Effect of short-term free fatty acids elevation on mitochondrial function in skeletal muscle of healthy individuals

Journal of Clinical Endocrinology and Metabolism

Volumn 95, Issue 1, 2010, Pages 422-429

  Chavez, Alberto O ^a   Kamath, Subhash ^a   Jani, Rucha ^a   Sharma, Lokendra K ^b   Monroy, Adriana ^a   Abdul Ghani, Muhammad A ^a   Centonze, Victoria E ^b   Sathyanarayana, Padma ^a   Coletta, Dawn K ^a   Jenkinson, Cristopher P ^a   Bai, Yidong ^b   Folli, Franco ^a   DeFronzo, Ralph A ^a   Tripathy, Devjit ^a  

^a Mays Cancer Center at UT Health San Antonio   (United States)

^b UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; CITRATE SYNTHASE; CYTOCHROME B; CYTOCHROME C OXIDASE; CYTOCHROME C OXIDASE 2; FATTY ACID; GLUCOSE; INSULIN; MESSENGER RNA; MITOCHONDRIAL DNA; MITOCHONDRIAL PROTEIN; MITOFILIN 1; MITOFUSIN 1; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1BETA; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE 8; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE 3; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE 5; RNA; UNCLASSIFIED DRUG; UNCOUPLING PROTEIN 2; UNCOUPLING PROTEIN 3;

ADULT; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; FATTY ACID BLOOD LEVEL; FEMALE; GENE EXPRESSION; GLUCOSE TOLERANCE; GLUCOSE TRANSPORT; HORMONE ACTION; HUMAN; HUMAN EXPERIMENT; HUMAN TISSUE; INSULIN BLOOD LEVEL; INSULIN RESISTANCE; LEAN BODY WEIGHT; MALE; MITOCHONDRIAL MEMBRANE POTENTIAL; MUSCLE BIOPSY; MUSCLE MITOCHONDRION; NORMAL HUMAN; PRIORITY JOURNAL; SKELETAL MUSCLE; VASTUS LATERALIS MUSCLE;

EID: 75149159121     PISSN: 0021972X     EISSN: 0021972X     Source Type: Journal    
DOI: 10.1210/jc.2009-1387     Document Type: Article

References (40)

