Mechanisms of disease: Mitochondrial dysfunction in sensory neuropathy and other complications in diabetes

Handbook of Clinical Neurology

Volumn 126, Issue , 2014, Pages 353-377

  Fernyhough, Paul ^a,b   McGavock, Jonathan ^a,c  

^a UNIVERSITY OF MANITOBA   (Canada)

^b ST BONIFACE GENERAL HOSPITAL   (Canada)

^c MANITOBA INSTITUTE OF CHILD HEALTH   (Canada)

Author keywords

Bioenergetics; Cardiovascular disease; Diabetes; Dorsal root ganglia; Nerve regeneration; Neurodegeneration

Indexed keywords

ANIMAL; CARDIOVASCULAR DISEASES; DIABETES MELLITUS; DIABETIC NEUROPATHIES; HUMAN; METABOLISM; MITOCHONDRIAL DISEASES; MITOCHONDRION; NEURODEGENERATIVE DISEASES; OXIDATIVE STRESS; PHYSIOLOGY;

ANIMALS; CARDIOVASCULAR DISEASES; DIABETES MELLITUS; DIABETIC NEUROPATHIES; HUMANS; MITOCHONDRIA; MITOCHONDRIAL DISEASES; NEURODEGENERATIVE DISEASES; OXIDATIVE STRESS;

EID: 84921972920     PISSN: 00729752     EISSN: 22124152     Source Type: Book Series    
DOI: 10.1016/B978-0-444-53480-4.00027-8     Document Type: Chapter

References (229)

1. Akude E., Zherebitskaya E., Chowdhury S.K., et al. Diminished superoxide generation is associated with respiratory chain dysfunction and changes in the mitochondrial proteome of sensory neurons from diabetic rats. Diabetes 2011, 60:288-297.
2. 2 emission and cellular redox state link excess fat intake to insulin resistance in both rodents and humans. J Clin Invest 2009, 119:573-581.
3. Azzu V., Parker N., Brand M.D. High membrane potential promotes alkenal-induced mitochondrial uncoupling and influences adenine nucleotide translocase conformation. Biochem J 2008, 413:323-332.
4. Balaban R.S., Nemoto S., Finkel T. Mitochondria, oxidants, and aging. Cell 2005, 120:483-495.
5. Belfort R., Mandarino L., Kashyap S., et al. Dose-response effect of elevated plasma free fatty acid on insulin signaling. Diabetes 2005, 54:1640-1648.
6. Benton C.R., Nickerson J.G., Lally J., et al. Modest PGC-1alpha overexpression in muscle in vivo is sufficient to increase insulin sensitivity and palmitate oxidation in subsarcolemmal, not intermyofibrillar, mitochondria. J Biol Chem 2008, 283:4228-4240.
7. Benton C.R., Holloway G.P., Han X.X., et al. Increased levels of peroxisome proliferator-activated receptor gamma, coactivator 1 alpha (PGC-1alpha) improve lipid utilisation, insulin signalling and glucose transport in skeletal muscle of lean and insulin-resistant obese Zucker rats. Diabetologia 2010, 53:2008-2019.
8. Bergman R.N., Phillips L.S., Cobelli C. Physiologic evaluation of factors controlling glucose tolerance in man: measurement of insulin sensitivity and beta-cell glucose sensitivity from the response to intravenous glucose. J Clin Invest 1981, 68:1456-1467.
9. Bergmann S.R., Herrero P., Markham J., et al. Noninvasive quantitation of myocardial blood flow in human subjects with oxygen-15-labeled water and positron emission tomography. J Am Coll Cardiol 1989, 14:639-652.
10. Bertoni A.G., Clark J.M., Feeney P., et al. Suboptimal control of glycemia, blood pressure, and LDL cholesterol in overweight adults with diabetes: the Look AHEAD Study. J Diabetes Complications 2008, 22:1-9.
11. Boden G., Jadali F., White J., et al. Effects of fat on insulin-stimulated carbohydrate metabolism in normal men. J Clin Invest 1991, 88:960-966.
12. Borradaile N.M., Schaffer J.E. Lipotoxicity in the heart. Curr Hypertens Rep 2005, 7:412-417.
13. Boudina S., Abel E.D. Mitochondrial uncoupling: a key contributor to reduced cardiac efficiency in diabetes. Physiology (Bethesda) 2006, 21:250-258.
14. Boudina S., Sena S., O'Neill B.T., et al. Reduced mitochondrial oxidative capacity and increased mitochondrial uncoupling impair myocardial energetics in obesity. Circulation 2005, 112:2686-2695.
15. Boudina S., Sena S., Theobald H., et al. Mitochondrial energetics in the heart in obesity-related diabetes: direct evidence for increased uncoupled respiration and activation of uncoupling proteins. Diabetes 2007, 56:2457-2466.
16. Boule N.G., Haddad E., Kenny G.P., et al. Effects of exercise on glycemic control and body mass in type 2 diabetes mellitus: a meta-analysis of controlled clinical trials. JAMA 2001, 286:1218-1227.
17. Boussageon R., Bejan-Angoulvant T., Saadatian-Elahi M., et al. Effect of intensive glucose lowering treatment on all cause mortality, cardiovascular death, and microvascular events in type 2 diabetes: meta-analysis of randomised controlled trials. BMJ 2011, 343:d4169.
18. Brand M.D., Esteves T.C. Physiological functions of the mitochondrial uncoupling proteins UCP2 and UCP3. Cell Metab 2005, 2:85-93.
19. Brehm A., Krssak M., Schmid A.I., et al. Increased lipid availability impairs insulin-stimulated ATP synthesis in human skeletal muscle. Diabetes 2006, 55:136-140.
