Skeletal muscle insulin resistance: Role of mitochondria and other ROS sources

Journal of Endocrinology

Volumn 233, Issue 1, 2017, Pages R15-R42

  Di Meo, Sergio ^a   Iossa, Susanna ^a   Venditti, Paola ^a  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

Author keywords

Diabetes; Exercise; Insulin resistance; Mitochondria; Obesity; Oxidative stress; ROS production; ROS sources

Indexed keywords

HYDROGEN PEROXIDE; INSULIN; LIPID; REACTIVE OXYGEN METABOLITE;

ADIPOSE TISSUE; BIOACCUMULATION; DISORDERS OF MITOCHONDRIAL FUNCTIONS; HUMAN; HYPERLIPIDEMIA; INSULIN RESISTANCE; MITOCHONDRION; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; OXIDATIVE STRESS; POSITIVE FEEDBACK; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; ANIMAL; METABOLISM; MUSCLE MITOCHONDRION; PHYSIOLOGY;

ANIMALS; DIABETES MELLITUS, TYPE 2; HUMANS; INSULIN RESISTANCE; MITOCHONDRIA, MUSCLE; MUSCLE, SKELETAL; OBESITY; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES;

EID: 85015707316     PISSN: 00220795     EISSN: 14796805     Source Type: Journal    
DOI: 10.1530/JOE-16-0598     Document Type: Review

References (278)

1. Abdul-Ghani MA, Muller FL, Liu Y, Chavez AO, Balas B, Zuo P, Chang Z, Tripathy D, Jani R, Molina-Carrion M, Monroy A, et al. 2008 Deleterious action of FA metabolites on ATP synthesis: possible link between lipotoxicity, mitochondrial dysfunction, and insulin resistance. American Journal of Physiology 295 E678-E685. (doi:10.1152/ajpendo.90287.2008)
2. Aguirre V, Uchida T, Yenush L, Davis R & White MF 2000 The c-Jun NH2-terminal kinase promotes insulin resistance during association with insulin receptor substrate-1 and phosphorylation of Ser307. Journal of Biological Chemistry 275 9047-9054. (doi:10.1074/jbc.275.12.9047)
3. Aguirre V, Werner ED, Giraud J, Lee YH, Shoelson SE & White MF 2002 Phosphorylation of Ser307 in insulin receptor substrate-1 blocks interactions with the insulin receptor and inhibits insulin action. Journal of Biological Chemistry 277 1531-1537. (doi:10.1074/jbc. M101521200)
4. Amati F, Dubé JJ, Coen PM, Stefanovic-Racic M, Toledo FGS & Goodpaster BH 2009 Physical inactivity and obesity underlie the insulin resistance of aging. Diabetes Care 32 1547-1549. (doi:10.2337/dc09-0267)
5. Anderson EJ, Yamazaki H & Neufer PD 2007 Induction of endogenous uncoupling protein 3 suppresses mitochondrial oxidant emission during fatty acid-supported respiration. Journal of Biological Chemistry 282 31257-31266. (doi:10.1074/jbc.M706129200)
6. 2 emission and cellular redox state link excess fat intake to insulin resistance in both rodents and humans. Journal of Clinical Investigation 119 573-581. (doi:10.1172/JCI37048)
7. Andreozzi F, Laratta E, Sciacqua A, Perticone F & Sesti G 2004 Angiotensin II impairs the insulin signaling pathway promoting production of nitric oxide by inducing phosphorylation of insulin receptor substrate-1 on Ser(312) and Ser(616) in human umbilical vein endothelial cells. Circulation Research 94 1211-1218. (doi:10.1161/01.RES.0000126501.34994.96)
8. Anflous-Pharayra K, Cai ZJ & Craigen WJ 2007 VDAC1 serves as a mitochondrial binding site for hexokinase in oxidative muscles. Biochimica et Biophysica Acta 1767 136-142. (doi:10.1016/j. bbabio.2006.11.013)
9. Aon MA, Cortassa S, Marbán E & O'Rourke B 2003 Synchronized whole cell oscillations in mitochondrial metabolism triggered by a local release of reactive oxygen species in cardiac myocytes. Journal of Biological Chemistry 278 44735-44744. (doi:10.1074/jbc.M302673200)
10. Ara I, Larsen S, Stallknecht B, Guerra B, Morales-Alamo D, Andersen JL, Ponce-González JG, Guadalupe-Grau A, Galbo H, Calbet JA, et al. 2011 Normal mitochondrial function and increased fat oxidation capacity in leg and arm muscles in obese humans. International Journal of Obesity 35 99-108. (doi:10.1038/ijo.2010.123)
11. Atgié C, Marette A, Desautels M, Tulp O & Bukowiecki LJ 1993 Specific decrease of mitochondrial thermogenic capacity in brown adipose tissue of obese SHR/N-cp rats. American Journal of Physiology 265 C1674-C1680.
12. Babior BM 1999 NADPH oxidase: an update. Blood 93 1464-1476.
13. Bach D, Naon D, Pich S, Soriano FX, Vega N, Rieusset J, Laville M, Guillet C, Boirie Y, Wallberg-Henriksson H, et al. 2005 Expression of Mfn2, the Charcot-Marie-Tooth neuropathy type 2A gene, in human skeletal muscle: effects of type 2 diabetes, obesity, weight loss, and the regulatory role of tumor necrosis factor a and interleukin-6. Diabetes 54 2685-2693. (doi:10.2337/diabetes.54.9.2685)
14. Bachmann OP, Dahl DB, Brechtel K, Machann J, Haap M, Maier T, Loviscach M, Stumvoll M, Claussen CD, Schick F, et al. 2001 Effects of intravenous and dietary lipid challenge on intramyocellular lipid content and the relation with insulin sensitivity in humans. Diabetes 50 2579-2584. (doi:10.2337/diabetes.50.11.2579)
15. Balakirev MY, Khramtsov VV & Zimmer G 1997 Modulation of the mitochondrial permeability transition by nitric oxide. European Journal of Biochemistry 246 710-718. (doi:10.1111/j.1432-1033.1997.00710.x)
16. Balteau M, Tajeddine N, de Meester C, Ginion A, Des Rosiers C, Brady NR, Sommereyns C, Horman S, Vanoverschelde JL, Gailly P, et al. 2011 NADPH oxidase activation by hyperglycaemia in cardiomyocytes is independent of glucose metabolism but requires SGLT1. Cardiovascular Research 2 237-246. (doi:10.1093/cvr/cvr230)
17. Bandyopadhyay G, Standaert ML, Galloway L, Moscat J, & Farese RV 1997 Evidence for involvement of protein kinase C (PKC)-γ and noninvolvement of diacylglycerol-sensitive PKCs in insulinstimulated glucose transport in L6 myotubes. Endocrinology 138 4721-4731. (doi:10.1210/endo.138.11.5473)
18. Bandyopadhyay G, Standaert ML, Sajan MP, Karnitz LM, Cong L, Quon MJ & Farese RV 1999 Dependence of insulin-stimulated glucose transporter 4 translocation on 3-phosphoinositide-dependent protein kinase-1 and its target threonine-410 in the activation loop of protein kinase C-γ. Molecular Endocrinology 13 1766-1772. (doi:10.1210/mend.13.10.0364)
19. Barazzoni R, Zanetti M, Gortan Cappellari G, Semolic A, Boschelle M, Codarin E, Pirulli A, Cattin L & Guarnieri G 2012 Fatty acids acutely enhance insulin-induced oxidative stress and cause insulin resistance by increasing mitochondrial reactive oxygen species (ROS) generation and nuclear factor-κB inhibitor (IκB)-nuclear factor-κB (NFκB) activation in rat muscle, in the absence of mitochondrial dysfunction. Diabetologia 55 773-782. (doi:10.1007/s00125-011-2396-x)
20. Befroy DE, Petersen KF, Dufour S, Mason GF, de Graaf RA, Rothman DL & Shulman GI 2007 Impaired mitochondrial substrate oxidation in muscle of insulin-resistant offspring of type 2 diabetic patients. Diabetes 56 1376-1381. (doi:10.2337/db06-0783)
21. 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. (doi:10.2337/diabetes.54.6.1640)
22. Berg AH, Combs TP, Du X, Brownlee M & Scherer PE 2001 The adipocytesecreted protein Acrp30 enhances hepatic insulin action. Nature Medicine 7 947-953. (doi:10.1038/90992)
23. Berniakovich I, Trinei M, Stendardo M, Migliaccio E, Minucci S, Bernardi P, Pelicci PG & Giorgio M 2008 p66Shc-generated oxidative signal promotes fat accumulation. Journal of Biological Chemistry 283 34283-34293.
24. Bjornholm M, Kawano Y, Lehtihet M & Zierath JR 1997 Insulin receptor substrate-1 phosphorylation and phosphatidylinositol 3-kinase activity in skeletal muscle from NIDDM subjects after in vivo insulin stimulation. Diabetes 46 524-527. (doi:10.2337/diab.46.3.524)
25. Blendea MC, Jacobs D, Stump CS, McFarlane SI, Ogrin C, Bahtyiar G, Stas S, Kumar P, Sha Q, Ferrario CM, et al. 2005 Abrogation of oxidative stress improves insulin sensitivity in the Ren-2 rat model of tissue angiotensin II overexpression. American Journal of Physiology 288 E353-E359.
