Mitochondria as potential targets in antidiabetic therapy

Handbook of Experimental Pharmacology

Volumn 203, Issue , 2011, Pages 331-356

  Moreira, Paula I ^a   Oliveira, Catarina R ^a  

^a UNIVERSITY OF COIMBRA   (Portugal)

Author keywords

Cardiac muscle; Diabetes; Insulin; Insulin sensitizing drugs; Liver; Mitochondria; Mitochondria targeted antioxidants; Nervous tissue; Pancreas; Skeletal muscle

Indexed keywords

ANTIDIABETIC AGENT; ANTIOXIDANT; BIOTIN; CIGLITAZONE; GLITAZONE DERIVATIVE; INSULIN; INSULIN SENSITIZING AGENT; LEVACECARNINE; MITOQ; NICOTINAMIDE; PEPTIDE DERIVATIVE; PIOGLITAZONE; ROSIGLITAZONE; SS 20; SS 31; THIOCTIC ACID; UBIDECARENONE; UBIQUINONE; UNCLASSIFIED DRUG; PANCRELIPASE;

BRAIN; DIABETES MELLITUS; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DRUG EFFICACY; DRUG TARGETING; FRIEDREICH ATAXIA; HEART MUSCLE; HUMAN; HYPERGLYCEMIA; INSULIN RELEASE; INSULIN RESISTANCE; INSULIN SENSITIVITY; LIVER; MAXIMUM PLASMA CONCENTRATION; NERVOUS TISSUE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OXIDATIVE STRESS; PANCREAS; PANCREAS ISLET BETA CELL; PARKINSON DISEASE; PATHOGENESIS; PRIORITY JOURNAL; REVIEW; SKELETAL MUSCLE; ANIMAL; DRUG EFFECT; HEART MITOCHONDRION; LIVER MITOCHONDRION; METABOLISM; MITOCHONDRION; MUSCLE MITOCHONDRION;

ANIMALS; ANTIOXIDANTS; DIABETES MELLITUS; HUMANS; HYPOGLYCEMIC AGENTS; INSULIN; INSULIN RESISTANCE; MITOCHONDRIA; MITOCHONDRIA, HEART; MITOCHONDRIA, LIVER; MITOCHONDRIA, MUSCLE; PANCRELIPASE;

EID: 79955615960     PISSN: 01712004     EISSN: None     Source Type: Book Series    
DOI: 10.1007/978-3-642-17214-4_14     Document Type: Review

References (141)

1. Ahrén B (2000) Autonomic regulation of islet hormone secretion - implications for health and disease. Diabetologia 43:393-410
2. Ahrén B (2005) Type 2 diabetes, insulin secretion and beta-cell mass. Curr Mol Med 5:275-286
3. Aliev G, Liu J, Shenk JC et al (2009) Neuronal mitochondrial amelioration by feeding acetyl-Lcarnitine and lipoic acid to aged rats. J Cell Mol Med 13:320-333
4. Anello M, Lupi R, Spampinato D et al (2005) Functional and morphological alterations of mitochondria in pancreatic beta cells from type 2 diabetic patients. Diabetologia 48:282-289 (Pubitemid 40543300)
5. Balkis Budin S, Othman F, Louis SR et al (2009) Effect of alpha lipoic acid on oxidative stress and vascular wall of diabetic rats. Rom J Morphol Embryol 50:23-30
6. Basu R, Oudit GY, Wang X et al (2009) Type 1 diabetic cardiomyopathy in the Akita (Ins2WT/C96Y) mouse model is characterized by lipotoxicity and diastolic dysfunction with preserved systolic function. Am J Physiol Heart Circ Physiol 297:H2096-H2108
7. Bedogni B, Pani G, Colavitti R et al (2003) Redox regulation of cAMP-responsive element-binding protein and induction of manganous superoxide dismutase in nerve growth factor-dependent cell survival. J Biol Chem 278:16510-16519 (Pubitemid 36799511)
8. Befroy DE, Petersen KF, Dufour S et al (2007) Impaired mitochondrial substrate oxidation in muscle of insulin-resistant offspring of type 2 diabetic patients. Diabetes 56:1376-1381 (Pubitemid 46715630)
9. Bijur GN, Jope RS (2003) Rapid accumulation of Akt in mitochondria following phosphatidylinositol 3-kinase activation. J Neurochem 87:1427-1435 (Pubitemid 38020576)
10. Bogacka I, Xie H, Bray GA, Smith SR (2005) Pioglitazone induces mitochondrial biogenesis in human subcutaneous adipose tissue in vivo. Diabetes 54:1392-1399 (Pubitemid 40586669)