20. Brookes P.S., Yoon Y., Robotham J.L., et al. Calcium, ATP, and ROS: a mitochondrial love-hate triangle. Am J Physiol Cell Physiol 2004, 287:C817-C833.
21. Brownlee M. Biochemistry and molecular cell biology of diabetic complications. Nature 2001, 414:813-820.
22. Bugger H., Abel E.D. Mitochondria in the diabetic heart. Cardiovasc Res 2010, 88:229-240.
23. Bugger H., Chen D., Riehle C., et al. Tissue-specific remodeling of the mitochondrial proteome in type 1 diabetic akita mice. Diabetes 2009, 58:1986-1997.
24. Cai L., Wang J., Li Y., et al. Inhibition of superoxide generation and associated nitrosative damage is involved in metallothionein prevention of diabetic cardiomyopathy. Diabetes 2005, 54:1829-1837.
25. Camello-Almaraz C., Gomez-Pinilla P.J., Pozo M.J., et al. Mitochondrial reactive oxygen species and Ca2+ signaling. Am J Physiol Cell Physiol 2006, 291:C1082-C1088.
26. Cameron N.E., Eaton S.E., Cotter M.A., et al. Vascular factors and metabolic interactions in the pathogenesis of diabetic neuropathy. Diabetologia 2001, 44:1973-1988.
27. Campanucci V., Krishnaswamy A., Cooper E. Diabetes depresses synaptic transmission in sympathetic ganglia by inactivating nAChRs through a conserved intracellular cysteine residue. Neuron 2010, 66:827-834.
28. Canto C., Auwerx J. PGC-1alpha, SIRT1 and AMPK, an energy sensing network that controls energy expenditure. Curr Opin Lipidol 2009, 20:98-105.
29. Casanova-Molla J., Morales M., Garrabou G., et al. Mitochondrial loss indicates early axonal damage in small fiber neuropathies. J Peripher Nerv Syst 2012, 17:147-157.
30. Choi C.S., Befroy D.E., Codella R., et al. Paradoxical effects of increased expression of PGC-1alpha on muscle mitochondrial function and insulin-stimulated muscle glucose metabolism. Proc Natl Acad Sci U S A 2008, 105:19926-19931.
31. Choi S.W., Gerencser A.A., Lee D.W., et al. Intrinsic bioenergetic properties and stress sensitivity of dopaminergic synaptosomes. J Neurosci 2011, 31:4524-4534.
32. Chow L., From A., Seaquist E. Skeletal muscle insulin resistance: the interplay of local lipid excess and mitochondrial dysfunction. Metabolism 2010, 59:70-85.
33. Chowdhury S.K., Zherebitskaya E., Smith D.R., et al. Mitochondrial respiratory chain dysfunction in dorsal root ganglia of streptozotocin-induced diabetic rats and its correction by insulin treatment. Diabetes 2010, 59:1082-1091.
34. Coatesworth W., Bolsover S. Spatially organised mitochondrial calcium uptake through a novel pathway in chick neurones. Cell Calcium 2006, 39:217-225.
35. Crowther G.J., Milstein J.M., Jubrias S.A., et al. Altered energetic properties in skeletal muscle of men with well-controlled insulin-dependent (type 1) diabetes. Am J Physiol Endocrinol Metab 2003, 284:E655-E662.
36. David G., Barrett E.F. Stimulation-evoked increases in cytosolic [Ca(2+)] in mouse motor nerve terminals are limited by mitochondrial uptake and are temperature-dependent. J Neurosci 2000, 20:7290-7296.
37. David G., Barrett J.N., Barrett E.F. Evidence that mitochondria buffer physiological Ca2+ loads in lizard motor nerve terminals. J Physiol 1998, 509:59-65.
38. DCCT/EDIC Retinopathy and nephropathy in patients with type 1 diabetes four years after a trial of intensive therapy. The Diabetes Control and Complications Trial/Epidemiology of Diabetes Interventions and Complications Research Group. N Engl J Med 2000, 342:381-389.
39. Devereux R.B., Roman M.J., Paranicas M., et al. Impact of diabetes on cardiac structure and function: the strong heart study. Circulation 2000, 101:2271-2276.
40. Diamant M., Lamb H.J., Groeneveld Y., et al. Diastolic dysfunction is associated with altered myocardial metabolism in asymptomatic normotensive patients with well-controlled type 2 diabetes mellitus. J Am Coll Cardiol 2003, 42:328-335.
41. Duncan J.G., Fong J.L., Medeiros D.M., et al. Insulin-resistant heart exhibits a mitochondrial biogenic response driven by the peroxisome proliferator-activated receptor-alpha/PGC-1alpha gene regulatory pathway. Circulation 2007, 115:909-917.
42. Duncan J.G., Bharadwaj K.G., Fong J.L., et al. Rescue of cardiomyopathy in peroxisome proliferator-activated receptor-alpha transgenic mice by deletion of lipoprotein lipase identifies sources of cardiac lipids and peroxisome proliferator-activated receptor-alpha activators. Circulation 2010, 121:426-435.
43. Ebenezer G.J., McArthur J.C., Thomas D., et al. Denervation of skin in neuropathies: the sequence of axonal and Schwann cell changes in skin biopsies. Brain 2007, 130:2703-2714.
44. el Midaoui A., Tancrede G., Nadeau A. Effect of physical training on mitochondrial function in skeletal muscle of normal and diabetic rats. Metabolism 1996, 45:810-816.