26. Bloch-Damti A & Bashan N 2005 Proposed mechanisms for the induction of insulin resistance by oxidative stress. Antioxidant and Redox Signaling 7 1553-1567. (doi:10.1089/ars.2005.7.1553)
27. Boden G & Chen XH 1995 Effects of fat on glucose-uptake and utilization in patients with non-insulin-dependent diabetes. Journal of Clinical Investigation 96 1261-1268. (doi:10.1172/JCI118160)
28. Boden G, Jadali F, White J, Liang Y, Mozzoli M, Chen X, Coleman E & Smith C 1991 Effects of fat on insulin-stimulated carbohydratemetabolism in normal men. Journal of Clinical Investigation 88 960-966. (doi:10.1172/JCI115399)
29. Boden MJ, Brandon AE, Tid-Ang JD, Preston E, Wilks D, Stuart E, Cleasby ME, Turner N, Cooney GJ & Kraegen EW 2012 Overexpression of manganese superoxide dismutase ameliorates high-fat diet-induced insulin resistance in rat skeletal muscle. American Journal of Physiology 303 E798-E805. (doi:10.1152/ajpendo.00577.2011)
30. Bogdan C 2001 Nitric oxide and the regulation of gene expression. Trends in Cell Biology 11 66-75. (doi:10.1016/S0962-8924(00)01900-0)
31. Bonadonna RC, Del Prato S, Bonora E, Saccomani MP, Gulli G, Natali A, Frascerra S, Pecori N, Ferrannini E, Bier D, et al. 1996 Roles of glucose transport and glucose phosphorylation in muscle insulin resistance of NIDDM. Diabetes 45 915-925. (doi:10.2337/diab.45.7.915)
32. Bonnard C, Durand A, Peyrol S, Chanseaume E, Chauvin MA, Morio B, Vidal H & Rieusset J 2008 Mitochondrial dysfunction results from oxidative stress in the skeletal muscle of diet-induced insulin-resistant mice Journal of Clinical Investigation 118 789-800. (doi:10.1172/JCI32601)
33. Boudina S, Sena S, Sloan C, Tebbi A, Han YH, O'Neill BT, Cooksey RC, Jones D, Holland WL, McClain DA, et al. 2012 Early mitochondrial adaptations in skeletal muscle to diet-induced obesity are strain dependent and determine oxidative stress and energy expenditure but not insulin sensitivity. Endocrinology 153 2677-2688. (doi:10.1210/en.2011-2147)
34. Boushel R, Gnaiger E, Schjerling P, Skovbro M, Kraunsøe R & Dela F 2007 Patients with type 2 diabetes have normal mitochondrial function in skeletal muscle. Diabetologia 50 790-796. (doi:10.1007/s00125-007-0594-3)
35. Boustany CM, Bhardwaj K, Daugherty A, Brown DR, Randall DC & Cassis LA 2004 Activation of the systemic and adipose reninangiotensin system in rats with diet-induced obesity and hypertension. American Journal of Physiology 287 R943-R949. (doi:10.1152/ajpregu.00265.2004)
36. Boveris A, Poderoso JJ, Carreras MC & Cadenas E 2000 Regulation of mitochondrial respiration by oxygen and nitric oxide. Annals of the New York Academy of Sciences 899 121-135. (doi:10.1111/j.1749-6632.2000.tb06181.x)
37. Brand MD 2010 The sites and topology of mitochondrial superoxide production. Experimental Gerontology 45 466-472. (doi:10.1016/j. exger.2010.01.003)
38. Brechtel K, Dahl DB, Machann J, Bachmann OP, Wenzel I, Maier T, Claussen CD, Häring HU, Jacob S & Schick F 2001 Fast elevation of the intramyocellular lipid content in the presence of circulating free fatty acids and hyperinsulinemia: a dynamic H-1-MRS study. Magnetic Resonance in Medicine 45 179-183. (doi:10.1002/1522-2594(200102)45:2<179::AID-MRM1023>3.0.CO;2-D)
39. Brieger K, Schiavone S, Miller FJ & Krause K-H 2012 Reactive oxygen species: from health to disease. Swiss Medical Weekly 142 w13659.
40. Brownlee M 2001 Biochemistry and molecular cell biology of diabetic complications. Nature 414 813-820. (doi:10.1038/414813a)
41. Cai D, Yuan M, Frantz DF, Melendez PA, Hansen L, Lee J & Shoelson SE 2005 Local and systemic insulin resistance resulting from hepatic activation of IKK-β and NF-κB. Nature Medicine 11 183-190. (doi:10.1038/nm1166)
42. Camici GG, Cosentino F, Tanner FC & Lüscher TF 2008 The role of p66Shc deletion in age-associated arterial dysfunction and disease states. Journal of Applied Physiology 105 1628-1631. (doi:10.1152/japplphysiol.90579.2008)
43. Camões F, Bonekamp NA, Delille HK & Schrader M 2009 Organelle dynamics and dysfunction: a closer link between peroxisomes and mitochondria. Journal Inherited Metabolic Disease 32 163-180. (doi:10.1007/s10545-008-1018-3)
44. Caro JF, Dohm LG, Pories WJ & Sinha MK 1989 Cellular alterations in liver, skeletal muscle, and adipose tissue responsible for insulin resistance in obesity and type II diabetes. Diabetes/Metabolism Reviews 5 665-689. (doi:10.1002/dmr.5610050804)
45. Carvalho-Filho MA, Ueno M, Hirabara SM, Seabra AB, Carvalheira JB, de Oliveira MG, Velloso LA, Curi R & Saad MJ 2005 S-nitrosation of the insulin receptor, insulin receptor substrate 1, and protein kinase B/Akt: a novel mechanism of insulin resistance. Diabetes 54 959-967. (doi:10.2337/diabetes.54.4.959)
46. Chance B & Williams GR 1956 The respiratory chain and oxidative phosphorylation. Advances in Enzymology and Related Subjects of Biochemistry 17 65-134. (doi:10.1002/9780470122624.ch2)
47. Chanock SJ, el Benna J, Smith RM & Babior BM 1994 The respiratory burst oxidase. Journal of Biological Chemistry 269 24519-24522.
48. Chanseaume E, Malpuech-Brugère C, Patrac V, Bielicki G, Rousset P, Couturier K, Salles J, Renou JP, Boirie Y & Morio B 2006 Diets high in sugar, fat, and energy induce muscle type-specific adaptations in mitochondrial functions in rats. Journal of Nutrition 136 2194-2200.
49. Chanseaume E, Tardy AL, Salles J, Giraudet C, Rousset P, Tissandier A, Boirie Y & Morio B 2007 Chronological approach of diet-induced alterations in muscle mitochondrial functions in rats. Obesity 15 50-59. (doi:10.1038/oby.2007.511)
50. Cheatham B, Vlahos CJ, Cheatham L, Wang L, Blenis J & Kahn CR 1994 Phosphatidylinositol 3-kinase activation is required for insulin stimulation of Pp70 S6 kinase, DNA-synthesis, and glucosetransporter translocation. Molecular and Cellular Biology 14 4902-4911. (doi:10.1128/MCB.14.7.4902)
51. 2 by overexpressing peroxiredoxin 3 improves glucose tolerance in mice. Aging Cell 7 866-878. (doi:10.1111/j.1474-9726.2008.00432.x)
52. Chen-Zion M, Bassukevitz Y & Beitner R 1992 Sequence of insulin effects on cytoskeletal and cytosolic phosphofructokinase, mitochondrial hexokinase, glucose 1,6-bisphosphate and fructose 2,6-bisphosphate levels, and the antagonistic action of calmodulin inhibitors, in diaphragm muscle. International Journal of Biochemistry 24 1661-1667. (doi:10.1016/0020-711X(92)90185-4)
53. Cho D-H, Nakamura T, Fang J, Cieplak P, Godzik A, Gu Z & Lipton SA 2009 S-Nitrosylation of Drp1 mediates β-amyloid-related mitochondrial fission and neuronal injury. Science 324 102-105. (doi:10.1126/science.1171091)
54. Chow L, From A & Seaquist E 2010 Skeletal muscle insulin resistance: the interplay of local lipid excess and mitochondrial dysfunction. Metabolism 59 70-85. (doi:10.1016/j.metabol.2009.07.009)
55. Chu KY, Lau T, Carlsson PO & Leung PS 2006 Angiotensin II type 1 receptor blockade improves β-cell function and glucose tolerance in a mouse model of type 2 diabetes. Diabetes 55 367-374. (doi:10.2337/diabetes.55.02.06.db05-1022)
56. Cipolat S, de Brito MO, Dal Zilio B & Scorrano L 2004 OPA1 require smitofusin1 to promote mitochondrial fusion. PNAS 101 15927-15932. (doi:10.1073/pnas.0407043101)
57. Coen PM & Goodpaster BH 2012 Role of intramyocelluar lipids in human health. Trends in Endocrinology and Metabolism 23 391-398. (doi:10.1016/j.tem.2012.05.009)
58. Copps KD, Hancer NJ, Opare-Ado L, Qiu W, Walsh C & White MF 2010 Irs1 serine 307 promotes insulin sensitivity in mice. Cell Metabolism 11 84-92. (doi:10.1016/j.cmet.2009.11.003)
59. Crescenzo R, Bianco F, Coppola P, Mazzoli A, Cigliano L, Liverini G & Iossa S 2013 Increased skeletal muscle mitochondrial efficiency in rats with fructose-induced alteration in glucose tolerance. British Journal of Nutrition 110 1996-2003. (doi:10.1017/S0007114513001566)
60. Crescenzo R, Bianco F, Coppola P, Mazzoli A, Liverini G & Iossa S 2014 Subsarcolemmal and intermyofibrillar mitochondrial responses to short-term high-fat feeding in rat skeletal muscle. Nutrition 30 75-81. (doi:10.1016/j.nut.2013.05.022)
61. Crescenzo R, Bianco F, Coppola P, Mazzoli A, Cigliano L, Liverini G & Iossa S 2015 The effect of high-fat-high-fructose diet on skeletal muscle mitochondrial energetics in adult rats. European Journal of Nutrition 54 183-192. (doi:10.1007/s00394-014-0699-7)
62. Cross DA, Alessi DR, Cohen P, Andjelkovich M & Hemmings BA 1995 Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature 378 785-789. (doi:10.1038/378785a0)
63. Cusi K, Maezono K, Osman A, Pendergrass M, Patti ME, Pratipanawatr T, DeFronzo RA, Kahn CR & Mandarino LJ 2000 Insulin resistance differentially affects the PI3-kinase-and MAP kinase-mediated signaling in human muscle. Journal of Clinical Investigation 105 311-320. (doi:10.1172/JCI7535)
64. 2+-dependent thiol activation of fat cell glucose utilization. Journal of Biological Chemistry 249 1001-1006.