11. Boirie Y, Short KR, Ahlman B et al (2001) Tissue-specific regulation of mitochondrial and cytoplasmic protein synthesis rates by insulin. Diabetes 50:2652-2658 (Pubitemid 33733114)
12. Bolten CW, Blanner PM, McDonald WG et al (2007) Insulin sensitizing pharmacology of thiazolidinediones correlates with mitochondrial gene expression rather than activation of PPARgamma. Gene Regul Syst Bio 1:73-82
13. Boudina S, Sena S, O'Neill BT et al (2005) Reduced mitochondrial oxidative capacity and increased mitochondrial uncoupling impair myocardial energetics in obesity. Circulation 112:2686-2695 (Pubitemid 41532606)
14. Boudina S, Sena S, Theobald H et al (2007) Mitochondrial energetics in the heart in obesity-related diabetes: direct evidence for increased uncoupled respiration and activation of uncoupling proteins. Diabetes 56:2457-2466 (Pubitemid 47523253)
15. Boushel R, Gnaiger E, Schjerling P et al (2007) Patients with type 2 diabetes have normal mitochondrial function in skeletal muscle. Diabetologia 50:790-796 (Pubitemid 46355830)
16. Bugger H, Chen D, Riehle C et al (2009) Tissue-specific remodeling of the mitochondrial proteome in type 1 diabetic akita mice. Diabetes 58:1986-1997
17. Butler AE, Janson J, Bonner-Weir S et al (2003) Beta-cell deficit and increased beta-cell apoptosis in humans with type 2 diabetes. Diabetes 52:102-110 (Pubitemid 36042113)
18. Cardoso S, Correia S, Santos RX et al (2009a) Insulin is a two-edged knife on the brain. J Alzheimers Dis 18:483-507
19. Cardoso S, Santos R, Correia S et al (2009b) Insulin and insulin-sensitizing drugs in neurodegeneration: mitochondria as therapeutic targets. Pharmaceuticals 2:250-286
20. Coletta DK, Sriwijitkamol A, Wajcberg E et al (2009) Pioglitazone stimulates AMP-activated protein kinase signalling and increases the expression of genes involved in adiponectin signalling, mitochondrial function and fat oxidation in human skeletal muscle in vivo: a randomised trial. Diabetologia 52:723-732
21. Combs CK, Johnson DE, Karlo JC et al (2000) Inflammatory mechanisms in Alzheimer's disease: inhibition of beta-amyloid-stimulated proinflammatory responses and neurotoxicity by PPARgamma agonists. J Neurosci 20:558-567 (Pubitemid 30225558)
22. Cooney GJ, Thompson AL, Furler SM et al (2002) Muscle long-chain acyl CoA esters and insulin resistance. Ann NY Acad Sci 967:196-207 (Pubitemid 34721906)
23. Cui L, Jeong H, Borovecki F et al (2006) Transcriptional repression of PGC-1alpha by mutant huntingtin leads to mitochondrial dysfunction and neurodegeneration. Cell 127:59-69 (Pubitemid 44466642)
24. Deng S, Vatamaniuk M, Huang X et al (2004) Structural and functional abnormalities in the islets isolated from type 2 diabetic subjects. Diabetes 53:624-632 (Pubitemid 38270631)
25. Dhanasekaran A, Kotamraju S, Kalivendi SV et al (2004) Supplementation of endothelial cells with mitochondria-targeted antioxidants inhibit peroxide-induced mitochondrial iron uptake, oxidative damage, and apoptosis. J Biol Chem 279:37575-37587 (Pubitemid 39195471)
26. Edwards JL, Quattrini A, Lentz SI et al (2010) Diabetes regulates mitochondrial biogenesis and fission in mouse neurons. Diabetologia 53:160-169
27. Ernster L, Forsmark P, Nordenbrand K (1992) The mode of action of lipid-soluble antioxidants in biological membranes: relationship between the effects of ubiquinol and vitamin E as inhibitors of lipid peroxidation in submitochondrial particles. Biofactors 3:241-248
28. Evans JL, Goldfine ID, Maddux BA, Grodsky GM (2003) Are oxidative stress-activated signaling pathways mediators of insulin resistance and beta-cell dysfunction? Diabetes 52:1-8
