Amelioration of lipid-induced insulin resistance in rat skeletal muscle by overexpression of Pgc-1β involves reductions in long-chain acyl-CoA levels and oxidative stress

Diabetologia

Volumn 54, Issue 6, 2011, Pages 1417-1426

  Wright, L E ^a   Brandon, A E ^a   Hoy, A J ^a   Forsberg, G B ^b   Lelliott, C J ^b   Reznick, J ^a,b,c   Lofgren L ^b   Oscarsson, J ^b   Stromstedt M ^b   Cooney, G J ^a,c   Turner, N ^a,c  

^a GARVAN INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b ASTRAZENECA R AND D   (Sweden)

^c UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

Insulin resistance; Lipid metabolism; Mitochondria; Oxidative stress; Pgc 1 ; Skeletal muscle

Indexed keywords

ACYL COENZYME A; MESSENGER RNA; MITOCHONDRIAL DNA; MITOCHONDRIAL PROTEIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1BETA; PPARGC1A PROTEIN, RAT; REACTIVE OXYGEN METABOLITE; RNA BINDING PROTEIN; TRANSCRIPTION FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL FUNCTION; CONTROLLED STUDY; DNA CONTENT; ENZYME ACTIVITY; GENE; GENE OVEREXPRESSION; GLUCOSE TRANSPORT; INSULIN RESISTANCE; INSULIN RESPONSE; LIPID METABOLISM; MALE; MITOCHONDRION; NONHUMAN; OXIDATION; OXIDATIVE STRESS; PGC 1BETA GENE; PRIORITY JOURNAL; RAT; SKELETAL MUSCLE; ANIMAL; FAT INTAKE; METABOLISM; MUSCLE MITOCHONDRION; PHYSIOLOGY; TIME; WISTAR RAT;

ACYL COENZYME A; ANIMALS; DIETARY FATS; INSULIN RESISTANCE; LIPID METABOLISM; MALE; MITOCHONDRIA, MUSCLE; MODELS, ANIMAL; MUSCLE, SKELETAL; OXIDATIVE STRESS; RATS; RATS, WISTAR; REACTIVE OXYGEN SPECIES; RNA-BINDING PROTEINS; TIME FACTORS; TRANSCRIPTION FACTORS;

EID: 80052530278     PISSN: 0012186X     EISSN: 14320428     Source Type: Journal    
DOI: 10.1007/s00125-011-2068-x     Document Type: Article

References (50)