65. Czech MP, Lawrence JC Jr & Lynn WS 1974b Evidence for the involvement of sulfhydryl oxidation in the regulation of fat cell hexose transport by insulin. PNAS 71 4173-4177. (doi:10.1073/pnas.71.10.4173)
66. Daiber A 2010 Redox signaling (cross-talk) fromand to mitochondria involves mitochondrial pores and reactive oxygen species. Biochimica et Biophysica Acta 1797 897-906. (doi:10.1016/j.bbabio.2010.01.032)
67. Davies KJA 2000 Oxidative stress, antioxidant defenses, and damage removal, repair, and replacement systems. IUBMB Life 50 279-289. (doi:10.1080/15216540051081010)
68. de Ferranti S & Mozaffarian D 2008 The perfect storm: obesity, adipocyte dysfunction, and metabolic consequences. Clinical Chemistry 54 945-955. (doi:10.1373/clinchem.2007.100156)
69. De Feyter HM, Lenaers E, Houten SM, Schrauwen P, Hesselink MK, Wanders RJ, Nicolay K & Prompers JJ 2008a Increased intramyocellular lipid content but normal skeletal muscle mitochondrial oxidative capacity throughout the pathogenesis of type 2 diabetes. FASEB Journal 22 3947-3955. (doi:10.1096/fj.08-112318)
70. De Feyter HM, van den Broek NM, Praet SF, Nicolay K, van Loon LJ & Prompers JJ 2008b Early or advanced stage type 2 diabetes is not accompanied by in vivo skeletal muscle mitochondrial dysfunction. European Journal of Endocrinology 158 643-653. (doi:10.1530/eje-07-0756)
71. De Palma C, Falcone S, Pisoni S, Cipolat S, Panzeri C, Pambianco S, Pisconti A, Allevi R, Bassi MT, Cossu G, et al. 2010 Nitric oxide inhibition of Drp1-mediated mitochondrial fission is critical for myogenic differentiation. Cell Death and Differentiation 17 1684-1696. (doi:10.1038/cdd.2010.48)
72. de Wilde J, Mohren R, van den Berg S, Boekschoten M, Dijk KW, de Groot P, Müller M, Mariman E & Smit E 2008 Short-term high fat-feeding results in morphological and metabolic adaptations in the skeletal muscle of C57BL/6J mice. Physiological Genomics 32 360-369. (doi:10.1152/physiolgenomics.00219.2007)
73. DeFronzo RA & Ferrannini E 1991 Insulin resistance. A multifaceted syndrome responsible for NIDDM, obesity, hypertension, dyslipidemia, and atherosclerotic cardiovascular disease. Diabetes Care 14 173-194. (doi:10.2337/diacare.14.3.173)
74. Di Meo S & Venditti P 2001 Mitochondria in exercise-induced oxidative stress. Biological Signals and Receptors 10 125-140. (doi:10.1159/000046880)
75. Di Meo S, Reed TT, Venditti P & Victor MV 2016 Role of ROS and RNS sources in physiological and pathological conditions. Oxidative Medicine and Cellular Longevity 2016 1-44. (doi:10.1155/2016/1245049)
76. Diamond-Stanic MK & Henriksen EJ 2010 Direct inhibition by angiotensin II of insulin-dependent glucose transport activity in mammalian skeletal muscle involves a ROS-dependent mechanism. Archives of Physiology and Biochemistry 116 88-95. (doi:10.3109/13813451003758703)
77. Dikalov S 2011 Cross talk between mitochondria and NADPH oxidases. Free Radical Biology and Medicine 51 1289-1301. (doi:10.1016/j. freeradbiomed.2011.06.033)
78. Dokken BB, Saengsirisuwan V, Kim JS, Teachey MK & Henriksen EJ 2008 Oxidative stress induced insulin resistance in rat skeletal muscle: role of glycogen synthase kinase-3. American Journal of Physiology 294 E615-E621. (doi:10.1152/ajpendo.00578.2007)
79. Doughan AK, Harrison DG & Dikalov SI 2008 Molecular mechanisms of angiotensin II-mediated mitochondrial dysfunction: linking mitochondrial oxidative damage and vascular endothelial dysfunction. Circulation Research 102 488-496. (doi:10.1161/CIRCRESAHA.107.162800)
80. Elchebly M, Payette P, Michaliszyn E, Cromlish W, Collins S, Loy AL, Normandin D, Cheng A, Himms-Hagen J, Chan CC, et al. 1999 Increased insulin sensitivity and obesity resistance in mice lacking the protein tyrosine phosphatase-1B gene. Science 283 1544-1548. (doi:10.1126/science.283.5407.1544)
81. Eldar-Finkelman H, Schreyer SA, Shinohara MM, LeBoeuf RC & Krebs EG 1999 Increased glycogen synthase kinase-3 activity in diabetes-and obesity-prone C57BL/6J mice. Diabetes 48 1662-1666. (doi:10.2337/diabetes.48.8.1662)
82. Engeli S, Bohnke J, Gorzelniak K, Janke J, Schling P, Bader M, Luft FC & Sharma AM 2005 Weight loss and the renin-angiotensinaldosterone system. Hypertension 45 356-362. (doi:10.1161/01. HYP.0000154361.47683.d3)
83. Ernster L & Lee C-P 1967 Energy-linked reduction of NAD+ by succinate. Methods in Enzymology 10 729-738. (doi:10.1016/0076-6879(67)10120-1)
84. Espinosa A, Garcia A, Hartel S, Hidalgo C & Jaimovich E 2009 NADPH oxidase and hydrogen peroxide mediate insulin-induced calcium increase in skeletal muscle cells. Journal of Biological Chemistry 284 2568-2575. (doi:10.1074/jbc.M804249200)
85. Evans JL, Goldfine ID, Maddux BA & Grodsky GM 2002 Oxidative stress and stress-activated signaling pathways: a unifying hypothesis of type 2 diabetes. Endocrine Reviews 23 599-622. (doi:10.1210/er.2001-0039)
86. Evans JL, Maddux BA & Goldfine ID 2005 The molecular basis for oxidative stress-induced insulin resistance. Antioxidant and Redox Signaling 7 1040-1052. (doi:10.1089/ars.2005.7.1040)
87. 2-induced mitochondrial fragmentation in C2C12 myocytes. Free Radical Biology and Medicine 49 1646-1654. (doi:10.1016/j.freeradbiomed.2010.08.024)
88. Finkel T & Holbrook NJ 2000 Oxidants, oxidative stress and the biology of ageing. Nature 408 239-247. (doi:10.1038/35041687)
89. Fisher-Wellman KH & Neufer PD 2012 Linking mitochondrial bioenergetics to the etiology of insulin resistance via redox biology. Trends in Endocrinology and Metabolism 23 142-153. (doi:10.1016/j. tem.2011.12.008)
90. Fisher-Wellman KH, Weber TM, Cathey BL, Brophy PM, Gilliam LA, Kane CL, Maples JM, Gavin TP, Houmard JA & Neufer PD 2014 Mitochondrial respiratory capacity and content are normal in young insulin-resistant obese humans. Diabetes 63 132-141. (doi:10.2337/db13-0940)
91. Fleischman A, Kron M, Systrom DM, Hrovat M & Grinspoon SK 2009 Mitochondrial function and insulin resistance in overweight and normal-weight children. Journal of Clinical Endocrinology & Metabolism 94 4923-4930. (doi:10.1210/jc.2009-1590)
92. Folli F, Kahn CR, Hansen H, Bouchie JL & Feener EP 1997 Angiotensin II inhibits insulin signaling in aortic smooth muscle cells at multiple levels - a potential role for serine phosphorylation in insulin/angiotensin II crosstalk. Journal of Clinical Investigation 100 2158-2169. (doi:10.1172/JCI119752)
93. Forman HJ & Fridovich I 1973 Superoxide dismutase: a comparison of rate constants. Archives of Biochemistry and Biophysics 158 396-400. (doi:10.1016/0003-9861(73)90636-X)
94. Forman HJ, Maiorino M & Ursini F 2010 Signaling functions of reactive oxygen species. Biochemistry 49 835-842. (doi:10.1021/bi9020378)
95. Frazier AE, Kiu C, Stojanovski D, Hoogenraad NJ & Ryan MT 2006 Mitochondrial morphology and distribution in mammalian cells. Journal of Biological Chemistry 387 1551-1558. (doi:10.1515/bc.2006.193)
96. Fridovich I 1995 Superoxide radical and superoxide dismutases. Annual Review of Biochemistry 64 97-112. (doi:10.1146/annurev. bi.64.070195.000525)
97. Fueger PT, Bracy DP, Malabanan CM, Pencek RR, Granner DK & Wasserman DH 2004 Hexokinase II overexpression improves exercise-stimulated but not insulin stimulated muscle glucose uptake in high-fat-fed C57BL/6J mice. Diabetes 53 306-314. (doi:10.2337/diabetes.53.2.306)
98. Furler SM, Oakes ND, Watkinson AL & Kraegen EW 1997 A high-fat diet influences insulin-stimulated post transport muscle glucose metabolism in rats. Metabolism 46 1101-1106. (doi:10.1016/S0026-0495(97)90286-9)
99. Gao ZG, Hwang D, Bataille F, Lefevre M, York D, Quon M & Ye J 2002 Serine phosphorylation of insulin receptor substrate 1 by inhibitor kappa B kinase complex. Journal of Biological Chemistry 277 48115- 48121. (doi:10.1074/jbc.M209459200)
100. Garlid KD & Beavis AD 1986 Evidence for the existence of an inner membrane anion channel in mitochondria. Biochimica et Biophysica Acta 853 187-204. (doi:10.1016/0304-4173(87)90001-2)
101. Gerich JE 2003 Clinical significance, pathogenesis, and management of postprandial hyperglycemia. Archives of Internal Medicine 163 1306-1316. (doi:10.1001/archinte.163.11.1306)
102. Gertz M, Fischer F, Wolters D & Steegborn C 2008 Activation of the lifespan regulator p66Shc through reversible disulfide bond formation. PNAS 105 5705-5709. (doi:10.1073/pnas.0800691105)
103. Giorgio M, Migliaccio E, Orsini F, Paolucci D, Moroni M, Contursi C, Pelliccia G, Luzi L, Minucci S, Marcaccio M, et al. 2005 Electron transfer between cytochrome c and p66Shc generates reactive oxygen species that trigger mitochondrial apoptosis. Cell 122 221-233. (doi:10.1016/j.cell.2005.05.011)
104. Gomes AP, Duarte FV, Nunes P, Hubbard BP, Teodoro JS, Varela AT, Jones JG, Sinclair DA, Palmeira CM & Rolo AP 2012 Berberine protects against high fat diet-induced dysfunction in muscle mitochondria by inducing SIRT1-dependent mitochondrial biogenesis. Biochimica et Biophysica Acta 1822 185-195. (doi:10.1016/j.bbadis.2011.10.008)
105. Gómez-Pérez Y, Capllonch-Amer G, Gianotti M, Lladó I & Proenza AM 2012 Long-term high-fat-diet feeding induces skeletal muscle mitochondrial biogenesis in rats in a sex-dependent and muscle-type specific manner. Nutrition and Metabolism 9 15. (doi:10.1186/1743-7075-9-15)
106. Goodyear LJ, Giorgino F, Sherman LA, Carey J, Smith RJ & Dohm GL 1995 Insulin-receptor phosphorylation, insulin-receptor substrate-1 phosphorylation, and phosphatidylinositol 3-kinase activity are decreased in intact skeletal-muscle strips from obese subjects. Journal of Clinical Investigation 95 2195-2204. (doi:10.1172/JCI117909)
107. Goossens GH, Jocken JW, Blaak EE, Schiffers PM, Saris WH & van Baak MA 2007 Endocrine role of the renin-angiotensin system in human adipose tissue and muscle: effect of β-adrenergic stimulation. Hypertension 49 542-547. (doi:10.1161/01.HYP.0000256091.55393.92)
108. Gorzelniak K, Engeli S, Janke J, Luft FC & Sharma AM 2002 Hormonal regulation of the human adipose-tissue renin-angiotensin system: relationship to obesity and hypertension. Journal of Hypertension 20 965-973. (doi:10.1097/00004872-200205000-00032)