29. Fowler SP, Williams K, Resendez RG et al (2008) Fueling the obesity epidemic? Artificially sweetened beverage use and long-term weight gain. Obesity (Silver Spring) 16:1894-1900
30. Fox CS, Coady S, Sorlie PD et al (2007) Increasing cardiovascular disease burden due to diabetes mellitus: the Framingham Heart Study. Circulation 115:1544-1550 (Pubitemid 46648639)
31. Fuenzalida K, Quintanilla R, Ramos P et al (2007) Peroxisome proliferator-activated receptor γ up-regulates the Bcl-2 anti-apoptotic protein in neurons and induces mitochondrial stabilization and protection against oxidative stress and apoptosis. J Biol Chem 282:37006-37015
32. Fujisawa K, Nishikawa T, Kukidome D et al (2009) TZDs reduce mitochondrial ROS production and enhance mitochondrial biogenesis. Biochem Biophys Res Commun 379:43-48
33. Galderisi M, Anderson KM, Wilson PW, Levy D (1991) Echocardiographic evidence for the existence of a distinct diabetic cardiomyopathy (the Framingham Heart Study). Am J Cardiol 68:85-89
34. Gerstein HC, Miller ME, Byington RP et al (2008) Effects of intensive glucose lowering in type 2 diabetes. N Engl J Med 358:2545-2559 (Pubitemid 351831356)
35. Ghosh S, Patel N, Rahn D et al (2007) The thiazolidinedione pioglitazone alters mitochondrial function in human neuron-like cells. Mol Pharmacol 71:1695-1702 (Pubitemid 47010922)
36. Gnoni GV, Giudetti AM, Mercuri E et al (2010) Reduced activity and expression of mitochondrial citrate carrier in streptozotocin-induced diabetic rats. Endocrinology 151:1551-1559
37. Greenfield V, Cheung O, Sanyal AJ (2008) Recent advances in nonalcholic fatty liver disease. Curr Opin Gastroenterol 24:320-327 (Pubitemid 351535891)
38. Gurlo T, Ryazantsev S, Huang CJ et al (2010) Evidence for proteotoxicity in beta cells in type 2 diabetes: toxic islet amyloid polypeptide oligomers form intracellularly in the secretory pathway. Am J Pathol 176:861-869
39. Gustafsson H, Söderdahl T, Jönsson G et al (2004) Insulin-like growth factor type 1 prevents hyperglycemia-induced uncoupling protein 3 down-regulation and oxidative stress. J Neurosci Res 77:285-291 (Pubitemid 38859413)
40. Handschin C, Spiegelman BM (2006) Peroxisome proliferator-activated receptor gamma coactivator 1 coactivators, energy homeostasis, and metabolism. Endocr Rev 27:728-735 (Pubitemid 44936056)
41. Hasan NM, Longacre MJ, Stoker SW et al (2008) Impaired anaplerosis and insulin secretion in insulinoma cells caused by small interfering RNA-mediated suppression of pyruvate carboxylase. J Biol Chem 283:28048-28059
42. Højlund K, Wrzesinski K, Larsen PM et al (2003) Proteome analysis reveals phosphorylation of ATP synthase beta -subunit in human skeletal muscle and proteins with potential roles in type 2 diabetes. J Biol Chem 278:10436-10442 (Pubitemid 36800309)
43. Holloszy JO (2009) Skeletal muscle "mitochondrial deficiency" does not mediate insulin resistance. Am J Clin Nutr 89:463S-466S
44. Hudson BI, Wendt T, Bucciarelli LG et al (2005) Diabetic vascular disease: it's all the RAGE. Antioxid Redox Signal 7:1588-1600 (Pubitemid 41767994)
45. Hunter RL, Choi DY, Ross SA, Bing G (2008) Protective properties afforded by pioglitazone against intrastriatal LPS in Sprague-Dawley rats. Neurosci Lett 432:198-201
46. Hwang PM, Bunz F, Yu J et al (2001) Ferredoxin reductase affects p53-dependent, 5-fluorouracil-induced apoptosis in colorectal cancer cells. Nat Med 7:1111-1117 (Pubitemid 33010018)
