppressor of cytokine signaling 3 expression and insulin resistance in skeletal muscle of obese and type 2 diabetic patients. Diabetes 53:2232-2241
25. Henry RR, Ciaraldi TP, Abrams-Carter L et al (1996) Glycogen synthase activity is reduced in cultured skeletal muscle cells of non-insulin-dependent diabetes mellitus subjects. Biochemical and molecular mechanisms. J Clin Invest 98:1231-1236
26. Gaster M, Petersen I, Hojlund K, Poulsen P, Beck-Nielsen H (2002) The diabetic phenotype is conserved in myotubes established from diabetic subjects: evidence for primary defects in glucose transport and glycogen synthase activity. Diabetes 51:921-927
27. Chomczynski P, Sacchi N (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162:156-159
28. Debard C, Laville M, Berbe V et al (2004) Expression of key genes of fatty acid oxidation, including adiponectin receptors, in skeletal muscle of type 2 diabetic patients. Diabetologia 47:917-925
29. Zabarovsky ER, Gizatullin R, Podowski RM et al (2000) NotI clones in the analysis of the human genome. Nucleic Acids Res 28:1635-1639
30. Al-Khalili L, Chibalin AV, Kannisto K et al (2003) Insulin action in cultured human skeletal muscle cells during differentiation: assessment of cell surface GLUT4 and GLUT1 content. Cell Mol Life Sci 60:991-998
31. Whitney KD, Watson MA, Goodwin B et al (2001) Liver X receptor (LXR) regulation of the LXRalpha gene in human macrophages. J Biol Chem 276:43509-43515
32. Laffitte BA, Joseph SB, Walczak R et al (2001) Autoregulation of the human liver X receptor alpha promoter. Mol Cell Biol 21:7558-7568
33. Kim JB, Spiegelman BM (1996) ADD1/SREBP1 promotes adipocyte differentiation and gene expression linked to fatty acid metabolism. Genes Dev 10:1096-1107
34. Oh SY, Park SK, Kim JW et al (2003) Acetyl-CoA carboxylase beta gene is regulated by sterol regulatory element-binding protein-1 in liver. J Biol Chem 278:28410-28417
35. Gosmain Y, Lefai E, Ryser S, Roques M, Vidal H (2004) Sterol regulatory element-binding protein-1 mediates the effect of insulin on hexokinase II gene expression in human muscle cells. Diabetes 53:321-329
36. Hegarty BD, Bobard A, Hainault I (2005) Distinct roles of insulin and liver X receptor in the induction and cleavage of sterol regulatory element-binding protein-1c. Proc Natl Acad Sci USA 102:791-796
37. Montell E, Turini M, Marotta M et al (2001) DAG accumulation from saturated fatty acids desensitizes insulin stimulation of glucose uptake in muscle cells. Am J Physiol Endocrinol Metab 280:E229-E237
38. Listenberger LL, Han X, Lewis SE et al (2003) Triglyceride accumulation protects against fatty acid-induced lipotoxicity. Proc Natl Acad Sci USA 100:3077-3082
39. Cao G, Liang Y, Broderick CL et al (2003) Antidiabetic action of a liver x receptor agonist mediated by inhibition of hepatic gluconeogenesis. J Biol Chem 278:1131-1136
40. Bouzakri K, Roques M, Debard C et al (2004) WY-14643 and 9-cis-retinoic acid induce IRS-2/PI 3-kinase signalling pathway and increase glucose transport in human skeletal muscle cells: differential effect in myotubes from healthy subjects and type 2 diabetic patients. Diabetologia 47:1314-1323