Targeting of mitochondrial reactive oxygen species production does not avert lipid-induced insulin resistance in muscle tissue from mice

Diabetologia

Volumn 55, Issue 10, 2012, Pages 2759-2768

  Paglialunga, S ^a   Van Bree, B ^a   Bosma, M ^a   Valdecantos, M P ^b   Amengual Cladera, E ^c   Jorgensen J A ^a   Van Beurden, D ^a   Den Hartog, G J M ^a   Ouwens, D M ^d   Briede J J ^e   Schrauwen, P ^a   Hoeks, J ^a  

^a MAASTRICHT UNIVERSITY MEDICAL CENTER   (Netherlands)

^b UNIVERSITY OF NAVARRA   (Spain)

^c Instituto de Salud Carlos III   (Spain)

^d LEIBNIZ CENTER FOR DIABETES RESEARCH AT HEINRICH HEINE UNIVERSITY DÜSSELDORF   (Germany)

^e MAASTRICHT UNIVERSITY   (Netherlands)

Author keywords

Antioxidant treatment; High fat high sucrose diet; Insulin resistance; Oxidative stress; Reactive oxygen species; SkQ

Indexed keywords

ANTIOXIDANT; INSULIN; LIPID; PLASTOQUINONE DECYLTRIPHENYLPHOSPHONIUM; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL STIMULATION; CONTROLLED STUDY; GLUCOSE TOLERANCE TEST; GLUCOSE TRANSPORT; INSULIN RESISTANCE; INSULIN SENSITIVITY; LIPID DIET; LOW FAT DIET; MALE; MITOCHONDRIAL RESPIRATION; MUSCLE CELL; MUSCLE MITOCHONDRION; MUSCLE TISSUE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN CARBONYLATION; RAT; RESPIROMETRY; SIGNAL TRANSDUCTION; TARGET CELL;

ANIMALS; DIETARY FATS; FREE RADICAL SCAVENGERS; GLUCOSE; INSULIN; INSULIN RESISTANCE; LIPIDS; MALE; MICE; MICE, INBRED C57BL; MITOCHONDRIA, MUSCLE; MODELS, ANIMAL; MUSCLE, SKELETAL; OXIDATIVE STRESS; PLASTOQUINONE; REACTIVE OXYGEN SPECIES;

EID: 84866107987     PISSN: 0012186X     EISSN: 14320428     Source Type: Journal    
DOI: 10.1007/s00125-012-2626-x     Document Type: Article

References (48)

