Acute inhibition of fatty acid import inhibits GLUT4 transcription in adipose tissue, but not skeletal or cardiac muscle tissue, partly through Liver X Receptor (LXR) signaling

Diabetes

Volumn 59, Issue 4, 2010, Pages 800-807

  Griesel, Beth A ^a   Weems, Juston ^a   Russell, Robert A ^a   Dale Abel, E ^b   Humphries, Kenneth ^a   Olson, Ann Louise ^a  

^a UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHLORAMPHENICOL ACETYLTRANSFERASE; ETOMOXIR; GLUCOSE TRANSPORTER 4; LIGAND; LIVER X RECEPTOR; LONG CHAIN FATTY ACID; MESSENGER RNA; N (2,2,2 TRIFLUOROETHYL) N [4 (2,2,2 TRIFLUORO 1 HYDROXY 1 TRIFLUOROMETHYLETHYL)PHENYL]BENZENESULFONAMIDE;

ADIPOSE TISSUE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BINDING SITE; DOWN REGULATION; FATTY ACID TRANSPORT; FEMALE; GENE EXPRESSION; GENE EXPRESSION REGULATION; GLUCOSE TRANSPORT; HEART MUSCLE; MALE; MITOCHONDRION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR BINDING; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; TRANSCRIPTION REGULATION; TRANSGENIC MOUSE;

ADIPOSE TISSUE; ANIMALS; CHLORAMPHENICOL O-ACETYLTRANSFERASE; DNA PRIMERS; EPOXY COMPOUNDS; GLUCOSE TRANSPORTER TYPE 4; HUMANS; HYPOGLYCEMIC AGENTS; INSULIN; MICE; MICE, TRANSGENIC; MITOCHONDRIA, HEART; MITOCHONDRIA, LIVER; MITOCHONDRIA, MUSCLE; ORGAN SPECIFICITY; PROMOTER REGIONS, GENETIC;

EID: 77951173235     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db09-1542     Document Type: Article

References (48)