47. Inestrosa NC, Godoy JA, Quintanilla RA et al (2005) Peroxisome proliferator-activated receptor gamma is expressed in hippocampal neurons and its activation prevents beta-amyloid neurodegeneration: role of Wnt signaling. Exp Cell Res 304:91-104 (Pubitemid 40227422)
48. Ishihara M, Inoue I, Kawagoe T et al (2001) Diabetes mellitus prevents ischemic preconditioning in patients with a first acute anterior wall myocardial infarction. J Am Coll Cardiol 38:1007-1011 (Pubitemid 32912703)
49. Jauslin ML, Meier T, Smith RA, Murphy MP (2003) Mitochondria targeted antioxidants protect Friedreich Ataxia fibroblasts from endogenous oxidative stress more effectively than untargeted antioxidants. FASEB J 17:1972-1974
50. Jung TW, Lee JY, Shim WS et al (2006) Rosiglitazone protects human neuroblastoma SH-SY5Y cells against acetaldehyde-induced cytotoxicity. Biochem Biophys Res Commun 340:221-227 (Pubitemid 41827669)
51. Jung TW, Lee JY, Shim WS et al (2007) Rosiglitazone protects human neuroblastoma SH-SY5Y cells against MPP+ induced cytotoxicity via inhibition of mitochondrial dysfunction and ROS production. J Neurol Sci 253:53-60 (Pubitemid 46185454)
52. Kalichman MW, Powell HC, Mizisin AP (1998) Reactive, degenerative, and proliferative Schwann cell responses in experimental galactose and human diabetic neuropathy. Acta Neuropathol 95:47-56 (Pubitemid 28075926)
53. Kalofoutis C, Piperi C, Kalofoutis A et al (2007) Type II diabetes mellitus and cardiovascular risk factors: current therapeutic approaches. Exp Clin Cardiol 12:17-28 (Pubitemid 46566811)
54. Kemp GJ (2008) The interpretation of abnormal 31P magnetic resonance saturation transfer measurements of Pi/ATP exchange in insulin-resistant skeletal muscle. Am J Physiol Endocrinol Metab 294:E640-622
55. Kim JY, Hickner RC, Cortright RL et al (2000) Lipid oxidation is reduced in obese human skeletal muscle. Am J Physiol Endocrinol Metab 279:E1039-E1044
56. Kohjima M, Enjoji M, Higuchi N et al (2007) Re-evaluation of fatty acid metabolism-related gene expression in nonalcoholic fatty liver disease. Int J Mol Med 20:351-358
57. Kraegen EW, Cooney GJ, Turner N (2008) Muscle insulin resistance: a case of fat overconsumption, not mitochondrial dysfunction. Proc Natl Acad Sci USA 105:7627-7628 (Pubitemid 351872687)
58. Kummer MP, Heneka MT (2008) PPARs in Alzheimer's disease. PPAR Res 2008:403896
59. Kuo WW, Chung LC, Liu CT et al (2009) Effects of insulin replacement on cardiac apoptotic and survival pathways in streptozotocin-induced diabetic rats. Cell Biochem Funct 27:479-487
60. Lee S, Jeong SY, Lim WC et al (2007) Mitochondrial fission and fusion mediators, hFis1 and OPA1, modulate cellular senescence. J Biol Chem 282:22977-22983 (Pubitemid 47267359)
61. Leinninger GM, Backus C, Sastry AM et al (2006) Mitochondria in DRG neurons undergo hyperglycemic mediated injury through Bim, Bax and the fission protein Drp1. Neurobiol Dis 23:11-22 (Pubitemid 44192383)
62. Leloup C, Tourrel-Cuzin C, Magnan C et al (2009) Mitochondrial reactive oxygen species are obligatory signals for glucose-induced insulin secretion. Diabetes 58:673-681
63. Li CJ, Zhang QM, Li MZ et al (2009a) Attenuation of myocardial apoptosis by alpha-lipoic acid through suppression of mitochondrial oxidative stress to reduce diabetic cardiomyopathy. Chin Med J 122:2580-2586
64. Li Y, Wu H, Khardori R et al (2009b) Insulin-like growth factor-1 receptor activation prevents high glucose-induced mitochondrial dysfunction, cytochrome-c release and apoptosis. Biochem Biophys Res Commun 384:259-264
65. Lillioja S, Young AA, Culter CL et al (1987) Skeletal muscle capillary density and fiber type are possible determinants of in vivo insulin resistance in man. J Clin Invest 80:415-424