45. Erion D.M., Shulman G.I. Diacylglycerol-mediated insulin resistance. Nat Med 2010, 16:400-402.
46. Feige J.N., Auwerx J. Transcriptional coregulators in the control of energy homeostasis. Trends Cell Biol 2007, 17:292-301.
47. Fein F.S., Sonnenblick E.H. Diabetic cardiomyopathy. Prog Cardiovasc Dis 1985, 27:255-270.
48. Fernyhough P., Schmidt R.E. Neurofilaments in diabetic neuropathy. Int Rev Neurobiol 2002, 50:115-144.
49. Finck B.N., Lehman J.J., Leone T.C., et al. The cardiac phenotype induced by PPARalpha overexpression mimics that caused by diabetes mellitus. J Clin Invest 2002, 109:121-130.
50. Finck B.N., Han X., Courtois M., et al. A critical role for PPARalpha-mediated lipotoxicity in the pathogenesis of diabetic cardiomyopathy: modulation by dietary fat content. Proc Natl Acad Sci U S A 2003, 100:1226-1231.
51. Gerstein H.C., Pogue J., Mann J.F., et al. The relationship between dysglycaemia and cardiovascular and renal risk in diabetic and non-diabetic participants in the HOPE study: a prospective epidemiological analysis. Diabetologia 2005, 48:1749-1755.
52. Gollnick P.D., Armstrong R.B., Saubert C.W., et al. Enzyme activity and fiber composition in skeletal muscle of untrained and trained men. J Appl Physiol 1972, 33:312-319.
53. Goodyear L.J., Kahn B.B. Exercise, glucose transport, and insulin sensitivity. Annu Rev Med 1998, 49:235-261.
54. Gumy L.F., Bampton E.T., Tolkovsky A.M. Hyperglycaemia inhibits Schwann cell proliferation and migration and restricts regeneration of axons and Schwann cells from adult murine DRG. Mol Cell Neurosci 2008, 37:298-311.
55. Gunter T.E., Buntinas L., Sparagna G., et al. Mitochondrial calcium transport: mechanisms and functions. Cell Calcium 2000, 28:285-296.
56. Gunter T.E., Yule D.I., Gunter K.K., et al. Calcium and mitochondria. FEBS Lett 2004, 567:96-102.
57. Hall K.E., Sima A.A., Wiley J.W. Voltage-dependent calcium currents are enhanced in dorsal root ganglion neurones from the Bio Bred/Worchester diabetic rat. J Physiol 1995, 486:313-322.
58. Hall K.E., Liu J., Sima A.A., et al. Impaired inhibitory G-protein function contributes to increased calcium currents in rats with diabetic neuropathy. J Neurophysiol 2001, 86:760-770.
59. Hammer S., van der Meer R.W., Lamb H.J., et al. Progressive caloric restriction induces dose-dependent changes in myocardial triglyceride content and diastolic function in healthy men. J Clin Endocrinol Metab 2008, 93:497-503.
60. Hammer S., Snel M., Lamb H.J., et al. Prolonged caloric restriction in obese patients with type 2 diabetes mellitus decreases myocardial triglyceride content and improves myocardial function. J Am Coll Cardiol 2008, 52:1006-1012.
61. Harmer A.R., Chisholm D.J., McKenna M.J., et al. Sprint training increases muscle oxidative metabolism during high-intensity exercise in patients with type 1 diabetes. Diabetes Care 2008, 31:2097-2102.
62. He J., Watkins S., Kelley D.E. Skeletal muscle lipid content and oxidative enzyme activity in relation to muscle fiber type in type 2 diabetes and obesity. Diabetes 2001, 50:817-823.
63. Hemmingsen B., Lund S.S., Gluud C., et al. Intensive glycaemic control for patients with type 2 diabetes: systematic review with meta-analysis and trial sequential analysis of randomised clinical trials. BMJ 2011, 343:d6898.
64. Henriksson J. Effects of physical training on the metabolism of skeletal muscle. Diabetes Care 1992, 15:1701-1711.
65. Henry R.R. Glucose control and insulin resistance in non-insulin-dependent diabetes mellitus. Ann Intern Med 1996, 124:97-103.
66. Herrero P., Peterson L.R., McGill J.B., et al. Increased myocardial fatty acid metabolism in patients with type 1 diabetes mellitus. J Am Coll Cardiol 2006, 47:598-604.
67. Hey-Mogensen M., Hojlund K., Vind B.F., et al. Effect of physical training on mitochondrial respiration and reactive oxygen species release in skeletal muscle in patients with obesity and type 2 diabetes. Diabetologia 2010, 53:1976-1985.
68. Ho E.C., Lam K.S., Chen Y.S., et al. Aldose reductase-deficient mice are protected from delayed motor nerve conduction velocity, increased c-Jun NH2-terminal kinase activation, depletion of reduced glutathione, increased superoxide accumulation, and DNA damage. Diabetes 2006, 55:1946-1953.
69. Holloszy J.O. Skeletal muscle "mitochondrial deficiency" does not mediate insulin resistance. Am J Clin Nutr 2009, 89:463S-466S.
70. Holloszy J.O., Booth F.W. Biochemical adaptations to endurance exercise in muscle. Annu Rev Physiol 1976, 38:273-291.
71. How O.J., Aasum E., Severson D.L., et al. Increased myocardial oxygen consumption reduces cardiac efficiency in diabetic mice. Diabetes 2006, 55:466-473.
72. Huang T.J., Sayers N.M., Fernyhough P., et al. Diabetes-induced alterations in calcium homeostasis in sensory neurones of streptozotocin-diabetic rats are restricted to lumbar ganglia and are prevented by neurotrophin-3. Diabetologia 2002, 45:560-570.