1. DeFronzo RA 2004 Pathogenesis of type 2 diabetes mellitus. Med Clin North Am 88:787-835, ix
2. Tripathy D, Eriksson KF, Orho-Melander M, Fredriksson J, Ahlqvist G, Groop L 2004 Parallel manifestation of insulin resistance and β-cell decompensation is compatible with a common defect in type 2 diabetes. Diabetologia 47:782-793
3. Belfort R, Mandarino L, Kashyap S, Wirfel K, Pratipanawatr T, Berria R, Defronzo RA, Cusi K 2005 Dose-response effect of elevated plasma free fatty acid on insulin signaling. Diabetes 54:1640-1648
4. Dresner A, Laurent D, Marcucci M, Griffin ME, Dufour S, Cline GW, Slezak LA, Andersen DK, Hundal RS, Rothman DL, Petersen KF, Shulman GI 1999 Effects of free fatty acids on glucose transport and IRS-1-associated phosphatidylinositol 3-kinase activity. J Clin Invest 103:253-259
5. 1HNMR spectroscopy study. Diabetologia 42:113-116
6. Roden M, Price TB, Perseghin G, Petersen KF, Rothman DL, Cline GW, Shulman GI 1996 Mechanism of free fatty acid-induced insulin resistance in humans. J Clin Invest 97:2859-2865
7. DeFronzo RA 1988 Lilly lecture 1987. The triumvirate: β-cell, muscle, liver. A collusion responsible for NIDDM. Diabetes 37:667-687
8. Ukropcova B, Sereda O, de Jonge L, Bogacka I, Nguyen T, Xie H, Bray GA, Smith SR 2007 Family history of diabetes links impaired substrate switching and reduced mitochondrial content in skeletal muscle. Diabetes 56:720-727
9. Kelley DE, He J, Menshikova EV, Ritov VB 2002 Dysfunction of mitochondria in human skeletal muscle in type 2 diabetes. Diabetes 51:2944-2950
10. Petersen KF, Dufour S, Befroy D, Garcia R, Shulman GI 2004 Impaired mitochondrial activity in the insulin-resistant offspring of patients with type 2 diabetes. N Engl J Med 350:664-671
11. Asmann YW, Stump CS, Short KR, Coenen-Schimke JM, Guo Z, Bigelow ML, Nair KS 2006 Skeletal muscle mitochondrial functions, mitochondrial DNA copy numbers, and gene transcript profiles in type 2 diabetic and nondiabetic subjects at equal levels of low or high insulin and euglycemia. Diabetes 55:3309-3319
12. Ritov VB, Menshikova EV, He J, Ferrell RE, Goodpaster BH, Kelley DE 2005 Deficiency of subsarcolemmal mitochondria in obesity and type 2 diabetes. Diabetes 54:8-14
13. Mootha VK, Lindgren CM, Eriksson KF, Subramanian A, Sihag S, Lehar J, Puigserver P, Carlsson E, Ridderstråle M, Laurila E, Houstis N, Daly MJ, Patterson N, Mesirov JP, Golub TR, Tamayo P, Spiegelman B, Lander ES, Hirschhorn JN, Altshuler D, Groop LC 2003 PGC-1α-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nature genetics 34:267-273
14. Patti ME, Butte AJ, Crunkhorn S, Cusi K, Berria R, Kashyap S, Miyazaki Y, Kohane I, Costello M, Saccone R, Landaker EJ, Goldfine AB, Mun E, DeFronzo R, Finlayson J, Kahn CR, Mandarino LJ 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
15. Szendroedi J, Schmid AI, Chmelik M, Toth C, Brehm A, Krssak M, Nowotny P, Wolzt M, Waldhausl W, Roden M 2007 Muscle mitochondrial ATP synthesis and glucose transport/phosphorylation in type 2 diabetes. PLoS Med 4:e154
16. Richardson DK, Kashyap S, Bajaj M, Cusi K, Mandarino SJ, Finlayson J, DeFronzo RA, Jenkinson CP, Mandarino LJ 2005 Lipid infusion decreases the expression of nuclear encoded mitochondrial genes and increases the expression of extracellular matrix genes in human skeletal muscle. J Biol Chem 280:10290-10297
17. Brehm A, Krssak M, Schmid AI, Nowotny P, Waldhäusl W, Roden M 2006 Increased lipid availability impairs insulin-stimulated ATP synthesis in human skeletal muscle. Diabetes 55:136-140
18. Brand MD, Reynafarje B, Lehninger AL 1976 Stoichiometric relationship between energy-dependent proton ejection and electron transport in mitochondria. Proc Natl Acad Sci USA 73:437-441
19. Scaduto Jr RC, Grotyohann LW 1999 Measurement of mitochondrial membrane potential using fluorescent rhodamine derivatives. Biophys J 76:469-477
20. Groop LC, Bonadonna RC, DelPrato S, Ratheiser K, Zyck K, Ferrannini E, DeFronzo RA 1989 Glucose and free fatty acid metabolism in non-insulin-dependent diabetes mellitus. Evidence for multiple sites of insulin resistance. J Clin Invest 84:205-213
21. Lemasters JJ, Chacon E, Ohata H, Harper IS, Nieminen AL, Tesfai SA, Herman B 1995 Measurement of electrical potential, pH, and free calcium ion concentration in mitochondria of living cells by laser scanning confocal microscopy. Methods Enzymol 260:428-444