66. Lowell BB, Shulman GI (2005) Mitochondrial dysfunction and type 2 diabetes. Science 307:384-387 (Pubitemid 40139974)
67. Lu C, Zhang D, Whiteman M, Armstrong JS (2008) Is antioxidant potential of the mitochondrial targeted ubiquinone derivative MitoQ conserved in cells lacking mtDNA? Antioxid Redox Signal 10:651-660
68. Lu H, Koshkin V, Allister EM et al (2010) Molecular and metabolic evidence for mitochondrial defects associated with beta-cell dysfunction in a mouse model of type 2 diabetes. Diabetes 59:448-459
69. Mariappan N, Elks CM, Sriramula S et al (2010) NF-kappaB-induced oxidative stress contributes to mitochondrial and cardiac dysfunction in type II diabetes. Cardiovasc Res 85:473-483
70. McGavock JM, Lingvay I, Zib I et al (2007) Cardiac steatosis in diabetes mellitus: a 1H-magnetic resonance spectroscopy study. Circulation 116:1170-1175 (Pubitemid 47360218)
71. Misu H, Takamura T, Matsuzawa N et al (2007) Genes involved in oxidative phosphorylation are coordinately upregulated with fasting hyperglycaemia in livers of patients with type 2 diabetes. Diabetologia 50:268-277
72. Modi K, Santani DD, Goyal RK, Bhatt PA (2006) Effect of coenzyme Q10 on catalase activity and other antioxidant parameters in streptozotocin-induced diabetic rats. Biol Trace Elem Res 109:25-34
73. Mogensen M, Sahlin K, Fernström M et al (2007) Mitochondrial respiration is decreased in skeletal muscle of patients with type 2 diabetes. Diabetes 56:1592-1599 (Pubitemid 46842617)
74. Mootha VK, Lindgren CM, Eriksson KF et al (2003) PGC-1alpha-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat Genet 34:267-273 (Pubitemid 36792858)
75. Moreira PI, Santos MS, Moreno AM (2003) Increased vulnerability of brain mitochondria in diabetic (Goto-Kakizaki) rats with aging and amyloid-beta exposure. Diabetes 52:1449-1456 (Pubitemid 36666200)
76. Moreira PI, Santos MS, Sena C et al (2005a) Insulin protects against amyloid beta-peptide toxicity in brain mitochondria of diabetic rats. Neurobiol Dis 18:628-637 (Pubitemid 40332720)
77. Moreira PI, Santos MS, Sena C et al (2005b) CoQ10 therapy attenuates amyloid beta-peptide toxicity in brain mitochondria isolated from aged diabetic rats. Exp Neurol 196:112-119 (Pubitemid 41416653)
78. Moreira PI, Rolo AP, Sena C et al (2006) Insulin attenuates diabetes-related mitochondrial alterations: a comparative study. Med Chem 2:299-308 (Pubitemid 44083149)
79. Moreira PI, Santos MS, Seiça R, Oliveira CR (2007a) Brain mitochondrial dysfunction as a link between Alzheimer's disease and diabetes. J Neurol Sci 257:206-214 (Pubitemid 46856489)
80. Moreira PI, Harris PLR, Zhu X et al (2007b) Lipoic acid and N-acetyl cysteine decrease mitochondrial-related oxidative stress in Alzheimer disease patient fibroblasts. J Alzheimer Dis 12:195-206 (Pubitemid 47509369)
81. Moreira PI, Cardoso SM, Pereira CM et al (2009) Mitochondria as a therapeutic target in Alzheimer's disease and diabetes. CNS Neurol Disord Drug Targets 8:492-511
82. Moreira PI, Carvalho C, Zhu X et al (2010) Mitochondrial dysfunction is a trigger of Alzheimer's disease pathophysiology. Biochim Biophys Acta 1802:2-10
83. Morino K, Petersen KF, Dufour S et al (2005) Reduced mitochondrial density and increased IRS-1 serine phosphorylation in muscle of insulin-resistant offspring of type 2 diabetic parents. J Clin Invest 115:3587-3593 (Pubitemid 43121847)