109. Halliwell B & Gutteridge JMC 2015 Free Radicals in Biology and Medicine. Oxford, UK: Oxford University Press.
110. Halseth AE, Bracy DP & Wasserman DH 2000 Limitations to basal and insulin-stimulated skeletal muscle glucose uptake in the high-fat-fed rat. American Journal of Physiology 279 E1064-E1071.
111. Hancock CR, Han DH, Chen M, Terada S, Yasuda T, Wright DC & Holloszy JO 2008 High-fat diets cause insulin resistance despite an increase in muscle mitochondria. PNAS 105 7815-7820. (doi:10.1073/pnas.0802057105)
112. Handy DE & Loscalzo J 2012 Redox regulation of mitochondrial function. Antioxidant and Redox Signaling 16 1323-1367. (doi:10.1089/ars.2011.4123)
113. He F & Zuo L 2015 Redox roles of reactive oxygen species in cardiovascular diseases. International Journal of Molecular Sciences 16 27770-27780. (doi:10.3390/ijms161126059)
114. 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. Journal of Clinical Endocrinology and Metabolism 92 1467-1473. (doi:10.1210/jc.2006-2210)
115. Henriksen EJ, Diamond-Stanic MK & Marchionne EM 2011. Oxidative stress and the etiology of insulin resistance and type 2 diabetes. Free Radical Biology and Medicine 51 993-999. (doi:10.1016/j. freeradbiomed.2010.12.005)
116. Hidalgo C, Sánchez G, Barrientos G & Aracena-Parks P 2006 A transverse tubule NADPH oxidase activity stimulates calcium release from isolated triads via ryanodine receptor type 1 S-glutathionylation. Journal of Biological Chemistry 281 26473-26482. (doi:10.1074/jbc. M600451200)
117. Hirabara SM, Curi R & Maechler P 2010 Saturated fatty acid-induced insulin resistance is associated with mitochondrial dysfunction in skeletal muscle cells. Journal of Cellular Physiology 222 187-194. (doi:10.1002/jcp.21936)
118. Hirosumi J, Tuncman G, Chang L, Gorgun CZ, Uysal KT, Maeda K, Karin M & Hotamisligil GS 2002 A central role for JNK in obesity and insulin resistance. Nature 420 333-336. (doi:10.1038/nature01137)
119. Hoehn KL, Hohnen-Behrens C, Cederberg A, Wu LE, Turner N, Yuasa T, Ebina Y & James DE 2008 IRS1-independent defects define major nodes of insulin resistance. Cell Metabolism 7 421-433. (doi:10.1016/j. cmet.2008.04.005)
120. Hoehn KL, Salmon AB, Hohnen-Behrens C, Turner N, Hoy AJ, Maghzal GJ, Stocker R, Van Remmen H, Kraegen EW, Cooney GJ, et al. 2009 Insulin resistance is a cellular antioxidant defense mechanism. PNAS 106 17787-17792. (doi:10.1073/pnas.0902380106)
121. Hoeks J, Briede JJ, de Vogel J, Schaart G, Nabben M, Moonen-Kornips E, Hesselink MK & Schrauwen P 2008 Mitochondrial function, content and ROS production in rat skeletal muscle: effect of high-fat feeding. FEBS Letters 582 510-516. (doi:10.1016/j.febslet.2008.01.013)
122. Hoeks J, van Herpen NA, Mensink M, Moonen-Kornips E, van Beurden D, Hesselink MK & Schrauwen P 2010 Prolonged fasting identifies skeletal muscle mitochondrial dysfunction as consequence rather than cause of human insulin resistance. Diabetes 59 2117-2125. (doi:10.2337/db10-0519)
123. Holloway GP, Thrush AB, Heigenhauser GJ, Tandon NN, Dyck DJ, Bonen A & Spriet LL 2007 Skeletal muscle mitochondrial FAT/CD36 content and palmitate oxidation are not decreased in obese women. American Journal of Physiology: Endocrinology and Metabolism 292 E1782-E1789. (doi:10.1152/ajpendo.00639.2006)
124. Holmström MH, Iglesias-Gutierrez E, Zierath JR & Garcia-Roves PM 2012 Tissue-specific control of mitochondrial respiration in obesity-related insulin resistance and diabetes. American Journal of Physiology 302 E731-E739. (doi:10.1152/ajpendo.00159.2011)
125. Hotamisligil GS, Shargill NS & Spiegelman BM 1993 Adipose expression of tumor necrosis factor-a: direct role in obesity-linked insulin resistance. Science 259 87-91. (doi:10.1126/science.7678183)
126. Houstis N, Rosen ED & Lander ES 2006 Reactive oxygen species have a causal role in multiple forms of insulin resistance. Nature 440 944-948. (doi:10.1038/nature04634)
127. Ignarro LJ, Buga GM, Wood KS, Byrns RE & Chaudhuri G 1987 Endothelium-derived relaxing factor produced and released from artery and vein is nitric oxide. PNAS 84 9265-9269. (doi:10.1073/pnas.84.24.9265)
128. Iwakami S, Misu H, Takeda T, Sugimori M, Matsugo S, Kaneko S & Takamura T 2011 Concentration-dependent dual effects of hydrogen peroxide on insulin signal transduction in H4IIEC hepatocytes. PLoS ONE 6 e27401. (doi:10.1371/journal.pone.0027401)
129. Jastroch M, Divakaruni AS, Mookerjee S, Treberg JR & Brand MD 2010 Mitochondrial proton and electron leaks. Essays in Biochemistry 47 53-67. (doi:10.1042/bse0470053)
130. Javesghani D, Magder SA, Barreiro E, Quinn MT & Hussain SN 2002 Molecular characterization of a superoxide generating NAD(P)H oxidase in the ventilatory muscles. American Journal of Respiratory and Critical Care Medicine 165 412-418. (doi:10.1164/ajrccm.165.3.2103028)
131. Jensen PK 1966 Antimycin-insensitive oxidation of succinate and reduced nicotinamide-adenine dinucleotide in electron transport particles. I. pH dependency and hydrogen peroxide formation. Biochimica et Biophysica Acta 122 157-166. (doi:10.1016/0926-6593(66)90057-9)
132. Jheng HF, Tsai PJ, Guo SM, Kuo LH, Chang CS, Su IJ, Chang CR & Tsai YS 2012 Mitochondrial fission contributes to mitochondrial dysfunction and insulin resistance in skeletal muscle. Molecular and Cellular Biology 32 309-319. (doi:10.1128/MCB.05603-11)
133. Jing E, Emanuelli B, Hirschey MD, Boucher J, Lee KY, Lombard D, Verdin EM & Kahn CR 2011 Sirtuin-3 (Sirt3) regulates skeletal muscle metabolism and insulin signaling via altered mitochondrial oxidation and reactive oxygen species production. PNAS 108 14608-14613. (doi:10.1073/pnas.1111308108)
134. Kalupahana NS & Moustaid-Moussa N 2011 The renin-angiotensin system: a link between obesity, inflammation and insulin resistance. Obesity Reviews 13 136-149. (doi:10.1111/j.1467-789X.2011.00942.x)
135. Kamata H, Manabe T, Oka S, Kamata K & Hirata H 2002 Hydrogen peroxide activates IκB kinases through phosphorylation of serine residues in the activation loops. FEBS Letters 519 231-237. (doi:10.1016/S0014-5793(02)02712-6)
136. Kaneto H, Nakatani Y, Miyatsuka T, Kawamori D, Matsuoka TA, Matsuhisa M, Kajimoto Y, Ichijo H, Yamasaki Y & Hori M 2004 Possible novel therapy for diabetes with cell-permeable JNK-inhibitory peptide. Nature Medicine 10 1128-1132. (doi:10.1038/nm1111)
137. Karakelides H, Irving BA, Short KR, O'Brien P & Nair KS 2010 Age, obesity, and sex effects on insulin sensitivity and skeletal muscle mitochondrial function. Diabetes 59 89-97. (doi:10.2337/db09-0591)
138. Katsuyama M 2010 NOX/NADPH oxidase, the superoxide-generating enzyme: its transcriptional regulation and physiological roles. Journal of Pharmacological Sciences 114 134-146. (doi:10.1254/jphs.10R01CR)
139. Kelley DE, Goodpaster B, Wing RR & Simoneau JA 1999 Skeletal muscle fatty acid metabolism in association with insulin resistance, obesity, and weight loss. American Journal of Physiology 277 E1130-E1141.