73. Huang T.J., Price S.A., Chilton L., et al. Insulin prevents depolarization of the mitochondrial inner membrane in sensory neurons of type 1 diabetic rats in the presence of sustained hyperglycemia. Diabetes 2003, 52:2129-2136.
74. Huang T.J., Sayers N.M., Verkhratsky A., et al. Neurotrophin-3 prevents mitochondrial dysfunction in sensory neurons of streptozotocin-diabetic rats. Exp Neurol 2005, 194:279-283.
75. Huss J.M., Kelly D.P. Mitochondrial energy metabolism in heart failure: a question of balance. J Clin Invest 2005, 115:547-555.
76. Ibsen H.K. The Crabtree effect: a review. Cancer Res 1961, 21:829-841.
77. Iozzo P., Lautamaki R., Borra R., et al. Contribution of glucose tolerance and gender to cardiac adiposity. J Clin Endocrinol Metab 2009, 94:4472-4482.
78. Ismail-Beigi F., Craven T., Banerji M.A., et al. Effect of intensive treatment of hyperglycaemia on microvascular outcomes in type 2 diabetes: an analysis of the ACCORD randomised trial. Lancet 2010, 376:419-430.
79. Itani S.I., Ruderman N.B., Schmieder F., et al. Lipid-induced insulin resistance in human muscle is associated with changes in diacylglycerol, protein kinase C, and IkappaB-alpha. Diabetes 2002, 51:2005-2011.
80. Jiang Y., Calcutt N.A., Ramos K.M., et al. Novel sites of aldose reductase immunolocalization in normal and streptozotocin-diabetic rats. J Peripher Nerv Syst 2006, 11:274-285.
81. Kalichman M.W., Powell H.C., Mizisin A.P. Reactive, degenerative, and proliferative Schwann cell responses in experimental galactose and human diabetic neuropathy. Acta Neuropathol 1998, 95:47-56.
82. Kamiya H., Zhang W., Sima A.A. Apoptotic stress is counterbalanced by survival elements preventing programmed cell death of dorsal root ganglions in subacute type 1 diabetic BB/Wor rats. Diabetes 2005, 54:3288-3295.
83. Kamiya H., Zhang W., Sima A.A. Degeneration of the Golgi and neuronal loss in dorsal root ganglia in diabetic BioBreeding/Worcester rats. Diabetologia 2006, 49:2763-2774.
84. Karamitsos T.D., Karvounis H.I., Didangelos T., et al. Impact of autonomic neuropathy on left ventricular function in normotensive type 1 diabetic patients: a tissue Doppler echocardiographic study. Diabetes Care 2008, 31:325-327.
85. Kelley D.E., He J., Menshikova E.V., et al. Dysfunction of mitochondria in human skeletal muscle in type 2 diabetes. Diabetes 2002, 51:2944-2950.
86. Kelly D.P., Strauss A.W. Inherited cardiomyopathies. N Engl J Med 1994, 330:913-919.
87. Kennedy W.R., Wendelschafer-Crabb G., Johnson T. Quantitation of epidermal nerves in diabetic neuropathy. Neurology 1996, 47:1042-1048.
88. Kirichok Y., Krapivinsky G., Clapham D.E. The mitochondrial calcium uniporter is a highly selective ion channel. Nature 2004, 427:360-364.
89. Kluding P.M., Pasnoor M., Singh R., et al. The effect of exercise on neuropathic symptoms, nerve function, and cutaneous innervation in people with diabetic peripheral neuropathy. J Diabetes Complications 2012, 26:424-429.
90. Knowler W.C., Barrett-Connor E., Fowler S.E., et al. Reduction in the incidence of type 2 diabetes with lifestyle intervention or metformin. N Engl J Med 2002, 346:393-403.
91. Knuuti J., Takala T.O., Nagren K., et al. Myocardial fatty acid oxidation in patients with impaired glucose tolerance. Diabetologia 2001, 44:184-187.
92. Kostyuk E., Pronchuk N., Shmigol A. Calcium signal prolongation in sensory neurones of mice with experimental diabetes. Neuroreport 1995, 6:1010-1012.
93. Kostyuk E., Svichar N., Shishkin V., et al. Role of mitochondrial dysfunction in calcium signalling alterations in dorsal root ganglion neurons of mice with experimentally-induced diabetes. Neuroscience 1999, 90:535-541.
94. Kostyuk E., Voitenko N., Kruglikov I., et al. Diabetes-induced changes in calcium homeostasis and the effects of calcium channel blockers in rat and mice nociceptive neurons. Diabetologia 2001, 44:1302-1309.
95. Koves T.R., Ussher J.R., Noland R.C., et al. Mitochondrial overload and incomplete fatty acid oxidation contribute to skeletal muscle insulin resistance. Cell Metab 2008, 7:45-56.
96. Krssak M., Falk Petersen K., Dresner A., et al. Intramyocellular lipid concentrations are correlated with insulin sensitivity in humans: a 1H NMR spectroscopy study. Diabetologia 1999, 42:113-116.
97. Kruglikov I., Gryshchenko O., Shutov L., et al. Diabetes-induced abnormalities in ER calcium mobilization in primary and secondary nociceptive neurons. Pflugers Arch 2004, 448:395-401.
98. Lanza I.R., Nair K.S. Muscle mitochondrial changes with aging and exercise. Am J Clin Nutr 2009, 89:467S-471S.
99. Lauria G., Morbin M., Lombardi R., et al. Axonal swellings predict the degeneration of epidermal nerve fibers in painful neuropathies. Neurology 2003, 61:631-636.