1. 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 119:573-581
2. Lefort N, Glancy B, Bowen B et al (2010) Increased reactive oxygen species production and lower abundance of complex I subunits and carnitine palmitoyltransferase 1B protein despite normal mitochondrial respiration in insulin-resistant human skeletal muscle. Diabetes 59:2444-2452
3. Haber CA, Lam TK, Yu Z et al (2003) N-acetylcysteine and taurine prevent hyperglycemia-induced insulin resistance in vivo: possible role of oxidative stress. Am J Physiol Endocrinol Metab 285:E744-E753
4. Houstis N, Rosen ED, Lander ES (2006) Reactive oxygen species have a causal role in multiple forms of insulin resistance. Nature 440:944-948
5. Lee HY, Choi CS, Birkenfeld AL et al (2010) Targeted expression of catalase to mitochondria prevents age-associated reductions in mitochondrial function and insulin resistance. Cell Metab 12:668-674
6. Kelley DE, He J, Menshikova EV, Ritov VB (2002) Dysfunction of mitochondria in human skeletal muscle in type 2 diabetes. Diabetes 51:2944-2950
7. 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 (Pubitemid 38364625)
8. Schrauwen-Hinderling VB, Kooi ME, Hesselink MK et al (2007) Impaired in vivo mitochondrial function but similar intramyocellular lipid content in patients with type 2 diabetes mellitus and BMI-matched control subjects. Diabetologia 50:113-120 (Pubitemid 46035859)
9. Heilbronn LK, Gan SK, Turner N, Campbell LV, Chisholm DJ (2007) Markers of mitochondrial biogenesis and metabolism are lower in overweight and obese insulin-resistant subjects. J Clin Endocrinol Metab 92:1467-1473 (Pubitemid 46556427)
10. Szendroedi J, Schmid AI, Chmelik M et al (2007) Muscle mitochondrial ATP synthesis and glucose transport/phosphorylation in type 2 diabetes. PLoS Med 4:e154 (Pubitemid 46842577)
11. Phielix E, Schrauwen-Hinderling VB, Mensink M et al (2008) Lower intrinsic ADP-stimulated mitochondrial respiration underlies in vivo mitochondrial dysfunction in muscle of male type 2 diabetic patients. Diabetes 57:2943-2949
12. Skulachev VP, Anisimov VN, Antonenko YN et al (2009) An attempt to prevent senescence: a mitochondrial approach. Biochim Biophys Acta 1787:437-461
13. Antonenko YN, Avetisyan AV, Bakeeva LE et al (2008) Mitochondria-targeted plastoquinone derivatives as tools to interrupt execution of the aging program. 1. Cationic plastoquinone derivatives: synthesis and in vitro studies. Biochemistry (Mosc) 73:1273-1287
14. Bakeeva LE, Barskov IV, Egorov MV et al (2008) Mitochondria-targeted plastoquinone derivatives as tools to interrupt execution of the aging program. 2. Treatment of some ROS- and age-related diseases (heart arrhythmia, heart infarctions, kidney ischemia, and stroke). Biochemistry (Mosc) 73:1288-1299
15. Hommelberg PP, Plat J, Sparks LM et al (2011) Palmitate-induced skeletal muscle insulin resistance does not require NF-kappaB activation. Cell Mol Life Sci 68:1215-1225
16. Neroev VV, Archipova MM, Bakeeva LE et al (2008) Mitochondria-targeted plastoquinone derivatives as tools to interrupt execution of the aging program. 4. Age-related eye disease. SkQ1 returns vision to blind animals. Biochemistry (Mosc) 73:1317-1328
17. Anisimov VN, Bakeeva LE, Egormin PA et al (2008) Mitochondria-targeted plastoquinone derivatives as tools to interrupt execution of the aging program. 5. SkQ1 prolongs lifespan and prevents development of traits of senescence. Biochemistry (Mosc) 73:1329-1342
18. Paglialunga S, Schrauwen P, Roy C et al (2007) Reduced adipose tissue triglyceride synthesis and increased muscle fatty acid oxidation in C5L2 knockout mice. J Endocrinol 194:293-304 (Pubitemid 47249668)
19. Ouwens DM, van der Zon GC, Pronk GJ et al (1994) A mutant insulin receptor induces formation of a Shc-growth factor receptor bound protein 2 (Grb2) complex and p21ras-GTP without detectable interaction of insulin receptor substrate 1 (IRS1) with Grb2. Evidence for IRS1-independent p21ras-GTP formation. J Biol Chem 269:33116-33122
20. Lenaers E, de Feyter HM, Hoeks J et al (2010) Adaptations in mitochondrial function parallel, but fail to rescue, the transition to severe hyperglycemia and hyperinsulinemia: a study in Zucker diabetic fatty rats. Obesity (Silver Spring) 18:1100-1107
21. Sparks LM, Xie H, Koza RA et al (2005) A high-fat diet coordinately downregulates genes required for mitochondrial oxidative phosphorylation in skeletal muscle. Diabetes 54:1926-1933 (Pubitemid 40911253)
22. Oberley LW, Spitz DR (1984) Assay of superoxide dismutase activity in tumor tissue. Methods Enzymol 105:457-464 (Pubitemid 14165412)
23. Paglia DE, Valentine WN (1967) Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med 70:158-169
24. Hoeks J, Arany Z, Phielix E, Moonen-Kornips E, Hesselink MK, Schrauwen P (2012) Enhanced lipid-but not carbohydrate-supported mitochondrial respiration in skeletal muscle of PGC-1alpha overexpressing mice. J Cell Physiol 227:1026-1033