1. Savage DB, Petersen KF, Shulman GI (2007) Disordered lipid metabolism and the pathogenesis of insulin resistance. Physiol Rev 87:507-520 (Pubitemid 47084679)
2. Kraegen EW, Cooney GJ (2008) Free fatty acids and skeletal muscle insulin resistance. Curr Opin Lipidol 19:235-241 (Pubitemid 351653560)
3. Turner N, Heilbronn LK (2008) Is mitochondrial dysfunction a cause of insulin resistance? Trends Endocrinol Metab 19:324-330
4. Turner N, Bruce CR, Beale SM et al (2007) Excess lipid availability increases mitochondrial fatty acid oxidative capacity in muscle: evidence against a role for reduced fatty acid oxidation in lipid-induced insulin resistance in rodents. Diabetes 56:2085-2092 (Pubitemid 47195821)
5. Hancock CR, Han DH, Chen M et al (2008) High-fat diets cause insulin resistance despite an increase in muscle mitochondria. Proc Natl Acad Sci U S A 105(22):7815-7820 (Pubitemid 351872721)
6. Pospisilik JA, Knauf C, Joza N et al (2007) Targeted deletion of AIF decreases mitochondrial oxidative phosphorylation and protects from obesity and diabetes. Cell 131:476-491 (Pubitemid 350017761)
7. Wredenberg A, Freyer C, Sandstrom ME et al (2006) Respiratory chain dysfunction in skeletal muscle does not cause insulin resistance. Biochem Biophys Res Commun 350:202-207 (Pubitemid 44466593)
8. Bruce CR, Hoy AJ, Turner N et al (2009) Overexpression of carnitine palmitoyltransferase-1 in skeletal muscle is sufficient to enhance fatty acid oxidation and improve high fat diet-induced insulin resistance. Diabetes 58:550-558
9. Turner N, Hariharan K, TidAng J et al (2009) Enhancement of muscle mitochondrial oxidative capacity and alterations in insulin action are lipid species dependent: potent tissue-specific effects of medium-chain fatty acids. Diabetes 58:2547-2554
10. Hoehn KL, Salmon AB, Hohnen-Behrens C et al (2009) Insulin resistance is a cellular antioxidant defense mechanism. Proc Natl Acad Sci USA 106:17787-17792
11. Anderson EJ, Lustig ME, Boyle KE et al (2009) Mitochondrial H2O2 emission and cellular redox state link excess fat intake to insulin resistance in both rodents and humans. J Clin Invest. doi:10.1172/JCI37048
12. Houstis N, Rosen ED, Lander ES (2006) Reactive oxygen species have a causal role in multiple forms of insulin resistance. Nature 440:944-948
13. Arany Z (2008) PGC-1 coactivators and skeletal muscle adaptations in health and disease. Curr Opin Genet Dev 18:426-434
14. St-Pierre J, Drori S, Uldry M et al (2006) Suppression of reactive oxygen species and neurodegeneration by the PGC-1 transcriptional coactivators. Cell 127:397-408 (Pubitemid 44572377)
15. St-Pierre J, Lin J, Krauss S et al (2003) Bioenergetic analysis of peroxisome proliferator-activated receptor gamma coactivators 1alpha and 1beta (PGC-1alpha and PGC-1beta) in muscle cells. J Biol Chem 278:26597-26603 (Pubitemid 36876804)
16. Vianna CR, Huntgeburth M, Coppari R et al (2006) Hypomorphic mutation of PGC-1beta causes mitochondrial dysfunction and liver insulin resistance. Cell Metab 4:453-464 (Pubitemid 44817352)
17. Lin J, Wu H, Tarr PT et al (2002) Transcriptional co-activator PGC-1 alpha drives the formation of slow-twitch muscle fibres. Nature 418:797-801
18. Arany Z, Lebrasseur N, Morris C et al (2007) The transcriptional coactivator PGC-1beta drives the formation of oxidative type IIX fibers in skeletal muscle. Cell Metab 5:35-46 (Pubitemid 44939399)
19. Espinoza DO, Boros LG, Crunkhorn S, Gami H, Patti ME (2010) Dual modulation of both lipid oxidation and synthesis by peroxisome proliferator-activated receptor-gamma coactivator- 1alpha and -1beta in cultured myotubes. FASEB J 24:1003-1014
20. Patti ME, Butte AJ, Crunkhorn S et al (2003) Coordinated reduction of genes of oxidative metabolism in humans with insulin resistance and diabetes: Potential role of PGC1 and NRF1. Proc Natl Acad Sci USA 100:8466-8471 (Pubitemid 36842568)
21. Ling C, Poulsen P, Carlsson E et al (2004) Multiple environmental and genetic factors influence skeletal muscle PGC-1alpha and PGC-1beta gene expression in twins. J Clin Invest 114:1518-1526 (Pubitemid 40385582)
22. Handschin C, Choi CS, Chin S et al (2007) Abnormal glucose homeostasis in skeletal muscle-specific PGC-1alpha knockout mice reveals skeletal muscle-pancreatic beta cell crosstalk. J Clin Invest 117:3463-3474 (Pubitemid 350097002)
23. Miura S, Kai Y, Ono M, Ezaki O (2003) Overexpression of peroxisome proliferator-activated receptor gamma coactivator- 1alpha down-regulates GLUT4 mRNA in skeletal muscles. J Biol Chem 278:31385-31390 (Pubitemid 36994659)
24. Choi CS, Befroy DE, Codella R et al (2008) Paradoxical effects of increased expression of PGC-1alpha on muscle mitochondrial function and insulin-stimulated muscle glucose metabolism. Proc Natl Acad Sci USA 105:19926-19931
25. Benton CR, Nickerson JG, Lally J et al (2008) Modest PGC- 1alpha overexpression in muscle in vivo is sufficient to increase insulin sensitivity and palmitate oxidation in subsarcolemmal, not intermyofibrillar, mitochondria. J Biol Chem 283:4228-4240
26. Benton CR, Holloway GP, Han XX et al (2010) Increased levels of peroxisome proliferator-activated receptor gamma, coactivator 1 alpha (PGC-1alpha) improve lipid utilisation, insulin signalling and glucose transport in skeletal muscle of lean and insulin-resistant obese Zucker rats. Diabetologia 53:2008-2019