100. Lee Y., Wang M.Y., Kakuma T., et al. Liporegulation in diet-induced obesity. The antisteatotic role of hyperleptinemia. J Biol Chem 2001, 276:5629-5635.
101. Lehman J.J., Boudina S., Banke N.H., et al. The transcriptional coactivator PGC-1alpha is essential for maximal and efficient cardiac mitochondrial fatty acid oxidation and lipid homeostasis. Am J Physiol Heart Circ Physiol 2008, 295:H185-H196.
102. Lipscombe L.L., Hux J.E. Trends in diabetes prevalence, incidence, and mortality in Ontario, Canada 1995-2005: a population-based study. Lancet 2007, 369:750-756.
103. Liu J.E., Palmieri V., Roman M.J., et al. The impact of diabetes on left ventricular filling pattern in normotensive and hypertensive adults: the Strong Heart Study. J Am Coll Cardiol 2001, 37:1943-1949.
104. Lopaschuk G.D., Katz S., McNeill J.H. The effect of alloxan- and streptozotocin-induced diabetes on calcium transport in rat cardiac sarcoplasmic reticulum. The possible involvement of long chain acylcarnitines. Can J Physiol Pharmacol 1983, 61:439-448.
105. Lopaschuk G.D., Ussher J.R., Folmes C.D., et al. Myocardial fatty acid metabolism in health and disease. Physiol Rev 2010, 90:207-258.
106. Lowell B.B., Shulman G.I. Mitochondrial dysfunction and type 2 diabetes. Science 2005, 307:384-387.
107. Malik R.A., Tesfaye S., Newrick P.G., et al. Sural nerve pathology in diabetic patients with minimal but progressive neuropathy. Diabetologia 2005, 48:578-585.
108. Martin B.C., Warram J.H., Krolewski A.S., et al. Role of glucose and insulin resistance in development of type 2 diabetes mellitus: results of a 25-year follow-up study. Lancet 1992, 340:925-929.
109. Mazzone T., Chait A., Plutzky J. Cardiovascular disease risk in type 2 diabetes mellitus: insights from mechanistic studies. Lancet 2008, 371:1800-1809.
110. McCormack J.G., Halestrap A.P., Denton R.M. Role of calcium ions in regulation of mammalian intramitochondrial metabolism. Physiol Rev 1990, 70:391-425.
111. McGarry J.D. Banting lecture 2001: dysregulation of fatty acid metabolism in the etiology of type 2 diabetes. Diabetes 2002, 51:7-18.
112. McGavock J., Mandic S., Lewanczuk R., et al. Cardiovascular adaptations to exercise training in postmenopausal women with type 2 diabetes mellitus. Cardiovasc Diabetol 2004, 3:3.
113. McGavock J.M., Eves N.D., Mandic S., et al. The role of exercise in the treatment of cardiovascular disease associated with type 2 diabetes mellitus. Sports Med 2004, 34:27-48.
114. McGavock J.M., Mandic S., Vonder Muhll I., et al. Low cardiorespiratory fitness is associated with elevated C-reactive protein levels in women with type 2 diabetes. Diabetes Care 2004, 27:320-325.
115. McGavock J.M., Victor R.G., Unger R.H., et al. Adiposity of the heart, revisited. Ann Intern Med 2006, 144:517-524.
116. McGavock J.M., Lingvay I., Zib I., et al. Cardiac steatosis in diabetes mellitus: a 1H-magnetic resonance spectroscopy study. Circulation 2007, 116:1170-1175.
117. Meex R.C., Schrauwen-Hinderling V.B., Moonen-Kornips E., et al. Restoration of muscle mitochondrial function and metabolic flexibility in type 2 diabetes by exercise training is paralleled by increased myocellular fat storage and improved insulin sensitivity. Diabetes 2010, 59:572-579.
118. Mitchell J.H., Blomqvist G. Maximal oxygen uptake. N Engl J Med 1971, 284:1018-1022.
119. Miura S., Kai Y., Ono M., et al. Overexpression of peroxisome proliferator-activated receptor gamma coactivator-1alpha down-regulates GLUT4 mRNA in skeletal muscles. J Biol Chem 2003, 278:31385-31390.
120. Miura S., Tomitsuka E., Kamei Y., et al. Overexpression of peroxisome proliferator-activated receptor gamma co-activator-1alpha leads to muscle atrophy with depletion of ATP. Am J Pathol 2006, 169:1129-1139.
121. Mizisin A.P., Vu Y., Shuff M., et al. Ciliary neurotrophic factor improves nerve conduction and ameliorates regeneration deficits in diabetic rats. Diabetes 2004, 53:1807-1812.
122. Mizisin A.P., Nelson R.W., Sturges B.K., et al. Comparable myelinated nerve pathology in feline and human diabetes mellitus. Acta Neuropathol 2007, 113:431-442.
123. Mookerjee S.A., Divakaruni A.S., Jastroch M., et al. Mitochondrial uncoupling and lifespan. Mech Ageing Dev 2010, 131:463-472.
124. Mootha V.K., Lindgren C.M., Eriksson K.F., et al. PGC-1alpha-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat Genet 2003, 34:267-273.
125. Muoio D.M., Neufer P.D. Lipid-induced mitochondrial stress and insulin action in muscle. Cell Metab 2012, 15:595-605.
126. Muoio D.M., Newgard C.B. Mechanisms of disease: molecular and metabolic mechanisms of insulin resistance and beta-cell failure in type 2 diabetes. Nat Rev Mol Cell Biol 2008, 9:193-205.
127. Musi N., Fujii N., Hirshman M.F., et al. AMP-activated protein kinase (AMPK) is activated in muscle of subjects with type 2 diabetes during exercise. Diabetes 2001, 50:921-927.