22. Manfredi G, Spinazzola A, Checcarelli N, Naini A 2001 Assay of mitochondrial ATP synthesis in animal cells. Methods Cell Biol 65:133-145
23. Srere PA 1968 Studies on purified citrate-enzymes: metabolic interpretations. Biochem Soc Symp 27:11-21
24. Sparks LM, Xie H, Koza RA, Mynatt R, Hulver MW, Bray GA, Smith SR 2005 A high-fat diet coordinately downregulates genes required for mitochondrial oxidative phosphorylation in skeletal muscle. Diabetes 54:1926-1933
25. Simonson DC, DeFronzo RA 1990 Indirect calorimetry: methodological and interpretative problems. Am J Physiol 258:E399-E412
26. Halliwell B 1999 Antioxidant defence mechanisms: from the beginning to the end (of the beginning). Free Radic Res 31:261-272
27. Cooke MS, Evans MD, Dizdaroglu M, Lunec J 2003 Oxidative DNA damage: mechanisms, mutation, and disease. FASEB J 17:1195-1214
28. 2+-independent permeabilization of the inner mitochondrial membrane by peroxynitrite is mediated by membrane protein thiol cross-linking and lipid peroxidation. Arch Biochem Biophys 345:243-250
29. Rachek LI, Musiyenko SI, LeDoux SP, Wilson GL 2007 Palmitate induced mitochondrial deoxyribonucleic acid damage and apoptosis in l6 rat skeletal muscle cells. Endocrinology 148:293-299
30. Tripathy D, Mohanty P, Dhindsa S, Syed T, Ghanim H, Aljada A, Dandona P 2003 Elevation of free fatty acids induces inflammation and impairs vascular reactivity in healthy subjects. Diabetes 52:2882-2887
31. Khalfallah Y, Fages S, Laville M, Langin D, Vidal H 2000 Regulation of uncoupling protein-2 and uncoupling protein-3 mRNA expression during lipid infusion in human skeletal muscle and subcutaneous adipose tissue. Diabetes 49:25-31
32. Echtay KS, Roussel D, St-Pierre J, Jekabsons MB, Cadenas S, Stuart JA, Harper JA, Roebuck SJ, Morrison A, Pickering S, Clapham JC, Brand MD 2002 Superoxide activates mitochondrial uncoupling proteins. Nature 415:96-99
33. Abdul-Ghani MA, Muller FL, Liu Y, Chavez AO, Balas B, Zuo P, Chang Z, Tripathy D, Jani R, Molina-Carrion M, Monroy A, Folli F, Van Remmen H, DeFronzo RA 2008 Deleterious action of FA metabolites on ATP synthesis: possible link between lipotoxicity, mitochondrial dysfunction, and insulin resistance. Am J Physiol Endocrinol Metab 295:E678-E685
34. Pospisilik JA, Knauf C, Joza N, Benit P, Orthofer M, Cani PD, Ebersberger I, Nakashima T, Sarao R, Neely G, Esterbauer H, Kozlov A, Kahn CR, Kroemer G, Rustin P, Burcelin R, Penninger JM 2007 Targeted deletion of AIF decreases mitochondrial oxidative phosphorylation and protects from obesity and diabetes. Cell 131:476-491
35. Choi CS, Befroy DE, Codella R, Kim S, Reznick RM, Hwang YJ, Liu ZX, Lee HY, Distefano A, Samuel VT, Zhang D, Cline GW, Handschin C, Lin J, Petersen KF, Spiegelman BM, Shulman GI 2008 Paradoxical effects of increased expression of PGC-1α on muscle mitochondrial function and insulin-stimulated muscle glucose metabolism. Proc Natl Acad Sci USA 105:19926-19931
36. Lelliott CJ, Medina-Gomez G, Petrovic N, Kis A, Feldmann HM, Bjursell M, Parker N, Curtis K, Campbell M, Hu P, Zhang D, Litwin SE, Zaha VG, Fountain KT, Boudina S, Jimenez-Linan M, Blount M, Lopez M, Meirhaeghe A, Bohlooly-Y M, Storlien L, Strömstedt M, Snaith M, Oresic M, Abel ED, Cannon B, Vidal-Puig A 2006 Ablation of PGC-1β results in defective mitochondrial activity, thermogenesis, hepatic function, and cardiac performance. PLoS Biol 4:e369
37. Vianna CR, Huntgeburth M, Coppari R, Choi CS, Lin J, Krauss S, Barbatelli G, Tzameli I, Kim YB, Cinti S, Shulman GI, Spiegelman BM, Lowell BB 2006 Hypomorphic mutation of PGC-1β causes mitochondrial dysfunction and liver insulin resistance. Cell Metab 4:453-464
38. Stump CS, Short KR, Bigelow ML, Schimke JM, Nair KS 2003 Effect of insulin on human skeletal muscle mitochondrial ATP production, protein synthesis, and mRNA transcripts. Proc Natl Acad Sci USA 100:7996-8001
39. Coletta DK, Balas B, Chavez AO, Baig M, Abdul-Ghani M, Kashyap SR, Folli F, Tripathy D, Mandarino LJ, Cornell JE, Defronzo RA, Jenkinson CP 2008 Effect of acute physiological hyperinsulinemia on gene expression in human skeletal muscle in vivo. Am J Physiol Endocrinol Metab 294:E910-E917
40. Holloszy JO 2009 Skeletal muscle "mitochondrial deficiency" does not mediate insulin resistance. Am J Clin Nutr 89:463S-466S