84. Muoio DM, Newgard CB (2008) Mechanisms of disease: molecular and metabolic mechanisms of insulin resistance and beta-cell failure in type 2 diabetes. Nat Rev Mol Cell Biol 9:193-205 (Pubitemid 351301824)
85. Murphy MP, Smith RA (2000) Drug delivery to mitochondria: the key to mitochondrial medicine. Adv Drug Deliv Rev 41:235-250 (Pubitemid 30122962)
86. Nishikawa T, Edelstein D, Du XL et al (2000) Normalizing mitochondrial superoxide production blocks three pathways of hyperglycaemic damage. Nature 404:787-790 (Pubitemid 30212409)
87. O'Connor MD, Landahl H, Grodsky GM (1980) Comparison of storage- and signal-limited models of pancreatic insulin secretion. Am J Physiol 238:R378-R389
88. Oliveira PJ, Seiça R, Coxito PM et al (2003) Enhanced permeability transition explains the reduced calcium uptake in cardiac mitochondria from streptozotocin-induced diabetic rats. FEBS Lett 554:511-514 (Pubitemid 37412541)
89. Opie LH (2004) Fuels: aerobic and anaerobic metabolism. In: Opie LH (ed) The heart, physiology, from cell to circulation, 4th edn. Lippincott - Raven, Philadelphia
90. Patel A, MacMahon S, Chalmers J et al (2008) Intensive blood glucose control and vascular outcomes in patients with type 2 diabetes. N Engl J Med 358:2560-2572 (Pubitemid 351831357)
91. Patti ME, Corvera S (2010) The role of mitochondria in the pathogenesis of type 2 diabetes. Endocrinol Rev 31(3):364-395
92. 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)
93. Pérez-Carreras M, Del Hoyo P, Martín MA et al (2003) Defective hepatic mitochondrial respiratory chain in patients with nonalcoholic steatohepatitis. Hepatology 38:999-1007 (Pubitemid 37221683)
94. Perseghin G, Scifo P, Danna M et al (2002) Normal insulin sensitivity and IMCL content in overweight humans are associated with higher fasting lipid oxidation. Am J Physiol Endocrinol Metab 283:E556-E564 (Pubitemid 35230493)
95. Petersen KF, Dufour S, Befroy D et al (2004) Impaired mitochondrial activity in the insulin-resistant offspring of patients with type 2 diabetes. N Engl J Med 350:664-671 (Pubitemid 38364625)
96. Petersen KF, Dufour S, Shulman GI (2005) Decreased insulin-stimulated ATP synthesis and phosphate transport in muscle of insulin-resistant offspring of type 2 diabetic parents. PLoS Med 2:e233
97. Petri S, Kiaei M, Damiano M et al (2006) Cell-permeable peptide antioxidants as a novel therapeutic approach in a mouse model of amyotrophic lateral sclerosis. J Neurochem 98:1141-1148 (Pubitemid 44127789)
98. 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
99. Pihlajamäki J, Boes T, Kim EY et al (2009) Thyroid hormone-related regulation of gene expression in human fatty liver. J Clin Endocrinol Metab 94:3521-3529
100. Puche JE, García-Fernández M, Muntané J et al (2008) Low doses of insulin-like growth factor-I induce mitochondrial protection in aging rats. Endocrinology 149:2620-2627 (Pubitemid 351574499)
101. Quintanilla RA, Jin YN, Fuenzalida K et al (2008) Rosiglitazone treatment prevents mitochondrial dysfunction in mutant huntingtin-expressing cells: possible role of peroxisome proliferatoractivated receptor-gamma (PPARgamma) in the pathogenesis of Huntington disease. J Biol Chem 283:25628-25637
102. Rabøl R, Larsen S, Højberg PM et al (2010) Regional anatomic differences in skeletal muscle mitochondrial respiration in type 2 diabetes and obesity. J Clin Endocrinol Metab 95:857-863
103. Reddy PH (2006) Mitochondrial oxidative damage in aging and Alzheimer's disease: implications for mitochondrially targeted antioxidant therapeutics. J Biomed Biotechnol 3:31372