128. Narayan K.M., Boyle J.P., Thompson T.J., et al. Lifetime risk for diabetes mellitus in the United States. JAMA 2003, 290:1884-1890.
129. Nathan D.M., Cleary P.A., Backlund J.Y., et al. Intensive diabetes treatment and cardiovascular disease in patients with type 1 diabetes. N Engl J Med 2005, 353:2643-2653.
130. Neschen S., Morino K., Hammond L.E., et al. Prevention of hepatic steatosis and hepatic insulin resistance in mitochondrial acyl-CoA:glycerol-sn-3-phosphate acyltransferase 1 knockout mice. Cell Metab 2005, 2:55-65.
131. Nicholls D.G. Mitochondrial dysfunction and glutamate excitotoxicity studied in primary neuronal cultures. Curr Mol Med 2004, 4:149-177.
132. Nicholls D.G. Mitochondria and calcium signaling. Cell Calcium 2005, 38:311-317.
133. Nicholls D.G. Simultaneous monitoring of ionophore- and inhibitor-mediated plasma and mitochondrial membrane potential changes in cultured neurons. J Biol Chem 2006, 281:14864-14874.
134. Nicholls D.G., Budd S.L. Mitochondria and neuronal survival. Physiol Rev 2000, 80:315-360.
135. Nielsen J., Mogensen M., Vind B.F., et al. Increased subsarcolemmal lipids in type 2 diabetes: effect of training on localization of lipids, mitochondria, and glycogen in sedentary human skeletal muscle. Am J Physiol Endocrinol Metab 2010, 298:E706-E713.
136. Nishikawa T., Edelstein D., Brownlee M. The missing link: a single unifying mechanism for diabetic complications. Kidney Int 2000, 58:S26-S30.
137. Nishikawa T., Edelstein D., Du X.L., et al. Normalizing mitochondrial superoxide production blocks three pathways of hyperglycaemic damage. Nature 2000, 404:787-790.
138. Nja A., Purves D. The effects of nerve growth factor and its antiserum on synapses in the superior cervical ganglion of the guinea-pig. J Physiol 1978, 277:53-75.
139. Obrosova I.G. How does glucose generate oxidative stress in peripheral nerve?. Int Rev Neurobiol 2002, 50:3-35.
140. Obrosova I.G., Van Huysen C., Fathallah L., et al. An aldose reductase inhibitor reverses early diabetes-induced changes in peripheral nerve function, metabolism, and antioxidative defense. FASEB J 2002, 16:123-125.
141. Obrosova I.G., Pacher P., Szabo C., et al. Aldose reductase inhibition counteracts oxidative-nitrosative stress and poly(ADP-ribose) polymerase activation in tissue sites for diabetes complications. Diabetes 2005, 54:234-242.
142. Pagel-Langenickel I., Bao J., Pang L., et al. The role of mitochondria in the pathophysiology of skeletal muscle insulin resistance. Endocr Rev 2010, 31:25-51.
143. Patti M.E., Corvera S. The role of mitochondria in the pathogenesis of type 2 diabetes. Endocr Rev 2010, 31:364-395.
144. Patti M.E., Butte A.J., Crunkhorn S., et al. Coordinated reduction of genes of oxidative metabolism in humans with insulin resistance and diabetes: potential role of PGC1 and NRF1. Proc Natl Acad Sci U S A 2003, 100:8466-8471.
145. Perez-Campo R., Lopez-Torres M., Cadenas S., et al. The rate of free radical production as a determinant of the rate of aging: evidence from the comparative approach. J Comp Physiol B 1998, 168:149-158.
146. Perseghin G., Price T.B., Petersen K.F., et al. Increased glucose transport-phosphorylation and muscle glycogen synthesis after exercise training in insulin-resistant subjects. N Engl J Med 1996, 335:1357-1362.
147. Perseghin G., Ntali G., De Cobelli F., et al. Abnormal left ventricular energy metabolism in obese men with preserved systolic and diastolic functions is associated with insulin resistance. Diabetes Care 2007, 30:1520-1526.
148. Petersen K.F., Befroy D., Dufour S., et al. Mitochondrial dysfunction in the elderly: possible role in insulin resistance. Science 2003, 300:1140-1142.
149. Petersen K.F., Dufour S., Befroy D., et al. Impaired mitochondrial activity in the insulin-resistant offspring of patients with type 2 diabetes. N Engl J Med 2004, 350:664-671.
150. Poirier P., Bogaty P., Garneau C., et al. Diastolic dysfunction in normotensive men with well-controlled type 2 diabetes: importance of maneuvers in echocardiographic screening for preclinical diabetic cardiomyopathy. Diabetes Care 2001, 24:5-10.
151. Poirier P., Bogaty P., Philippon F., et al. Preclinical diabetic cardiomyopathy: relation of left ventricular diastolic dysfunction to cardiac autonomic neuropathy in men with uncomplicated well-controlled type 2 diabetes. Metabolism 2003, 52:1056-1061.
152. Polydefkis M., Hauer P., Sheth S., et al. The time course of epidermal nerve fibre regeneration: studies in normal controls and in people with diabetes, with and without neuropathy. Brain 2004, 127:1606-1615.
153. Praet S.F., De Feyter H.M., Jonkers R.A., et al. 31P MR spectroscopy and in vitro markers of oxidative capacity in type 2 diabetes patients. MAGMA 2006, 19:321-331.
154. Puigserver P., Wu Z., Park C.W., et al. A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell 1998, 92:829-839.
155. Purves T., Middlemas A., Agthong S., et al. A role for mitogen-activated protein kinases in the etiology of diabetic neuropathy. FASEB J 2001, 15:2508-2514.