140. Kelley DE, He J, Menshikova EV & Ritov VB 2002 Dysfunction of mitochondria in human skeletal muscle in type 2 diabetes. Diabetes 51 2944-2950. (doi:10.2337/diabetes.51.10.2944)
141. Kim YB, Nikoulina SE, Ciaraldi TP, Henry RR & Kahn BB 1999 Normal insulin-dependent activation of Akt/protein kinase B, with diminished activation of phosphoinositide 3-kinase, in muscle in type 2 diabetes. Journal of Clinical Investigation 104 733-741. (doi:10.1172/JCI6928)
142. Kim YB, Kotani K, Ciaraldi TP, Henry RR & Kahn BB 2003 Insulinstimulated protein kinase C lambda/zeta activity is reduced in skeletal muscle of humans with obesity and type 2 diabetes - reversal with weight reduction. Diabetes 52 1935-1942. (doi:10.2337/diabetes.52.8.1935)
143. Kim S, Soltani-Bejnood M, Quignard-Boulange A, Massiera F, Teboul M, Ailhaud G, Kim JH, Moustaid-Moussa N & Voy BH 2006 The adipose rennin-angiotensin system modulates systemic markers of insulin sensitivity and activates the intrarenal renin-angiotensin system. Journal of Biomedicine and Biotechnology 2006 27012. (doi:10.1155/jbb/2006/27012)
144. Knowles RG & Moncada S 1994 Nitric oxide synthases in mammals. Biochemical Journal 298 249-258. (doi:10.1042/bj2980249)
145. Kohn AD, Summers SA, Birnbaum MJ & Roth RA 1996 Expression of a constitutively active Akt Ser/Thr kinase in 3T3-L1 adipocytes stimulates glucose uptake and glucose transporter 4 translocation. Journal of Biological Chemistry 271 31372-31378. (doi:10.1074/jbc.271.49.31372)
146. Koves TR, Ussher JR, Noland RC, Slentz D, Mosedale M, Ilkayeva O, Bain J, Stevens R, Dyck JR Newgard CB, et al. 2008 Mitochondrial overload and incomplete fatty acid oxidation contribute to skeletal muscle insulin resistance. Cell Metabolism 7 45-56. (doi:10.1016/j. cmet.2007.10.013)
147. Kraus RM, Houmard JA, Kraus WE, Tanner CJ, Pierce JR, Choi MD & Hickner RC 2012 Obesity, insulin resistance, and skeletal muscle nitric oxide synthase. Journal of Applied Physiology 113 758-765. (doi:10.1152/japplphysiol.01018.2011)
148. Kruszynska YT, Mulford MI, Baloga J, Yu JG & Olefsky JM 1998 Regulation of skeletal muscle hexokinase II by insulin in nondiabetic and NIDDM subjects. Diabetes 47 1107-1113. (doi:10.2337/diabetes.47.7.1107)
149. Lark DS, Fisher-Wellman KH & Neufer PD 2012 High-fat load: mechanism(s) of insulin resistance in skeletal muscle. International Journal of Obesity 2 S31-S36. (doi:10.1038/ijosup.2012.20)
150. Lark DS, Kang L, Lustig ME, Bonner JS, James FD, Neufer PD & Wasserman DH 2015 Enhanced mitochondrial superoxide scavenging does not improve muscle insulin action in the high fat-fed mouse. PLoS ONE 10 e0126732. (doi:10.1371/journal.pone.0126732)
151. Laurent D, Yerby B, Deacon R & Gao J 2007 Diet-induced modulation of mitochondrial activity in rat muscle. American Journal of Physiology 293 E1169-E1177. (doi:10.1152/ajpendo.00263.2007)
152. Leahy JL 2005 Pathogenesis of type 2 diabetes mellitus. Archives of Medical Research 36 197-209. (doi:10.1016/j.arcmed.2005.01.003)
153. Lee H-Y, Choi CS, Birkenfeld AL, Alves TC, Jornayvaz FR, Jurczak MJ, Zhang D, Woo DK, Shadel GS, Ladiges W, et al. 2010 Targeted expression of catalase to mitochondria prevents age-associated reductions in mitochondrial function and insulin resistance. Cell Metabolism 12 668-674. (doi:10.1016/j.cmet.2010.11.004)
154. Lefort N, Glancy B, Bowen B, Willis WT, Bailowitz Z, De Filippis EA, Brophy C, Meyer C, Højlund K, Yi Z, 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. (doi:10.2337/db10-0174)
155. Li JP, DeFea K & Roth RA 1999 Modulation of insulin receptor substrate-1 tyrosine phosphorylation by an Akt/phosphatidylinositol 3-kinase pathway. Journal of Biological Chemistry 274 9351-9356. (doi:10.1074/jbc.274.14.9351)
156. Li Y, Mouche S, Sajic T, Veyrat-Durebex C, Supale R, Pierroz D, Ferrari S, Negro F, Hasler U, Feraille E, et al. 2012 Deficiency in the NADPH oxidase 4 predisposes towards diet-induced obesity. International Journal of Obesity 36 1503-1513. (doi:10.1038/ijo.2011.279)
157. Liesa M, Palacín M & Zorzano A 2009 Mitochondrial dynamics in mammalian health and disease. Physiological Reviews 89 799-845. (doi:10.1152/physrev.00030.2008)
158. 2 formation. Free Radical Biology and Medicine 10 1465-1469. (doi:10.1016/j.freeradbiomed.2007.02.015)
159. Lionetti L, Mollica MP, Crescenzo R, D'Andrea E, Ferraro M, Bianco F, Liverini G & Iossa S 2007 Skeletal muscle subsarcolemmal mitochondrial dysfunction in high-fat fed rats exhibiting impaired glucose homeostasis. International Journal of Obesity 31 1596-1604. (doi:10.1038/sj.ijo.0803636)
160. Loh K, Deng H, Fukushima A, Cai X, Boivin B, Galic S, Bruce C, Shields BJ, Skiba B, Ooms LM, et al. 2009 Reactive oxygen species enhance insulin sensitivity. Cell Metabolism 10 260-272. (doi:10.1016/j.cmet.2009.08.009)
161. Loschen G, Azzi A, Richter R & Flohé L 1974 Superoxide radicals as precursors of mitochondrial hydrogen peroxide. FEBS Letters 42 68-72. (doi:10.1016/0014-5793(74)80281-4)
162. Lowell BB & Shulman GI 2005 Mitochondrial dysfunction and type 2 diabete. Science 307 384-387. (doi:10.1126/science.1104343)
163. Macconi D, Perico L, Longaretti L, Morigi M, Cassis P, Buelli S, Perico N, Remuzzi G & Benigni A 2015 Sirtuin3 dysfunction is the key determinant of skeletal muscle insulin resistance by angiotensin II. PLoS ONE 10 e0127172. (doi:10.1371/journal.pone.0127172)
164. Matsuzawa Y, Funahashi T & Nakamura T 1999 Molecular mechanism of metabolic syndrome X: contribution of adipocytokines adipocytederived bioactive substances. Annals of the New York Academy of Sciences 892 146-154. (doi:10.1111/j.1749-6632.1999.tb07793.x)
165. May JM & de Haen C 1979 Insulin-stimulated intracellular hydrogen peroxide production in rat epididymal fat cells. Journal of Biological Chemistry 254 2214-2220.
166. McCormack JG, Halestrap AP & Denton RM 1990 Role of calcium ions in regulation of mammalian intramitochondrial metabolism. Physiological Reviews 70 391-425.