104. Ritov VB, Menshikova EV, Azuma K et al (2009) Deficiency of electron transport chain in human skeletal muscle mitochondria in type 2 diabetes mellitus and obesity. Am J Physiol Endocrinol Metab 298:E49-E58
105. Ross SA, Gulve EA, Wang M (2004) Chemistry and biochemistry of type 2 diabetes. Chem Rev 104:1255-1282
106. Roy Chowdhury SK, Zherebitskaya E, Smith DR et al (2010) Mitochondrial respiratory chain dysfunction in dorsal root ganglia of streptozotocin-induced diabetic rats and its correction by insulin treatment. Diabetes 59(4):1082-1091
107. Sack MN (2009) Type 2 diabetes, mitochondrial biology and the heart. J Mol Cell Cardiol 46:842-849
108. Sanderson TH, Kumar R, Sullivan JM, Krause GS (2008) Insulin blocks cytochrome c release in the reperfused brain through PI3-K signaling and by promoting Bax/Bcl-XL binding. J Neurochem 106:1248-1258
109. Sanyal AJ, Campbell-Sargent C, Mirshahi F et al (2001) Nonalcoholic steatohepatitis: association of insulin resistance and mitochondrial abnormalities. Gastroenterology 120:1183-1192 (Pubitemid 32246672)
110. Sasaki H, Schmelzer JD, Zollman PJ, Low PA (1997) Neuropathology and blood flow of nerve, spinal roots and dorsal root ganglia in longstanding diabetic rats. Acta Neuropathol 93:118-128 (Pubitemid 27060903)
111. Satapati S, He T, Inagaki T et al (2008) Partial resistance to peroxisome proliferator-activated receptor-alpha agonists in ZDF rats is associated with defective hepatic mitochondrial metabolism. Diabetes 57:2012-2021
112. Scheuermann-Freestone M, Clarke K (2003) Abnormal cardiac high-energy phosphate metabolism in a patient with type 2 diabetes mellitus. J Cardiometab Syndr 1:366-368
113. Schmeichel AM, Schmelzer JD, Low PA (2003) Oxidative injury and apoptosis of dorsal root ganglion neurons in chronic experimental diabetic neuropathy. Diabetes 52:165-171 (Pubitemid 36042122)
114. 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)
115. Sena CM, Nunes E, Gomes A et al (2008) Supplementation of coenzyme Q10 and alphatocopherol lowers glycated hemoglobin level and lipid peroxidation in pancreas of diabetic rats. Nutr Res 28:113-121
116. Shen W, Hao J, Tian C et al (2008a) A combination of nutriments improves mitochondrial biogenesis and function in skeletal muscle of type 2 diabetic Goto-Kakizaki rats. PLoS One 3:e2328
117. Shen W, Liu K, Tian C et al (2008b) R-alpha-lipoic acid and acetyl-L-carnitine complementarily promote mitochondrial biogenesis in murine 3T3-L1 adipocytes. Diabetologia 51:165-174 (Pubitemid 50003767)
118. Siler-Marsiglio KI, Pan Q, Paiva M et al (2005) Mitochondrially targeted vitamin E and vitamin E mitigate ethanol-mediated effects on cerebellar granule cell antioxidant defense systems. Brain Res 1052:202-211 (Pubitemid 41116779)
119. Simoneau JA, Kelley DE (1997) Altered glycolytic and oxidative capacities of skeletal muscle contribute to insulin resistance in NIDDM. J Appl Physiol 83:166-171
120. Smith RA, Porteous CM, Gane AM, Murphy MP (1999) Selective targeting of an antioxidant to mitochondria. Eur J Biochem 263:709-716 (Pubitemid 29361943)
121. Smith RA, Porteous CM, Gane AM, Murphy MP (2003) Delivery of bioactive molecules to mitochondria in vivo. Proc Natl Acad Sci USA 100:5407-5412 (Pubitemid 36542718)
122. 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)
123. Strum JC, Shehee R, Virley D, Richardson J et al (2007) Rosiglitazone induces mitochondrial biogenesis in mouse brain. J Alzheimers Dis 11:45-51 (Pubitemid 46376708)