1. Tsao TS, Burcelin R, Katz EB, Huang L, Charron MJ. Enhanced insulin action due to targeted GLUT4 overexpression exclusively in muscle. Diabetes 1996;45:28-36 (Pubitemid 26010419)
2. Treadway JL, Hargrove DM, Nardone NA, McPherson RK, Russo JF, Milici AJ, Stukenbrok HA, Gibbs EM, Stevenson RW, Pessin JE. Enhanced peripheral glucose utilization in transgenic mice expressing the human GLUT4 gene. J Biol Chem 1994;269:29956-29961
3. Shepherd PR, Gnudi L, Tozzo E, Yang H, Leach F, Kahn BB. Adipose cell hyperplasia and enhanced glucose disposal in transgenic mice overexpressing GLUT4 selectively in adipose tissue. J Biol Chem 1993;268:22243-22246 (Pubitemid 23318260)
4. Liu ML, Gibbs EM, McCoid SC, Milici AJ, Stukenbrok HA, McPherson RK, Treadway JL, Pessin JE. Transgenic mice expressing the human GLUT4/muscle-fat facilitative glucose transporter protein exhibit efficient glycemic control. Proc Natl Acad Sci U S A 1993;90:11346-11350 (Pubitemid 23354426)
5. Katz EB, Stenbit AE, Hatton K, DePinho R, Charron MJ. Cardiac and adipose tissue abnormalities but not diabetes in mice deficient in GLUT4. Nature 1995;377:151-155
6. Stenbit AE, Tsao TS, Li J, Burcelin R, Geenen DL, Factor SM, Houseknecht K, Katz EB, Charron MJ. GLUT4 heterozygous knockout mice develop muscle insulin resistance and diabetes. Nat Med 1997;3:1096-1101
7. Olson AL. Regulated of GLUT4 transcription and gene expression. Curr Med Chem Immun Endoc Metab Agents 2005;5:219-225
8. Olson AL, Knight JB. Regulation of GLUT4 expression in vivo and in vitro. Front Biosci 2003;8:s401-s409
9. Richardson JM, Balon TW, Treadway JL, Pessin JE. Differential regulation of glucose transporter activity and expression in red and white skeletal muscle. J Biol Chem 1991;266:12690-12694
10. Charron MJ, Kahn BB. Divergent molecular mechanisms for insulin-resistant glucose transport in muscle and adipose cells in vivo. J Biol Chem 1990;265:7994-8000
11. Gerrits PM, Olson AL, Pessin JE. Regulation of the GLUT4/muscle-fat glucose transporter mRNA in adipose tissue of insulin-deficient diabetic rats. J Biol Chem 1993;268:640-644
12. Neufer PD, Carey JO, Dohm GL. Transcriptional regulation of the gene for glucose transporter GLUT4 in skeletal muscle: effects of diabetes and fasting. J Biol Chem 1993;268:13824-13829
13. Foley JE. Rationale and application of fatty acid oxidation inhibitors in treatment of diabetes mellitus. Diabetes Care 1992;15:773-784
14. Hübinger A, Knode O, Susanto F, Reinauer H, Gries FA. Effects of the carnitine-acyltransferase inhibitor etomoxir on insulin sensitivity, energy expenditure and substrate oxidation in NIDDM. Horm Metab Res 1997;29:436-439
15. Rafaeloff R, Patel R, Yip C, Goldfine ID, Hawley DM. Mutation of the high cysteine region of the human insulin receptor alpha-subunit increases insulin receptor binding affinity and transmembrane signaling. J Biol Chem 1989;264:15900-15904
16. Thai MV, Guruswamy S, Cao KT, Pessin JE, Olson AL. Myocyte enhancer factor 2 (MEF2)-binding site is required for GLUT4 gene expression in transgenic mice: regulation of MEF2 DNA binding activity in insulin-deficient diabetes. J Biol Chem 1998;273:14285-14292
17. Dalen KT, Ulven SM, Bamberg K, Gustafsson JA, Nebb HI. Expression of the insulin-responsive glucose transporter GLUT4 in adipocytes is dependent on liver X receptor alpha. J Biol Chem 2003;278:48283-48291
18. Belke DD, Betuing S, Tuttle MJ, Graveleau C, Young ME, Pham M, Zhang D, Cooksey RC, McClain DA, Litwin SE, Taegtmeyer H, Severson D, Kahn CR, Abel ED. Insulin signaling coordinately regulates cardiac size, metabolism, and contractile protein isoform expression. J Clin Invest 2002;109:629-639
19. Olson AL, Pessin JE. Transcriptional regulation of the human GLUT4 promoter in diabetic transgenic mice. J Biol Chem 1995;270:23491-23495
20. Eyster CA, Duggins QS, Olson AL. Expression of constitutively actin Akt/protein kinase B signals GLUT4 translocation in the absence of an intact actin cytoskeleton. J Biol Chem 2005;280:17978-17985
21. Sparling DP, Griesel BA, Weems J, Olson AL. GLUT4 enhancer factor (GEF) interacts with MEF2A and HDAC5 to regulate the GLUT4 promoter in adipocytes. J Biol Chem 2008;283:7429-7437
22. Kelley DE, Mandarino LJ. Fuel selection in human skeletal muscle in insulin resistance: a reexamination. Diabetes 2000;49:677-683
23. Koves TR, Ussher JR, Noland RC, Slentz D, Mosedale M, Ilkayeva O, Bain J, Stevens R, Dyck JR, Newgard CB, Lopaschuk GD, Muoio DM. Mitochondrial overload and incomplete fatty acid oxidation contribute to skeletal muscle insulin resistance. Cell Metab 2008;7:45-56
24. Kiorpes TC, Hoerr D, Ho W, Weaner LE, Inman MG, Tutwiler GF. Identification of 2-tetradecylglycidyl coenzyme A as the active form of methyl 2-tetradecylglycidate (methyl palmoxirate) and its characterization as an irreversible, active site-directed inhibitor of carnitine palmitoyltransferase A in isolated rat liver mitochondria. J Biol Chem 1984;259:9750-9755
25. Morillas M, Clotet J, Rubí B, Serra D, Ariño J, Hegardt FG, Asins G. Inhibition by etomoxir of rat liver carnitine octanoyltransferase is produced through the co-ordinate interaction with two histidine residues. Biochem J 2000;351:495-502
26. Blüher M, Michael MD, Peroni OD, Ueki K, Carter N, Kahn BB, Kahn CR. Adipose tissue selective insulin receptor knockout protects against obesity and obesity-related glucose intolerance. Dev Cell 2002;3:25-38