156. Quattrini C., Tavakoli M., Jeziorska M., et al. Surrogate markers of small fiber damage in human diabetic neuropathy. Diabetes 2007, 56:2148-2154.
157. Ribisl P.M., Lang W., Jaramillo S.A., et al. Exercise capacity and cardiovascular/metabolic characteristics of overweight and obese individuals with type 2 diabetes: the Look AHEAD clinical trial. Diabetes Care 2007, 30:2679-2684.
158. Rijzewijk L.J., van der Meer R.W., Smit J.W., et al. Myocardial steatosis is an independent predictor of diastolic dysfunction in type 2 diabetes mellitus. J Am Coll Cardiol 2008, 52:1793-1799.
159. Rijzewijk L.J., van der Meer R.W., Lamb H.J., et al. Altered myocardial substrate metabolism and decreased diastolic function in nonischemic human diabetic cardiomyopathy: studies with cardiac positron emission tomography and magnetic resonance imaging. J Am Coll Cardiol 2009, 54:1524-1532.
160. Roden M., Price T.B., Perseghin G., et al. Mechanism of free fatty acid-induced insulin resistance in humans. J Clin Invest 1996, 97:2859-2865.
161. Rodgers J.T., Lerin C., Gerhart-Hines Z., et al. Metabolic adaptations through the PGC-1 alpha and SIRT1 pathways. FEBS Lett 2008, 582:46-53.
162. Roy Chowdhury S.K., Smith D.R., Saleh A., et al. Impaired adenosine monophosphate-activated protein kinase signalling in dorsal root ganglia neurons is linked to mitochondrial dysfunction and peripheral neuropathy in diabetes. Brain 2012, 135:1751-1766.
163. Russell J.W., Golovoy D., Vincent A.M., et al. High glucose-induced oxidative stress and mitochondrial dysfunction in neurons. FASEB J 2002, 16:1738-1748.
164. Saleh A., Roy Chowdhury S.K., Smith D.R., et al. Ciliary neurotrophic factor activates NF-kappaB to enhance mitochondrial bioenergetics and prevent neuropathy in sensory neurons of streptozotocin-induced diabetic rodents. Neuropharmacology 2013, 65:65-73.
165. Samuel V.T., Shulman G.I. Mechanisms for insulin resistance: common threads and missing links. Cell 2012, 148:852-871.
166. Sandri M., Lin J., Handschin C., et al. PGC-1alpha protects skeletal muscle from atrophy by suppressing FoxO3 action and atrophy-specific gene transcription. Proc Natl Acad Sci U S A 2006, 103:16260-16265.
167. Savage D.B., Choi C.S., Samuel V.T., et al. Reversal of diet-induced hepatic steatosis and hepatic insulin resistance by antisense oligonucleotide inhibitors of acetyl-CoA carboxylases 1 and 2. J Clin Invest 2006, 116:817-824.
168. Scheuermann-Freestone M., Madsen P.L., Manners D., et al. Abnormal cardiac and skeletal muscle energy metabolism in patients with type 2 diabetes. Circulation 2003, 107:3040-3046.
169. Schmidt R.E., Beaudet L.N., Plurad S.B., et al. Axonal cytoskeletal pathology in aged and diabetic human sympathetic autonomic ganglia. Brain Res 1997, 769:375-383.
170. Schmidt R.E., Dorsey D., Parvin C.A., et al. Dystrophic axonal swellings develop as a function of age and diabetes in human dorsal root ganglia. J Neuropathol Exp Neurol 1997, 56:1028-1043.
171. Schmidt R.E., Dorsey D.A., Beaudet L.N., et al. Non-obese diabetic mice rapidly develop dramatic sympathetic neuritic dystrophy: a new experimental model of diabetic autonomic neuropathy. Am J Pathol 2003, 163:2077-2091.
172. Schmidt R.E., Parvin C.A., Green K.G. Synaptic ultrastructural alterations anticipate the development of neuroaxonal dystrophy in sympathetic ganglia of aged and diabetic mice. J Neuropathol Exp Neurol 2008, 67:1166-1186.
173. Schmidt R.E., Green K.G., Snipes L.L., et al. Neuritic dystrophy and neuronopathy in Akita (Ins2(Akita)) diabetic mouse sympathetic ganglia. Exp Neurol 2009, 216:207-218.
174. Schrauwen P., Hesselink M.K. Oxidative capacity, lipotoxicity, and mitochondrial damage in type 2 diabetes. Diabetes 2004, 53:1412-1417.
175. Shepherd P.R., Kahn B.B. Glucose transporters and insulin action - implications for insulin resistance and diabetes mellitus. N Engl J Med 1999, 341:248-257.
176. Short K.R., Vittone J.L., Bigelow M.L., et al. Impact of aerobic exercise training on age-related changes in insulin sensitivity and muscle oxidative capacity. Diabetes 2003, 52:1888-1896.
177. Shulman G.I. Unraveling the cellular mechanism of insulin resistance in humans: new insights from magnetic resonance spectroscopy. Physiology (Bethesda) 2004, 19:183-190.
178. Sidenius P., Jakobsen J. Reduced perikaryal volume of lower motor and primary sensory neurons in early experimental diabetes. Diabetes 1980, 29:182-186.
179. Sigal R.J., Kenny G.P., Boule N.G., et al. Effects of aerobic training, resistance training, or both on glycemic control in type 2 diabetes: a randomized trial. Ann Intern Med 2007, 147:357-369.
180. Sima A.A. Diabetic neuropathy in type 1 and type 2 diabetes and the effects of C-peptide. J Neurol Sci 2004, 220:133-136.