25. Hoeks J, Briede JJ, de Vogel J et al (2008) Mitochondrial function, content and ROS production in rat skeletal muscle: effect of high-fat feeding. FEBS Lett 582:510-516
26. Shabalina IG, Hoeks J, Kramarova TV, Schrauwen P, Cannon B, Nedergaard J (2010) Cold tolerance of UCP1-ablated mice: a skeletal muscle mitochondria switch toward lipid oxidation with marked UCP3 up-regulation not associated with increased basal, fatty acid- or ROS-induced uncoupling or enhanced GDP effects. Biochim Biophys Acta 1797:968-980
27. Tahara EB, Navarete FD, Kowaltowski AJ (2009) Tissue-, substrate-, and site-specific characteristics of mitochondrial reactive oxygen species generation. Free Radic Biol Med 46:1283-1297
28. Mansouri A, Muller FL, Liu Y et al (2006) Alterations in mitochondrial function, hydrogen peroxide release and oxidative damage in mouse hind-limb skeletal muscle during aging. Mech Ageing Dev 127:298-306 (Pubitemid 43214503)
29. Hoehn KL, Salmon AB, Hohnen-Behrens C et al (2009) Insulin resistance is a cellular antioxidant defense mechanism. Proc Natl Acad Sci U S A 106:17787-17792
30. Yuzefovych L, Wilson G, Rachek L (2010) Different effects of oleate vs palmitate on mitochondrial function, apoptosis, and insulin signaling in L6 skeletal muscle cells: role of oxidative stress. Am J Physiol Endocrinol Metab 299:E1096-E1105
31. Hansen LL, Ikeda Y, Olsen GS, Busch AK, Mosthaf L (1999) Insulin signaling is inhibited by micromolar concentrations of H(2)O(2). Evidence for a role of H(2)O(2) in tumor necrosis factor alpha-mediated insulin resistance. J Biol Chem 274:25078-25084 (Pubitemid 29404719)
32. Bonnard C, Durand A, Peyrol S et al (2008) Mitochondrial dysfunction results from oxidative stress in the skeletal muscle of diet-induced insulin-resistant mice. J Clin Invest 118:789-800 (Pubitemid 351206566)
33. Ruiz-Ramirez A, Chavez-Salgado M, Peneda-Flores JA, Zapata E, Masso F, El-Hafidi M (2011) High-sucrose diet increases ROS generation, FFA accumulation, UCP2 level, and proton leak in liver mitochondria. Am J Physiol Endocrinol Metab 301:E1198-E1207
34. Goldstein BJ, Mahadev K, Wu X (2005) Redox paradox: insulin action is facilitated by insulin-stimulated reactive oxygen species with multiple potential signaling targets. Diabetes 54:311-321
35. Rhee SG (2006) Cell signaling. H2O2, a necessary evil for cell signaling. Science 312:1882-1883 (Pubitemid 43993698)
36. Loh K, Deng H, Fukushima A et al (2009) Reactive oxygen species enhance insulin sensitivity. Cell Metab 10:260-272
37. McClung JP, Roneker CA, Mu W et al (2004) Development of insulin resistance and obesity in mice overexpressing cellular glutathione peroxidase. Proc Natl Acad Sci U S A 101:8852-8857 (Pubitemid 38781575)
38. Yokota T, Kinugawa S, Hirabayashi K et al (2009) Oxidative stress in skeletal muscle impairs mitochondrial respiration and limits exercise capacity in type 2 diabetic mice. Am J Physiol Heart Circ Physiol 297:H1069-H1077
39. Abdul-Ghani MA, Jani R, Chavez A, Molina-Carrion M, Tripathy D, Defronzo RA (2009) Mitochondrial reactive oxygen species generation in obese non-diabetic and type 2 diabetic participants. Diabetologia 52:574-582
40. Hoehn KL, Hohnen-Behrens C, Cederberg A et al (2008) IRS1-independent defects define major nodes of insulin resistance. Cell Metab 7:421-433 (Pubitemid 351598028)
41. 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)
42. Garcia-Roves P, Huss JM, Han DH et al (2007) Raising plasma fatty acid concentration induces increased biogenesis of mitochondria in skeletal muscle. Proc Natl Acad Sci U S A 104:10709-10713 (Pubitemid 47185729)
43. Ristow M, Zarse K, Oberbach A et al (2009) Antioxidants prevent health-promoting effects of physical exercise in humans. Proc Natl Acad Sci U S A 106:8665-8670
44. Strobel NA, Peake JM, Matsumoto A, Marsh SA, Coombes JS, Wadley GD (2011) Antioxidant supplementation reduces skeletal muscle mitochondrial biogenesis. Med Sci Sports Exerc 43:1017-1024
45. Higashida K, Kim SH, Higuchi M, Holloszy JO, Han DH (2011) Normal adaptations to exercise despite protection against oxidative stress. Am J Physiol Endocrinol Metab 301:E779-E784
46. Mogensen M, Sahlin K, Fernstrom M et al (2007) Mitochondrial respiration is decreased in skeletal muscle of patients with type 2 diabetes. Diabetes 56:1592-1599 (Pubitemid 46842617)
47. Barazzoni R, Zanetti M, Cappellari GG et al (2012) Fatty acids acutely enhance insulin-induced oxidative stress and cause insulin resistance by increasing mitochondrial reactive oxygen species (ROS) generation and nuclear factor-kappaB inhibitor (IkappaB)-nuclear factor-kappaB (NFkappaB) activation in rat muscle, in the absence of mitochondrial dysfunction. Diabetologia 55:773-782
48. Anisimov VN, Egorov MV, Krasilshchikova MS et al (2011) Effects of the mitochondria-targeted antioxidant SkQ1 on lifespan of rodents. Aging (Albany NY) 3:1110-1119