27. Cleasby ME, Davey JR, Reinten TA et al (2005) Acute bidirectional manipulation of muscle glucose uptake by in vivo electrotransfer of constructs targeting glucose transporter genes. Diabetes 54:2702-2711 (Pubitemid 41233593)
28. Lelliott CJ, Ljungberg A, Ahnmark A et al (2007) Hepatic PGC- 1beta overexpression induces combined hyperlipidemia and modulates the response to PPARalpha activation. Arterioscler Thromb Vasc Biol 27:2707-2713 (Pubitemid 350158926)
29. McMahon JM, Signori E, Wells KE, Fazio VM, Wells DJ (2001) Optimisation of electrotransfer of plasmid into skeletal muscle by pretreatment with hyaluronidase - increased expression with reduced muscle damage. Gene Ther 8:1264-1270 (Pubitemid 32780815)
30. Turner N, Li JY, Gosby A et al (2008) Berberine and its more biologically available derivative, dihydroberberine, inhibit mitochondrial respiratory complex I: a mechanism for the action of berberine to activate AMP-activated protein kinase and improve insulin action. Diabetes 57:1414-1418
31. Folch J, Lees M, Sloane Stanley GH (1957) A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226:497-509
32. Homan R, Anderson MK (1998) Rapid separation and quantitation of combined neutral and polar lipid classes by high-performance liquid chromatography and evaporative light-scattering mass detection. J Chromatogr B Biomed Sci Appl 708:21-26 (Pubitemid 28239884)
33. Ejsing CS, Sampaio JL, Surendranath V et al (2009) Global analysis of the yeast lipidome by quantitative shotgun mass spectrometry. Proc Natl Acad Sci USA 106:2136-2141
34. Antinozzi PA, Segall L, Prentki M, McGarry JD, Newgard CB (1998) Molecular or pharmacologic perturbation of the link between glucose and lipid metabolism is without effect on glucose-stimulated insulin secretion. A re-evaluation of the long-chain acyl-CoA hypothesis. J Biol Chem 273:16146-16154 (Pubitemid 28311386)
35. Flohe L, Gunzler WA (1984) Assays of glutathione peroxidase. Methods Enzymol 105:114-121 (Pubitemid 14165378)
36. Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95:351-358 (Pubitemid 9194347)
37. Wenz T, Rossi SG, Rotundo RL, Spiegelman BM, Moraes CT (2009) Increased muscle PGC-1alpha expression protects from sarcopenia and metabolic disease during aging. Proc Natl Acad Sci USA 106:20405-20410
38. Kamei Y, Ohizumi H, Fujitani Y et al (2003) PPARgamma coactivator 1beta/ERR ligand 1 is an ERR protein ligand, whose expression induces a high-energy expenditure and antagonizes obesity. Proc Natl Acad Sci USA 100:12378-12383 (Pubitemid 37271568)
39. Lelliott CJ, Medina-Gomez G, Petrovic N et al (2006) Ablation of PGC-1beta results in defective mitochondrial activity, thermogenesis, hepatic function, and cardiac performance. PLoS Biol 4:e369
40. Koves TR, Li P, An J et al (2005) Peroxisome proliferator-activated receptor-gamma co-activator 1alpha-mediated metabolic remodeling of skeletal myocytes mimics exercise training and reverses lipid-induced mitochondrial inefficiency. J Biol Chem 280:33588-33598 (Pubitemid 41397160)
41. Holloway GP, Perry CG, Thrush AB et al (2008) PGC-1alpha's relationship with skeletal muscle palmitate oxidation is not present with obesity despite maintained PGC-1alpha and PGC-1beta protein. Am J Physiol Endocrinol Metab 294:E1060-1069
42. Ristow M, Zarse K, Oberbach A et al (2009) Antioxidants prevent health-promoting effects of physical exercise in humans. Proc Natl Acad Sci USA 106:8665-8670
43. Hernandez-Alvarez MI, Chiellini C, Manco M et al (2009) Genes involved in mitochondrial biogenesis/function are induced in response to bilio-pancreatic diversion in morbidly obese individuals with normal glucose tolerance but not in type 2 diabetic patients. Diabetologia 52:1618-1627
44. Oita RC, Mazzatti DJ, Lim FL, Powell JR, Merry BJ (2009) Whole-genome microarray analysis identifies up-regulation of Nr4a nuclear receptors in muscle and liver from diet-restricted rats. Mech Ageing Dev 130:240-247
45. Frier BC, Williams DB, Wright DC (2009) The effects of apelin treatment on skeletal muscle mitochondrial content. Am J Physiol Regul Integr Comp Physiol 297:R1761-1768
46. Ellis BA, Poynten A, Lowy AJ et al (2000) Long-chain acyl-CoA esters as indicators of lipid metabolism and insulin sensitivity in rat and human muscle. Am J Physiol Endocrinol Metab 279:E554-560
47. Hoy AJ, Brandon AE, Turner N et al (2009) Lipid and insulin infusion-induced skeletal muscle insulin resistance is likely due to metabolic feedback and not changes in IRS-1, Akt, or AS160 phosphorylation. Am J Physiol Endocrinol Metab 297:E67-75
48. Tsintzas K, Chokkalingam K, Jewell K, Norton L, Macdonald IA, Constantin-Teodosiu D (2007) Elevated free fatty acids attenuate the insulin-induced suppression of PDK4 gene expression in human skeletal muscle: potential role of intramuscular long-chain acyl-coenzyme A. J Clin Endocrinol Metab 92:3967-3972 (Pubitemid 47607648)
49. Thompson AL, Cooney GJ (2000) Acyl-CoA inhibition of hexokinase in rat and human skeletal muscle is a potential mechanism of lipid-induced insulin resistance. Diabetes 49:1761-1765
50. Loh K, Deng H, Fukushima A et al (2009) Reactive oxygen species enhance insulin sensitivity. Cell Metab 10:260-272