167. Migliaccio E, Giorgio M, Mele S, Pelicci G, Reboldi P, Pandolfi PP, Lanfrancone L & Pelicci PG 1999 The p66(shc) adaptor protein controls oxidative stress response and life span in mammals. Nature 402 309-313. (doi:10.1038/46311)
168. Mitchell P & Moyle J 1965 Stoichiometry of proton translocation through the respiratory chain and adenosine triphosphatase systems of rat liver mitochondria. Nature 208 147-151. (doi:10.1038/208147a0)
169. Mitsuishi M, Miyashita K, Muraki A & Itoh H 2009 Angiotensin II reduces mitochondrial content in skeletal muscle and affects glycemic control. Diabetes 58 710-717. (doi:10.2337/db08-0949)
170. Mofarrahi M, Brandes RP, Gorlach A, Hanze J, Terada LS, Quinn MT, Mayaki D, Petrof B & Hussain SN 2008 Regulation of proliferation of skeletal muscle precursor cells by NADPH oxidase. Antioxidants and Redox Signaling 10 559-574. (doi:10.1089/ars.2007.1792)
171. Moncada S & Erusalimsky JD 2002 Does nitric oxide modulate mitochondrial energy generation and apoptosis? Nature Reviews Molecular Cell Biology 3 214-220. (doi:10.1038/nrm762)
172. Mootha VK, Lindgren CM, Eriksson KF, Subramanian A, Sihag S, Lehar J, Puigserver P, Carlsson E, Ridderstråle M, Laurila E, et al. 2003 PGC-1a-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nature Genetics 34 267-273. (doi:10.1038/ng1180)
173. Muller FL, Liu Y & Van Remmen H 2004 Complex III releases superoxide to both sides of the inner mitochondrial membrane. Journal of Biological Chemistry 279 49064-49073. (doi:10.1074/jbc.M407715200)
174. Muller FL, Lustgarten MS, Jang Y, Richardson A & Van Remmen H 2007 Trends in oxidative aging theories. Free Radical Biology and Medicine 43 477-503. (doi:10.1016/j.freeradbiomed.2007.03.034)
175. Muoio DM & Neufer PD 2012 Lipid-induced mitochondrial stress and insulin action in muscle. Cell Metabolism 15 595-605. (doi:10.1016/j. cmet.2012.04.010)
176. Nathan C & Xie Q-W 1994 Nitric oxide synthases: roles, tolls, and controls. Cell 78 915-918. (doi:10.1016/0092-8674(94)90266-6)
177. Navarro A & Boveris A 2007 The mitochondrial energy transduction system and the aging process. American Journal of Physiology 292 C670-C686. (doi:10.1152/ajpcell.00213.2006)
178. Nemoto S, Combs CA, French S, Ahn BH, Fergusson MM, Balaban RS & Finkel T 2006 The mammalian longevity-associated gene product p66shc regulates mitochondrial metabolism. Journal of Biological Chemistry 281 10555-10560. (doi:10.1074/jbc.M511626200)
179. Newsholme P, Haber EP, Hirabara SM, Rebelato EL, Procopio J, Morgan D, Oliveira-Emilio HC, Carpinelli AR & Curi R 2007 Diabetes associated cell stress and dysfunction: role of mitochondrial and nonmitochondrial ROS production and activity. Journal of Physiology 583 9-24. (doi:10.1113/jphysiol.2007.135871)
180. Nunnari J & Suomalainen A 2012 Mitochondria: in sickness and in health. Cell 148 1145-1159. (doi:10.1016/j.cell.2012.02.035)
181. Nunnari J, Wong ED, Meeusen S & Wagner JA 2002 Studying the behavior of mitochondria. Methods in Enzymology 351 381-393. (doi:10.1038/208147a0)
182. Ogihara T, Asano T, Ando K, Chiba Y, Sakoda H, Anai M, Shojima N, Ono H, Onishi Y, Fujishiro M, et al. 2002 Angiotensin II-induced insulin resistance is associated with enhanced insulin signaling. Hypertension 40 872-879. (doi:10.1161/01.HYP.0000040262.48405.A8)
183. Okado-Matsumoto A & Fridovich I 2001 Subcellular distribution of superoxide dismutases (SOD) in rat liver: Cu, Zn-SOD in mitochondria. Journal of Biological Chemistry 276 38388-38393. (doi:10.1074/jbc.M105395200)
184. Okamoto Y, Kihara S, Ouchi N, Nishida M, Arita Y, Kumada M, Ohashi K, Sakai N, Shimomura I, Kobayashi H, Terasaka N, et al. 2002 Adiponectin reduces atherosclerosis in apolipoprotein E-deficient mice. Circulation 106 2767-2770. (doi:10.1161/01. CIR.0000042707.50032.19)
185. Otto TC & Lane MD 2005 Adipose development: from stem cell to adipocyte. Critical Reviews in Biochemistry and Molecular Biology 40 229-242. (doi:10.1080/10409230591008189)
186. Pacher P, Beckman JS & Liaudet L 2007 Nitric oxide and peroxynitrite in health and disease. Physiological Reviews 87 315-424. (doi:10.1152/physrev.00029.2006)
187. Palmer CS, Osellame LD, Stojanovski D & Ryan MT 2011 The regulation of mitochondrial morphology: intricate mechanisms and dynamic machinery. Cellular Signalling 23 1534-1545. (doi:10.1016/j. cellsig.2011.05.021)
188. Pastorino JG, Hoek JB & Shulga N 2005 Activation of glycogen synthase kinase 3β disrupts the binding of hexokinase II to mitochondria by phosphorylating voltage-dependent anion channel and potentiates chemotherapy-induced cytotoxicity. Cancer Research 65 10545-10554. (doi:10.1158/0008-5472.CAN-05-1925)
189. Patti ME, Butte AJ, Crunkhorn S, Cusi K, Berria R, Kashyap S, Miyazaki Y, Kohane I & Costello M 2003 Coordinated reduction of genes of oxidative metabolism in humans with insulin resistance and diabetes: potential role of PGC-1 and NRF1. PNAS 100 8466-8471. (doi:10.1073/pnas.1032913100)
190. Paz K, Hemi R, LeRoith D, Karasik A, Elhanany E, Kanety H & Zick Y 1997 Elevated serine/threonine phosphorylation of IRS-1 and IRS-2 inhibits their binding to the juxtamembrane region of the insulin receptor and impairs their ability to undergo insulin-induced tyrosine phosphorylation. Journal of Biological Chemistry 272 29911-29918. (doi:10.1074/jbc.272.47.29911)
191. Pearce NJ, Arch JR, Clapham JC, Coghlan MP, Corcoran SL, Lister CA, Llano A, Moore GB, Murphy GJ, Smith SA, et al. 2004 Development of glucose intolerance in male transgenic mice overexpressing human glycogen synthase kinase-3β on a muscle-specific promoter. Metabolism 53 1322-1330. (doi:10.1016/j.metabol.2004.05.008)
192. Peluso G, Petillo O, Margarucci S, Mingrone G, Greco AV, Indiveri C, Palmieri F, Melone MA, Reda E & Calvani M 2002 Decreased mitochondrial carnitine translocase in skeletal muscles impairs utilization of fatty acids in insulin-resistant patients. Frontiers in Bioscience 7 a109-a116. (doi:10.2741/A745)
193. Pendergrass M, Koval J, Vogt C, Yki-Jarvinen H, Iozzo P, Pipek R, Ardehali H, Printz R, Granner D, DeFronzo RA, et al. 1998 Insulin induced hexokinase II expression is reduced in obesity and NIDDM. Diabetes 47 387-394. (doi:10.2337/diabetes.47.3.387)
194. Perreault M & Marette A 2001 Targeted disruption of inducible nitric oxide synthase protects against obesity-linked insulin resistance in muscle. Nature Medicine 7 1138-1143. (doi:10.1038/nm1001-1138)
195. 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. New England Journal of Medicine 350 664-671. (doi:10.1056/NEJMoa031314)
196. Phielix E, Schrauwen-Hinderling VB, Mensink M, Lenaers E, Meex R, Hoeks J, Kooi ME, Moonen-Kornips E, Sels JP, 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. (doi:10.2337/db08-0391)
197. Pilon G, Charbonneau A, White PJ, Dallaire P, Perreault M, Kapur S & Marette A 2010 Endotoxin mediated-iNOS induction causes insulin resistance via ONOO-induced tyrosine nitration of IRS-1 in skeletal muscle. PLoS ONE 5 e15912. (doi:10.1371/journal.pone.0015912)
198. Qiu X, Brown K, Hirschey MD, Verdin E & Chen D 2010 Calorie restriction reduces oxidative stress by SIRT3-mediated SOD2 activation. Cell Metabolism 12 662-667. (doi:10.1016/j. cmet.2010.11.015)
199. Radi R 2013 Peroxynitrite, a stealthy biological oxidant. Journal of Biological Chemistry 288 26464-26472. (doi:10.1074/jbc. R113.472936)
200. Radi R, Cassina A, Hodara R, Quijana C & Castro L 2002 Peroxynitrite reactions and formation in mitochondria. Free Radical Biology and Medicine 33 1451-1464. (doi:10.1016/S0891-5849(02)01111-5)
201. Randle PJ, Kerbey AL & Espinal J 1988 Mechanisms decreasing glucose oxidation in diabetes and starvation: role of lipid fuels and hormones. Diabetes/Metabolism Reviews 4 623-638. (doi:10.1002/dmr.5610040702)
202. Reed TT 2011 Lipid peroxidation and neurodegenerative disease. Free Radical Biology and Medicine 51 1302-1319. (doi:10.1016/j. freeradbiomed.2011.06.027)
203. Richey JM, Ader M, Moore D & Bergman RN 1999 Angiotensin II induces insulin resistance independent of changes in interstitial insulin. American Journal of Physiology 277 E920-E926.
