Knockdown of the gene encoding Drosophila tribbles homologue 3 (Trib3) improves insulin sensitivity through peroxisome proliferator-activated receptor-γ (PPAR-γ) activation in a rat model of insulin resistance

Diabetologia

Volumn 54, Issue 4, 2011, Pages 935-944

  Weismann, D ^a,d   Erion, D M ^a   Ignatova Todorava, I ^a   Nagai, Y ^a   Stark, R ^a   Hsiao, J J ^a   Flannery, C ^a   Birkenfeld, A L ^a   May, T ^a   Kahn, M ^a   Zhang, D ^a   Yu, X X ^c   Murray, S F ^c   Bhanot, S ^c   Monia, B P ^c   Cline, G W ^a   Shulman, G I ^a   Samuel, V T ^a,b  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VA CONNECTICUT HEALTHCARE SYSTEM   (United States)

^c ISIS PHARMACEUTICALS   (United States)

^d UNIVERSITY HOSPITAL WÜRZBURG   (Germany)

Author keywords

Antisense oligonucleotide; Euglycaemic hyperinsulinaemic clamp; Insulin sensitivity; PPAR gamma; TRIB3

Indexed keywords

2,2 BIS(4 GLYCIDYLOXYPHENYL)PROPANE; ACYL COENZYME A OXIDASE; ANTISENSE OLIGONUCLEOTIDE; CCAAT ENHANCER BINDING PROTEIN ALPHA; CD36 ANTIGEN; GLUCOSE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA ANTAGONIST; PROTEIN KINASE B BETA; TRIB 3 ANTISENSE OLIGONUCLEOTIDE; UNCLASSIFIED DRUG;

ADIPOSE TISSUE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COMBINATION CHEMOTHERAPY; CONTROLLED STUDY; DIET RESTRICTION; DROSOPHILA; DRUG ACTIVITY; DRUG EFFICACY; ENZYME ACTIVITY; GENE; GENE EXPRESSION; GENE FUNCTION; GENE INACTIVATION; GENE TARGETING; GLUCOSE BLOOD LEVEL; GLUCOSE TRANSPORT; HYPERINSULINEMIA; IN VIVO STUDY; INSULIN RESISTANCE; INSULIN SENSITIVITY; LIVER; MALE; MONOTHERAPY; NONHUMAN; PRIORITY JOURNAL; RAT; SKELETAL MUSCLE; TRIB3 GENE;

ANIMALS; DIABETES MELLITUS, TYPE 2; DISEASE MODELS, ANIMAL; EPOXY COMPOUNDS; GLUCOSE CLAMP TECHNIQUE; IMMUNOBLOTTING; INSULIN RESISTANCE; MALE; OLIGONUCLEOTIDES, ANTISENSE; PPAR GAMMA; PROTEIN KINASES; RATS; RATS, SPRAGUE-DAWLEY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 79953812287     PISSN: 0012186X     EISSN: 14320428     Source Type: Journal    
DOI: 10.1007/s00125-010-1984-5     Document Type: Article

References (43)