124. Suh JH, Wang H, Liu RM, Liu J, Hagen TM (2004) (R)-alpha-lipoic acid reverses the age-related loss in GSH redox status in post-mitotic tissues: evidence for increased cysteine requirement for GSH synthesis. Arch Biochem Biophys 423:126-135 (Pubitemid 38198222)
125. Szeto HH (2006) Cell-permeable, mitochondrial-targeted, peptide antioxidants. AAPS J 8: E277-E283
126. Szeto HH (2008) Mitochondria-targeted cytoprotective peptides for ischemia-reperfusion injury. Antioxid Redox Signal 10:601-619
127. Tabbi-Anneni I, Buchanan J, Cooksey RC, Abel ED (2008) Captopril normalizes insulin signaling and insulin-regulated substrate metabolism in obese (ob/ob) mouse hearts. Endocrinology 149:4043-4050
128. Takamura T, Misu H, Matsuzawa-Nagata N et al (2008) Obesity upregulates genes involved in oxidative phosphorylation in livers of diabetic patients. Obesity (Silver Spring) 16:2601-2609
129. The Diabetes Control and Complications Trial Research Group (1993) The effect of intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependent diabetes mellitus. N Engl J Med 329:977-986
130. Thomas DA, Stauffer C, Zhao K et al (2007) Mitochondrial targeting with antioxidant peptide SS- 31 prevents mitochondrial depolarization, reduces islet cell apoptosis, increases islet cell yield, and improves post-transplantation function. J Am Soc Nephrol 18:213-222 (Pubitemid 46053434)
131. Thyfault JP, Kraus RM, Hickner RC et al (2004) Impaired plasma fatty acid oxidation in extremely obese women. Am J Physiol Endocrinol Metab 287:E1076-E1081 (Pubitemid 39491949)
132. Trifunovic A, Larsson NG (2008) Mitochondrial dysfunction as a cause of ageing. J Intern Med 263:167-178
133. Tsuneki H, Sekizaki N, Suzuki T et al (2007) Coenzyme Q10 prevents high glucose-induced oxidative stress in human umbilical vein endothelial cells. Eur J Pharmacol 566:1-10 (Pubitemid 46782791)
134. UK Prospective Diabetes Study (UKPDS) Group (1998) Intensive blood-glucose control with sulphonylureas or insulin compared with conventional treatment and risk of complications in patients with type 2 diabetes (UKPDS 33). Lancet 352:837-853
135. Weydt P, Pineda VV, Torrence AE et al (2006) Thermoregulatory and metabolic defects in Huntington's disease transgenic mice implicate PGC-1alpha in Huntington's disease neurodegeneration. Cell Metab 4:349-362 (Pubitemid 44645069)
136. Wu JS, Lin TN, Wu KK (2009) Rosiglitazone and PPAR-gamma overexpression protect mitochondrial membrane potential and prevent apoptosis by upregulating anti-apoptotic Bcl-2 family proteins. J Cell Physiol 220:58-71
137. Yang L, Zhao K, Calingasan NY et al (2009) Mitochondria targeted peptides protect against 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine neurotoxicity. Antioxid Redox Signal 11:2095-2104
138. Yu T, Sheu SS, Robotham JL, Yoon Y (2008) Mitochondrial fission mediates high glucose-induced cell death through elevated production of reactive oxygen species. Cardiovasc Res 79:341-351 (Pubitemid 351951612)
139. Zhao K, Luo G, Zhao GM et al (2003) Transcellular transport of a highly polar 3+ net charge opioid tetrapeptide. J Pharmacol Exp Ther 304:425-432 (Pubitemid 36008956)
140. Zhao K, Zhao GM, Wu D et al (2004) Cell-permeable peptide antioxidants targeted to inner mitochondrial membrane inhibit mitochondrial swelling, oxidative cell death, and reperfusion injury. J Biol Chem 279:34682-34690 (Pubitemid 39318098)
141. Zhao K, Luo G, Giannelli S, Szeto HH (2005) Mitochondria-targeted peptide prevents mitochondrial depolarization and apoptosis induced by tert-butyl hydroperoxide in neuronal cell lines. Biochem Pharmacol 70:1796-1806 (Pubitemid 41612010)