204. Rindler PM, Crewe CL, Fernandes J, Kinter M & Szweda LI 2013 Redox regulation of insulin sensitivity due to enhanced fatty acid utilization in the mitochondria. American Journal of Physiology 305 H634-H643. (doi:10.1152/ajpheart.00799.2012)
205. Ristow M & Schmeisser S 2011 Extending life span by increasing oxidative stress. Free Radical Biology and Medicine 51 327-336. (doi:10.1016/j.freeradbiomed.2011.05.010)
206. 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. (doi:10.2337/diabetes.54.1.8)
207. Ritov VB, Menshikova EV, Azuma K, Wood R, Toledo FG, Goodpaster BH, Ruderman NB & Kelley DE 2010 Deficiency of electron transport chain in human skeletal muscle mitochondria in type 2 diabetes mellitus and obesity. American Journal of Physiology 298 E49-E58. (doi:10.1152/ajpendo.00317.2009)
208. Roos G & Messens J 2011 Protein sulfenic acid formation: from cellular damage to redox regulation. Free Radical Biology and Medicine 51 314-326. (doi:10.1016/j.freeradbiomed.2011.04.031)
209. Sakamoto K & Holman GD 2008 Emerging role for AS160/TBC1D4 and TBC1D1 in the regulation of GLUT4 traffic. American Journal of Physiology 295 E29-E37. (doi:10.1152/ajpcell.00466.2007)
210. Sakellariou GK, Vasilaki A, Palomero J, Kayani A, Zibrik L, McArdle A & Jackson MJ 2013 Studies of mitochondrial and nonmitochondrial sources implicate nicotinamide adenine dinucleotide phosphate oxidase(s) in the increased skeletal muscle superoxide generation that occurs during contractile activity. Antioxidants and Redox Signaling 18 603-621. (doi:10.1089/ars.2012.4623)
211. Sakellariou GK, Jackson MJ & Vasilaki M 2014 Redefining the major contributors to superoxide production in contracting skeletal muscle. The role of NAD(P)H oxidases. Free Radical Research 48 12-29. (doi:10. 3109/10715762.2013.830718)
212. Samjoo IA, Safdar A, Hamadeh MJ, Glover AW, Mocellin NJ, Santana J, Little JP, Steinberg GR, Raha S & Tarnopolsky MA 2013 Markers of skeletal muscle mitochondrial function and lipid accumulation are moderately associated with the homeostasis model assessment index of insulin resistance in obese men. PLoS ONE 8 e66322. (doi:10.1371/journal.pone.0066322)
213. Samocha-Bonet D, Campbell LV, Mori TA, Croft KD, Greenfield JR, Turner N & Heilbronn LK 2012 Overfeeding reduces insulin sensitivity and increases oxidative stress, without altering markers of mitochondrial content and function in humans. PLoS ONE 7 e36320. (doi:10.1371/journal.pone.0036320)
214. Schmieder RE, Hilgers KF, Schlaich MP & Schmidt BM 2007 Reninangiotensin system and cardiovascular risk. Lancet 369 1208-1219. (doi:10.1016/S0140-6736(07)60242-6)
215. Schoenmakers E, Agostini M, Mitchell C, Schoenmakers N, Papp L, Rajanayagam O, Padidela R, Ceron-Gutierrez L, Doffinger R, Prevosto C, et al. 2010 Mutations in the selenocysteine insertion sequence-binding protein 2 gene lead to a multisystem selenoprotein deficiency disorder in humans. Journal of Clinical Investigation 120 4220-4235. (doi:10.1172/JCI43653)
216. Schonfeld P & Wojtczak L 2008 Fatty acids as modulators of the cellular production of reactive oxygen species. Free Radical Biology and Medicine 45 231-241. (doi:10.1016/j.freeradbiomed.2008.04.029)
217. Schrauwen-Hinderling VB, Kooi ME, Hesselink MK, Jeneson JA, Backes WH, van Echteld CJ, van Engelshoven JM, Mensink M & Schrauwen P 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. (doi:10.1007/s00125-006-0475-1)
218. Sebastián D, Hernández-Alvarez MI, Segalés J, Sorianello E, Muñoz JP, Sala D, Waget A, Liesa M, Paz JC, Gopalacharyulu P, et al. 2012 Mitofusin 2 (Mfn2) links mitochondrial and endoplasmic reticulum function with insulin signaling and is essential for normal glucose homeostasis. PNAS 109 5523-5528. (doi:10.1073/pnas.1108220109)
219. 2 emission during long-chain fatty acid oxidation. Journal of Biological Chemistry 285 5748-5758. (doi:10.1074/jbc.M109.026203)
220. Sethi JK & Vidal-Puig AJ 2007 Thematic review series: adipocyte biology. Adipose tissue function and plasticity orchestrate nutritional adaptation. Journal of Lipid Research 48 1253-1262. (doi:10.1194/jlr. R700005-JLR200)
221. Shelley P, Martin-Gronert MS, Rowlerson A, Poston L, Heales SJ, Hargreaves IP, McConnell JM, Ozanne SE & Fernandez-Twinn DS 2009 Altered skeletal muscle insulin signaling and mitochondrial complex II-III linked activity in adult offspring of obese mice. American Journal of Physiology 297 R675-R681. (doi:10.1152/ajpregu.00146.2009)
222. Shimomura I, Funahashi T, Takahashi M, Maeda K, Kotani K, Nakamura T, Yamashita S, Miura M, Fukuda Y, Takemura K, et al. 1996 Enhanced expression of PAI-1 in visceral fat: possible contributor to vascular disease in obesity. Nature Medicine 2 800-803. (doi:10.1038/nm0796-800)
223. Shiuchi T, Iwai M, Li HS, Wu L, Min LJ, Li JM, Okumura M, Cui TX & Horiuchi M 2004 Angiotensin II type-1 receptor blocker valsartan enhances insulin sensitivity in skeletal muscles of diabetic mice. Hypertension 43 1003-1010. (doi:10.1161/01. HYP.0000125142.41703.64)
224. Shulman GI 2000 Cellular mechanisms of insulin resistance. Journal of Clinical Investigation 106 171-176. (doi:10.1172/JCI10583)
225. Sies H 1997 Oxidative stress: oxidants and antioxidants. Experimental Physiology 82 291-295. (doi:10.1113/expphysiol.1997.sp004024)
226. Simoneau J-A, Veerkamp JH, Turcotte LP & Kelley DE 1999 Markers of capacity to utilize fatty acids in human skeletal muscle: relation to insulin resistance and obesity and effects of weight loss. FASEB Journal 13 2051-2060.
227. Sleigh A, Raymond-Barker P, Thackray K, Porter D, Hatunic M, Vottero A, Burren C, Mitchell C, McIntyre M, Brage S, et al. 2011 Mitochondrial dysfunction in patients with primary congenital insulin resistance. Journal of Clinical Investigation 121 2457-2461. (doi:10.1172/JCI46405)
228. Soliman MA, Abdel Rahman AM, Lamming DW, Birsoy K, Pawling J, Frigolet ME, Lu H, Fantus IG, Pasculescu A, Zheng Y, et al. 2014 The adaptor protein p66Shc inhibits mTOR-dependent anabolic metabolism. Science Signaling 7 ra17. (doi:10.1126/scisignal.2004785)
229. Someya S, Yu W, Hallows WC, Xu J, Vann JM, Leeuwenburgh C, Tanokura M, Denu JM & Prolla TA 2010 Sirt3 mediates reduction of oxidative damage and prevention of age-related hearing loss under caloric restriction. Cell 143 802-812. (doi:10.1016/j.cell.2010.10.002)
230. 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. (doi:10.2337/diabetes.54.7.1926)
231. Suh YA, Arnold RS, Lassegue B, Shi J, Xu X, Sorescu D, Chung AB, Griendling KK & Lambeth JD 1999 Cell transformation by the superoxide-generating oxidase Mox1. Nature 401 79-82. (doi:10.1038/43459)
232. 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 Medicine 4 e154. (doi:10.1371/journal. pmed.0040154)
233. Taddeo EP, Laker RC, Breen DS, Akhtar YN, Kenwood BM, Liao JA, Zhang M, Fazakerley DJ, Tomsig JL, Harris TE, et al. 2014 Opening of the mitochondrial permeability transition pore links mitochondrial dysfunction to insulin resistance in skeletal muscle. Molecular Metabolism 3 124-134. (doi:10.1016/j.molmet.2013.11.003)
234. Takada S, Kinugawa S, Hirabayashi K, Suga T, Yokota T, Takahashi M, Fukushima A, Homma T, Ono T, Sobirin MA, et al. 2013 Angiotensin II receptor blocker improves the lowered exercise capacity and impaired mitochondrial function of the skeletal muscle in type 2 diabetic mice. Journal of Applied Physiology 114 844-857. (doi:10.1152/japplphysiol.00053.2012)
235. Teodoro BG, Baraldi FG, Sampaio IH, Bomfim LH, Queiroz AL, Passos MA, Carneiro EM, Alberici LC, Gomis R, Amaral FG, et al. 2014 Melatonin prevents mitochondrial dysfunction and insulin resistance in rat skeletal muscle. Journal of Pineal Research 57 155-167. (doi:10.1111/jpi.12157)
236. Tirosh A, Potashnik R, Bashan N & Rudich A 1999 Oxidative stress disrupts insulin-induced cellular redistribution of insulin receptor substrate-1 and phosphatidylinositol 3-kinase in 3T3-L1 adipocytes. A putative cellular mechanism for impaired protein kinase B activation and GLUT4 translocation. Journal of Biological Chemistry 274 10595-10602. (doi:10.1074/jbc.274.15.10595)
237. Tomilov AA, Bicocca V, Schoenfeld RA, Giorgio M, Migliaccio E, Ramsey JJ, Hagopian K, Pelicci PG & Cortopassi GA 2010 Decreased superoxide production in macrophages of long-lived p66Shc knockout mice. Journal of Biological Chemistry 285 1153-1165. (doi:10.1074/jbc.M109.017491)
238. Tonks NK 2006 Protein tyrosine phosphatases: from genes, to function, to disease. Nature Reviews Molecular Cell Biology 7 833-846. (doi:10.1038/nrm2039)
239. Troisi RJ, Weiss ST, Parker DR, Sparrow D, Young JB & Landsberg L 1991 Relation of obesity and diet to sympathetic nervous system activity. Hypertension 17 669-677. (doi:10.1161/01.HYP.17.5.669)
240. Turner N, Bruce CR, Beale SM, Hoehn KL, So T, Rolph MS & Cooney GJ 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. (doi:10.2337/db07-0093)
241. Turrens JF & Boveris AV 1980 Generation of superoxide anion by the NADH dehydrogenase of bovine heart mitochondria. Biochemical Journal 191 421-427. (doi:10.1042/bj1910421)
242. Uckaya G, Ozata M, Sonmez A, Kinalp C, Eyileten T, Bingol N, Koc B, Kocabalkan F & Ozdemir IC 1999 Plasma leptin levels strongly correlate with plasma rennin activity in patients with essential hypertension. Hormone and Metabolic Research 31 435-438. (doi:10.1055/s-2007-978769)
243. Valko M, Leibfritz D, Moncol J, Cronin MT, Mazur M & Telser J 2007 Free radicals and antioxidants in normal physiological functions and human disease. International Journal of Biochemistry and Cell Biology 39 44-84. (doi:10.1016/j.biocel.2006.07.001)
244. Vannuvel K, Renard P, Raes M & Arnould T 2013 Functional and morphological impact of ER stress on mitochondria. Journal of Cellular Physiology 228 1802-1818. (doi:10.1002/jcp.24360)
245. Venditti P & Di Meo S 2006 Thyroid hormone-induced oxidative stress. Cellular and Molecular Life Sciences 63 414-434. (doi:10.1007/s00018-005-5457-9)
246. Venditti P, Di Stefano L & Di Meo S 2013 Mitochondrial metabolism of reactive oxygen species. Mitochondrion 13 71-82. (doi:10.1016/j. mito.2013.01.008)
247. Venditti P, Napolitano G & Di Meo S 2015 Role of mitochondria and other ROS sources in hyperthyroidism-linked oxidative stress. Immunology, Endocrine and Metabolic Agents in Medicinal Chemistry 15 5-36. (doi:10.2174/187152221501150710124951)
248. Vercesi AE, Kowaltowski AJ, Grijalba MT, Meinicke AR & Castilho RF 1997 The role of reactive oxygen species in mitochondrial permeability transition. Bioscience Reports 17 43-52. (doi:10.102 3/A:1027335217774)
249. Verdin E, Hirschey MD, Finley LW & Haigis MC 2010 Sirtuin regulation of mitochondria: energy production, apoptosis, and signaling. Trends in Biochemical Sciences 35 669-675. (doi:10.1016/j.tibs.2010.07.003)
250. Vettor R, Milan G, Rossato M & Federspil G 2005 Review article: adipocytokines and insulin resistance. Alimentary Pharmacology and Therapeutics 22 3-10. (doi:10.1111/j.1365-2036.2005.02587.x)
251. Vieira H & Kroemer G 2003 Mitochondria as targets of apoptosis regulation by nitric oxide. IUBMB Life 55 613-616. (doi:10.1080/1521 6540310001639652)
252. Viitanen PV, Geiger PJ, Erickson-Viitanen S & Bessman SP 1984 Evidence for functional hexokinase compartmentation in rat skeletal muscle mitochondria. Journal of Biological Chemistry 259 9679-9686.