1. Shulman GI (2000) Cellular mechanisms of insulin resistance. J Clin Invest 106:171-176
2. Okada T, Kawano Y, Sakakibara T, Hazeki O, Ui M (1994) Essential role of phosphatidylinositol 3-kinase in insulin-induced glucose transport and antilipolysis in rat adipocytes. Studies with a selective inhibitor wortmannin. J Biol Chem 269:3568-3573
3. Taniguchi CM, Emanuelli B, Kahn CR (2006) Critical nodes in signalling pathways: insights into insulin action. Nat Rev Mol Cell Biol 7:85-96 (Pubitemid 43278292)
4. Samuel VT, Liu ZX, Wang A et al (2007) Inhibition of protein kinase Cepsilon prevents hepatic insulin resistance in nonalcoholic fatty liver disease. J Clin Invest 117:739-745 (Pubitemid 46348532)
5. Morino K, Petersen KF, Shulman GI (2006) Molecular mechanisms of insulin resistance in humans and their potential links with mitochondrial dysfunction. Diabetes 55(Suppl 2):S9-S15 (Pubitemid 44927027)
6. Du K, Herzig S, Kulkarni RN, Montminy M (2003) TRB3: a tribbles homolog that inhibits Akt/PKB activation by insulin in liver. Science 300:1574-1577 (Pubitemid 36682889)
7. Matsushima R, Harada N, Webster NJ, Tsutsumi YM, Nakaya Y (2006) Effect of TRB3 on insulin and nutrient-stimulated hepatic p70 S6 kinase activity. J Biol Chem 281:29719-29729 (Pubitemid 44536981)
8. Bi XP, Tan HW, Xing SS et al (2008) Overexpression of TRB3 gene in adipose tissue of rats with high fructose-induced metabolic syndrome. Endocr J 55:747-752
9. He L, Simmen FA, Mehendale HM, Ronis MJ, Badger TM (2006) Chronic ethanol intake impairs insulin signaling in rats by disrupting Akt association with the cell membrane. Role of TRB3 in inhibition of Akt/protein kinase B activation. J Biol Chem 281:11126-11134 (Pubitemid 43855537)
10. Ding J, Kato S, Du K (2008) PI3K activates negative and positive signals to regulate TRB3 expression in hepatic cells. Exp Cell Res 314:1566-1574
11. Liu J, Wu X, Franklin JL et al (2010) Mammalian tribbles homolog 3 impairs insulin action in skeletal muscle: role in glucose-induced insulin resistance. Am J Physiol Endocrinol Metab 298:E565-E576
12. Prudente S, Hribal ML, Flex E et al (2005) The functional Q84R polymorphism of mammalian Tribbles homolog TRB3 is associated with insulin resistance and related cardiovascular risk in Caucasians from Italy. Diabetes 54:2807-2811 (Pubitemid 41233606)
13. Shi Z, Liu J, Guo Q et al (2009) Association of TRB3 gene Q84R polymorphism with type 2 diabetes mellitus in Chinese population. Endocrine 35:414-419
14. Prudente S, Scarpelli D, Chandalia M et al (2009) The TRIB3 Q84R polymorphism and risk of early-onset type 2 diabetes. J Clin Endocrinol Metab 94:190-196
15. Andreozzi F, Formoso G, Prudente S et al (2008) TRIB3 R84 variant is associated with impaired insulin-mediated nitric oxide production in human endothelial cells. Arterioscler Thromb Vasc Biol 28:1355-1360
16. Iynedjian PB (2005) Lack of evidence for a role of TRB3/NIPK as an inhibitor of PKB-mediated insulin signalling in primary hepatocytes. Biochem J 386:113-118
17. Okamoto H, Latres E, Liu R et al (2007) Genetic deletion of Trb3, the mammalian Drosophila tribbles homolog, displays normal hepatic insulin signaling and glucose homeostasis. Diabetes 56:1350-1356 (Pubitemid 46715621)
18. Liew CW, Bochenski J, Kawamori D et al (2010) The pseudokinase tribbles homolog 3 interacts with ATF4 to negatively regulate insulin exocytosis in human and mouse beta cells. J Clin Invest 120:2876-2888
19. Takahashi Y, Ohoka N, Hayashi H, Sato R (2008) TRB3 suppresses adipocyte differentiation by negatively regulating PPARgamma transcriptional activity. J Lipid Res 49:880-892
20. Samuel VT, Beddow SA, Iwasaki T et al (2009) Fasting hyperglycemia is not associated with increased expression of PEPCK or G6Pc in patients with type 2 diabetes. Proc Natl Acad Sci U S A 106:12121-12126
21. Erion DM, Ignatova ID, Yonemitsu S et al (2009) Prevention of hepatic steatosis and hepatic insulin resistance by knock-down of cAMP response element-binding protein. Cell Metab 10:499-506