27. Brüning JC, Michael MD, Winnay JN, Hayashi T, Hörsch D, Accili D, Goodyear LJ, Kahn CR. A muscle-specific insulin receptor knockout exhibits features of the metabolic syndrome of NIDDM without altering glucose tolerance. Mol Cell 1998;2:559-569
28. Kalaany NY, Gauthier KC, Zavacki AM, Mammen PP, Kitazume T, Peterson JA, Horton JD, Garry DJ, Bianco AC, Mangelsdorf DJ. LXRs regulate the balance between fat storage and oxidation. Cell Metab 2005;1:231-244
29. Chibalin AV, Leng Y, Vieira E, Krook A, Björnholm M, Long YC, Kotova O, Zhong Z, Sakane F, Steiler T, Nylén C, Wang J, Laakso M, Topham MK, Gilbert M, Wallberg-Henriksson H, Zierath JR. Downregulation of diacylglycerol kinase delta contributes to hyperglycmia-induced insulin resistance. Cell 2008;132:375-386
30. Holland WL, Brozinick JT, Wang LP, Hawkins ED, Sargent KM, Liu Y, Narra K, Hoehn KL, Knotts TA, Siesky A, Nelson DH, Karathanasis SK, Fontenot GK, Birnbaum MJ, Summers SA. Inhibition of ceramide synthesis amelio-rates glucocorticoid-, saturated-fat-, and obesity-induced insulin resistance. Cell Metab 2007;5:167-179
31. Dobbins RL, Szczepaniak LS, Bentley B, Esser V, Myhill J, McGarry JD. Prolonged inhibition of muscle carnitine palmitoyltransferase-1 promotes intramyocellular lipid accumulation and insulin resistance in rats. Diabetes 2001;50:123-130
32. Yagyu H, Chen G, Yokoyama M, Hirata K, Augustus A, Kako Y, Seo T, Hu Y, Lutz EP, Merkel M, Bensadoun A, Homma S, Goldberg IJ. Lipoprotein lipase (LpL) on the surface of cardiomyocytes increases lipid uptake and produces cardiomyopathy. J Clin Invest 2003;111:419-426
33. Garvey WT, Maianu L, Huecksteadt TP, Birnbaum MJ, Molina JM, Ciaraldi TP. Pretranslational suppression of a glucose transporter protein causes insulin restistance in adipocytes from patients with non-insulin-dependent diabetes mellitus and obesity. J Clin Invest 1991;87:1072-1081
34. Sivitz WI, DeSautel SL, Kayano T, Bell GI, Pessin JE. Regulation of glucose transporter messenger RNA levels in insulin-deficient states. Nature 1989;340:72-74
35. Carlson CJ, Koterski S, Sciotti RJ, Poccard GB, Rondinone CM. Enhanced basal activation of mitogen-activated protein kinases in adipocytes form type 2 diabetes: potential role of p38 in the downregulation of GLUT4 expression. Diabetes 2003;52:634-641
36. Sivitz WI, DeSautel SL, Kayano T, Bell GI, Pessin JE. Regulation of glucose transporter messenger RNA levels in rat adipose tissue by insulin. Mol Endocrinol 1990;4:583-588
37. Nurjhan N, Consoli A, Gerich J. Increased lipolysis and its consequences on gluconeogenesis in non-insulin-dependent diabetes mellitus. J Clin Invest 1992;89:169-175
38. Kelley DE, Goodpaster B, Wing RR, Simoneau JA. Skeletal muscle fatty acid metabolism in association with insulin resistance, obesity, and weight loss. Am J Physiol 1999;277:E1130-E1141
39. Ranalletta M, Jiang H, Li J, Tsao TS, Stenbit AE, Yokoyama M, Katz EB, Charron MJ. Altered hepatic and muscle substrate utilization provoked by GLUT4 ablation. Diabetes 2005;54:935-943
40. Ranalletta M, Du XQ, Seki Y, Glenn AS, Kruse M, Fiallo A, Estrada I, Tsao TS, Stenbit AE, Katz EB, Charron MJ. Hepatic response to restoration of GLUT4 in skeletal muscle of GLUT4 null mice. Am J Physiol Endocrinol Metabol 2007;293:E1178-E1187
41. Gaidhu MP, Fediuc S, Ceddia RB. 5-Aminoimidazole-4-carboxamide-1-beta-D ribofuranoside-induced AMP-activated protein kinase phosphorylation inhibits basal and insulin-stimulated glucose uptake, lipid synthesis, and fatty acid oxidation in isolated rat adipocytes. J Biol Chem 2006;281:25956-25964
42. Krämer DK, Al-Khalili L, Guigas B, Leng Y, Garcia-Roves PM, Krook A. Role of AMP kinase and PPARdelta in the regulation of lipid and glucose metabolism in human skeletal muscle. J Biol Chem 2007;282:19313-19320
43. McGee SL, van Denderen BJ, Howlett KF, Mollica J, Schertzer JD, Kemp BE, Hargreaves M. AMP-activated protein kinase regulates GLUT4 transcription by phosphorylating histone deacetylase 5. Diabetes 2008;57:860-867
44. Murgia M, Jensen TE, Cusinato M, Garcia M, Richter EA, Schiaffino S. Multiple signalling pathways redundantly control glucose transporter GLUT4 gene transcription in skeletal muscle. J Physiol 2009;587:4319-4327
45. Mitro N, Mak PA, Vargas L, Godio C, Hampton E, Molteni V, Kreusch A, Saez E. The nuclear receptor LXR is a glucose sensor. Nature 2007;445:219-223
46. Sponarova J, Mustard KJ, Horakova O, Flachs P, Rossmeisl M, Brauner P, Bardova K, Thomason-Hughes M, Braunerova R, Janovska P, Hardie DG, Kopecky J. Involvement of AMP-activated protein kinase in fat depot-specific metabolic changes during starvation. FEBS Lett 2005;579:6105-6110
47. Yang J, Craddock L, Hong S, Liu ZM. AMP-activated protein kinase suppresses LXR-dependent sterol regulatory element-binding protein-1c transcription in rat hepatoma McA-RH7777 cells. J Cell Biochem 2009;106:414-426
48. Laffitte BA, Chao LC, Li J, Walczak R, Hummasti S, Joseph SB, Castrillo A, Wilpitz DC, Mangelsdorf DJ, Collins JL, Saez E, Tontonoz P. Activation of liver X receptor improves glucose tolerance through coordinate regulation of glucose metabolism in liver and adipose tissue. Proc Natl Acad Sci U S A 2003;100:5419-5424