253. Vogel R, Wiesinger H, Hamprecht B & Dringen R 1999 The regeneration of reduced glutathione in rat forebrain mitochondria identifies metabolic pathways providing the NADPH required. Neuroscience Letters 275 97-100. (doi:10.1016/S0304-3940(99)00748-X)
254. Vogt C, Yki-Jarvinen H, Iozzo P, Pipek R, Pendergrass M, Koval J. Ardehali H, Printz R, Granner D, Defronzo R, et al. 1998 Effects of insulin on subcellular localization of hexokinase II in human skeletal muscle in vivo. Journal of Clinical Endocrinology and Metabolism 83 230-234. (doi:10.1210/jc.83.1.230)
255. Vogt C, Ardehali H, Iozzo P, Yki-Jarvinen H, Koval J, Maezono K, Pendergrass M, Printz R, Granner D, DeFronzo R, et al. 2000 Regulation of hexokinase II expression in human skeletal muscle in vivo. Metabolism 49 814-818. (doi:10.1053/meta.2000.6245)
256. Walker JE, Collinson IR, Van Raaij MJ & Runswick MJ 1995 Structural analysis of ATP synthase from bovine heart mitochondria. Methods in Enzymology 260 163-190. (doi:10.1016/0076-6879(95)60136-8)
257. Warren BE & Lou PH, Lucchinetti E, Zhang L, Clanachan AS, Affolter A, Hersberger M, Zaugg M & Lemieux H 2014 Early mitochondrial dysfunction in glycolytic muscle, but not oxidative muscle, of the fructose-fed insulin-resistant rat. American Journal of Physiology 306 E658-E667. (doi:10.1152/ajpendo.00511.2013)
258. Wei Y, Sowers JR, Nistala R, Gong H, Uptergrove G M-E, Clark SE, Morris EM, Szary N, Manrique C & Stump CS 2006 Angiotensin II-induced NADPH oxidase activation impairs insulin signaling in skeletal muscle cells. Journal of Biological Chemistry 281 35137-35146. (doi:10.1074/jbc.M601320200)
259. Wei Y, Sowers JR, Clark SE, Li W, Ferrario CM & Stump CS 2008 Angiotensin II-induced skeletal muscle insulin resistance mediated by NF-kB activation via NADPH oxidase. American Journal of Physiology 294 E345-E351. (doi:10.1152/ajpcell.00216.2007)
260. Wessels B, van den Broek NM, Ciapaite J, Houten SM, Wanders RJ, Nicolay K & Prompers JJ 2015 Carnitine supplementation in highfat diet-fed rats does not ameliorate lipid-induced skeletal muscle mitochondrial dysfunction in vivo. American Journal of Physiology 309 E670-E678. (doi:10.1152/ajpendo.00144.2015)
261. White MF 2002 IRS proteins and the common path to diabetes. American Journal of Physiology 283 E413-E422. (doi:10.1152/ajpendo.00514.2001)
262. White MF & Kahn CR 1994 The insulin signaling system. Journal of Biological Chemistry 269 1-4.
263. Wijesekara N, Konrad D, Eweida M, Jefferies C, Liadis N, Giacca A, Crackower M, Suzuki A, Mak TW, Kahn CR, et al. 2005 Musclespecific Pten deletion protects against insulin resistance and diabetes. Molecular and Cellular Biology 25 1135-1145. (doi:10.1128/MCB.25.3.1135-1145.2005)
264. Winterbourn CC & Metodiewa D 1995 Reaction of superoxide with glutathione and other thiols. Methods in Enzymology 251 81-86. (doi:10.1016/0076-6879(95)51112-1)
265. Wredenberg A, Freyer C, Sandström ME, Katz A, Wibom R, Westerblad H & Larsson NG 2006 Respiratory chain dysfunction in skeletal muscle does not cause insulin resistance. Biochemical and Biophysical Research Communications 350 202-207. (doi:10.1016/j.bbrc.2006.09.029)
266. Wu Z, Rogers B, Kachi S, Hackett SF, Sick A & Campochiaro PA 2006 Reduction of p66Shc suppresses oxidative damage in retinal pigmented epithelial cells and retina. Journal of Cellular Physiology 209 996-1005. (doi:10.1002/jcp.20819)
267. Wu R, Smeele KM, Wyatt E, Ichikawa Y, Eerbeek O, Sun L, Chawla K, Hollmann MW, Nagpal V, Heikkinen S, et al. 2011a Reduction in hexokinase II levels results in decreased cardiac function and altered remodeling after ischemia/reperfusion injury. Circulation Research 108 60-69. (doi:10.1161/CIRCRESAHA.110.223115)
268. Wu S, Zhou F, Zhang Z & Xing D 2011b Mitochondrial oxidative stress causes mitochondrial fragmentation via differential modulation of mitochondrial fission-fusion proteins. FEBS Journal 278 941-954. (doi:10.1111/j.1742-4658.2011.08010.x)
269. Yamada T, Ida T, Yamaoka Y, Ozawa K, Takasan H & Honjo I 1975 Two distinct patterns of glucose intolerance in icteric rats and rabbits. Relationship to impaired liver mitochondria function. Journal of Laboratory and Clinical Medicine 86 38-45.
270. Yamauchi T, Kamon J, Minokoshi Y, Ito Y, Waki H, Uchida S, Yamashita S, Noda M, Kita S, Ueki K, et al. 2002 Adiponectin stimulates glucose utilization and fatty-acid oxidation by activating AMP-activated protein kinase. Nature Medicine 8 1288-1295. (doi:10.1038/nm788)
271. Yang C, Aye CC, Li X, Diaz Ramos A, Zorzano A & Mora S 2012 Mitochondrial dysfunction in insulin resistance: differential contributions of chronic insulin and saturated fatty acid exposure in muscle cells. Bioscience Reports 32 465-478. (doi:10.1042/BSR20120034)
272. Yu BP 1994 Cellular defenses against damage from reactive oxygen species. Physiological Reviews 74 139-162.
273. Yu T, Sheu SS, Robotham JL & Yoon Y 2008 Mitochondrial fission mediates high glucose-induced cell death through elevated production of reactive oxygen species. Cardiovascular Research 79 341-351. (doi:10.1093/cvr/cvn104)
274. Yuzefovych LV, Musiyenko SI, Wilson GL & Rachek LI 2013 Mitochondrial DNA damage and dysfunction, and oxidative stress are associated with endoplasmic reticulum stress, protein degradation and apoptosis in high fat diet-induced insulin resistance mice. PLoS ONE 8 e54059. (doi:10.1371/journal.pone.0054059)
275. Zhande R, Mitchell JJ, Wu J & Sun XJ 2002 Molecular mechanism of insulin induced degradation of insulin receptor substrate 1. Molecular and Cellular Biology 22 1016-1026. (doi:10.1128/MCB.22.4.1016-1026.2002)
276. Zierath JR, Krook A & Wallberg-Henriksson H 2000 Insulin action and insulin resistance in human skeletal muscle. Diabetologia 43 821-835. (doi:10.1007/s001250051457)
277. Zisman A, Peroni OD, Abel ED, Michael MD, Mauvais-Jarvis F, Lowell BB, Wojtaszewski JF, Hirshman MF, Virkamaki A, Goodyear LJ, et al. 2000 Targeted disruption of the glucose transporter 4 selectively in muscle causes insulin resistance and glucose intolerance. Nature Medicine 6 924-928. (doi:10.1038/78693)
278. Zorov DB, Filburn CR, Klotz L-O, Zweier JL & Sollott SJ 2000 Reactive oxygen species (ROS)-induced ROS release: a new phenomenon accompanying induction of the mitochondrial permeability transition in cardiacmyocytes. Journal of Experimental Medicine 192 1001-1014. (doi:10.1084/jem.192.7.1001)