22. Watts LM, Manchem VP, Leedom TA et al (2005) Reduction of hepatic and adipose tissue glucocorticoid receptor expression with antisense oligonucleotides improves hyperglycemia and hyperlipidemia in diabetic rodents without causing systemic glucocorticoid antagonism. Diabetes 54:1846-1853 (Pubitemid 40770776)
23. Graham MJ, Crooke ST, Monteith DK et al (1998) In vivo distribution and metabolism of a phosphorothioate oligonucleotide within rat liver after intravenous administration. J Pharmacol Exp Ther 286:447-458
24. McKay RA, Miraglia LJ, Cummins LL, Owens SR, Sasmor H, Dean NM (1999) Characterization of a potent and specific class of antisense oligonucleotide inhibitor of human protein kinase C-alpha expression. J Biol Chem 274:1715-1722
25. Neschen S, Morino K, Rossbacher JC et al (2006) Fish oil regulates adiponectin secretion by a peroxisome proliferator-activated receptor-gamma-dependent mechanism in mice. Diabetes 55:924-928 (Pubitemid 44100165)
26. Savage DB, Choi CS, Samuel VT et al (2006) Reversal of diet-induced hepatic steatosis and hepatic insulin resistance by antisense oligonucleotide inhibitors of acetyl-CoA carboxylases 1 and 2. J Clin Invest 116:817-824 (Pubitemid 43326891)
27. Hundal RS, Petersen KF, Mayerson AB et al (2002) Mechanism by which high-dose aspirin improves glucose metabolism in type 2 diabetes. J Clin Invest 109:1321-1326 (Pubitemid 34546896)
28. Neschen S, Moore I, Regittnig W et al (2002) Contrasting effects of fish oil and safflower oil on hepatic peroxisomal and tissue lipid content. Am J Physiol Endocrinol Metab 282:E395-E401 (Pubitemid 34654810)
29. Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911-917
30. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45
31. R Development Core Team (2005) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. ISBN 3-900051-07-0. Available from www.R-project.org
32. Du K, Ding J (2009) Insulin regulates TRB3 and other stress-responsive gene expression through induction of C/EBPbeta. Mol Endocrinol 23:475-485
33. Civitarese AE, Ukropcova B, Carling S et al (2006) Role of adiponectin in human skeletal muscle bioenergetics. Cell Metab 4:75-87 (Pubitemid 43942255)
34. Cheng KK, Iglesias MA, Lam KS et al (2009) APPL1 potentiates insulin-mediated inhibition of hepatic glucose production and alleviates diabetes via Akt activation in mice. Cell Metab 9:417-427
35. Kato S, Du K (2007) TRB3 modulates C2C12 differentiation by interfering with Akt activation. Biochem Biophys Res Commun 353:933-938 (Pubitemid 46080386)
36. Chen R, Kim O, Yang J et al (2001) Regulation of Akt/PKB activation by tyrosine phosphorylation. J Biol Chem 276:31858-31862
37. Rosen ED (2005) The transcriptional basis of adipocyte development. Prostaglandins, Leukot Essent Fatty Acids 73:31-34
38. 3 and C/EBP factors orchestrate adipocyte biology via adjacent binding on a genome-wide scale. Genes & Development 22:2941-2952
39. Bezy O, Vernochet C, Gesta S, Farmer SR, Kahn CR (2007) TRB3 blocks adipocyte differentiation through the inhibition of C/EBPbeta transcriptional activity. Mol Cell Biol 27:6818-6831 (Pubitemid 47483632)
40. Tontonoz P, Spiegelman BM (2008) Fat and beyond: the diverse biology of PPARγ. Annu Rev Biochem 77:289-312
41. Bajaj M, Suraamornkul S, Romanelli A et al (2005) Effect of a sustained reduction in plasma free fatty acid concentration on intramuscular long-chain fatty Acyl-CoAs and insulin action in type 2 diabetic patients. Diabetes 54:3148-3153 (Pubitemid 43334368)
42. Bergeron R, Russell RR 3rd, Young LH et al (1999) Effect of AMPK activation on muscle glucose metabolism in conscious rats. Am J Physiol 276:E938-E944 (Pubitemid 29249614)
43. Wright HM, Clish CB, Mikami T et al (2000) A synthetic antagonist for the peroxisome proliferator-activated receptor γ inhibits adipocyte differentiation. J Biol Chem 275:1873-1877 (Pubitemid 30060811)