181. Simoneau J.A., Kelley D.E. Altered glycolytic and oxidative capacities of skeletal muscle contribute to insulin resistance in NIDDM. J Appl Physiol 1997, 83:166-171.
182. Simoneau J.A., Colberg S.R., Thaete F.L., et al. Skeletal muscle glycolytic and oxidative enzyme capacities are determinants of insulin sensitivity and muscle composition in obese women. FASEB J 1995, 9:273-278.
183. Simoneau J.A., Veerkamp J.H., Turcotte L.P., et al. Markers of capacity to utilize fatty acids in human skeletal muscle: relation to insulin resistance and obesity and effects of weight loss. FASEB J 1999, 13:2051-2060.
184. Sinha R., Dufour S., Petersen K.F., et al. Assessment of skeletal muscle triglyceride content by (1)H nuclear magnetic resonance spectroscopy in lean and obese adolescents: relationships to insulin sensitivity, total body fat, and central adiposity. Diabetes 2002, 51:1022-1027.
185. Smith A.G., Russell J., Feldman E.L., et al. Lifestyle intervention for pre-diabetic neuropathy. Diabetes Care 2006, 29:1294-1299.
186. Soyal S., Krempler F., Oberkofler H., et al. PGC-1alpha: a potent transcriptional cofactor involved in the pathogenesis of type 2 diabetes. Diabetologia 2006, 49:1477-1488.
187. Srinivasan S., Stevens M., Wiley J.W. Diabetic peripheral neuropathy: evidence for apoptosis and associated mitochondrial dysfunction. Diabetes 2000, 49:1932-1938.
188. Struthers A.D., Morris A.D. Screening for and treating left-ventricular abnormalities in diabetes mellitus: a new way of reducing cardiac deaths. Lancet 2002, 359:1430-1432.
189. Stumvoll M., Goldstein B.J., van Haeften T.W. Type 2 diabetes: principles of pathogenesis and therapy. Lancet 2005, 365:1333-1346.
190. Suarez J., Belke D.D., Gloss B., et al. In vivo adenoviral transfer of sorcin reverses cardiac contractile abnormalities of diabetic cardiomyopathy. Am J Physiol Heart Circ Physiol 2004, 286:H68-H75.
191. Suarez J., Hu Y., Makino A., et al. Alterations in mitochondrial function and cytosolic calcium induced by hyperglycemia are restored by mitochondrial transcription factor A in cardiomyocytes. Am J Physiol Cell Physiol 2008, 295:C1561-C1568.
192. Sung J., Song Y.M., Ebrahim S., et al. Fasting blood glucose and the risk of stroke and myocardial infarction. Circulation 2009, 119:812-819.
193. Szczepaniak L.S., Dobbins R.L., Metzger G.J., et al. Myocardial triglycerides and systolic function in humans: in vivo evaluation by localized proton spectroscopy and cardiac imaging. Magn Reson Med 2003, 49:417-423.
194. Szendroedi J., Roden M. Mitochondrial fitness and insulin sensitivity in humans. Diabetologia 2008, 51:2155-2167.
195. Szendroedi J., Schmid A.I., Chmelik M., et al. Muscle mitochondrial ATP synthesis and glucose transport/phosphorylation in type 2 diabetes. PLoS Med 2007, 4:e154.
196. Taegtmeyer H., McNulty P., Young M.E. Adaptation and maladaptation of the heart in diabetes. Part I: general concepts. Circulation 2002, 105:1727-1733.
197. Territo P.R., French S.A., Dunleavy M.C., et al. Calcium activation of heart mitochondrial oxidative phosphorylation: rapid kinetics of mVO2, NADH, AND light scattering. J Biol Chem 2001, 276:2586-2599.
198. Thyfault J.P., Cree M.G., Zheng D., et al. Contraction of insulin-resistant muscle normalizes insulin action in association with increased mitochondrial activity and fatty acid catabolism. Am J Physiol Cell Physiol 2007, 292:C729-C739.
199. Toledo F.G., Menshikova E.V., Ritov V.B., et al. Effects of physical activity and weight loss on skeletal muscle mitochondria and relationship with glucose control in type 2 diabetes. Diabetes 2007, 56:2142-2147.
200. Trost S.U., Belke D.D., Bluhm W.F., et al. Overexpression of the sarcoplasmic reticulum Ca(2+)-ATPase improves myocardial contractility in diabetic cardiomyopathy. Diabetes 2002, 51:1166-1171.
201. Tuomilehto J. Prevention of type 2 diabetes mellitus by changes in lifestyle among subjects with impaired glucose tolerance. N Engl J Med 2001, 344:1343-1350.
202. Turner N., Bruce C.R., Beale S.M., et al. 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 2007, 56:2085-2092.
203. UKPDS Intensive blood-glucose control with sulphonylureas or insulin compared with conventional treatment and risk of complications in patients with type 2 diabetes (UKPDS 33). UK Prospective Diabetes Study (UKPDS) Group. Lancet 1998, 352:837-853.
204. UKPDS Effect of intensive blood-glucose control with metformin on complications in overweight patients with type 2 diabetes (UKPDS 34). UK Prospective Diabetes Study (UKPDS) Group. Lancet 1998, 352:854-865.
205. Urban M.J., Pan P., Farmer K.L., et al. Modulating molecular chaperones improves sensory fiber recovery and mitochondrial function in diabetic peripheral neuropathy. Exp Neurol 2012, 235:388-396.
206. van der Meer R.W., Hammer S., Smit J.W., et al. Short-term caloric restriction induces accumulation of myocardial triglycerides and decreases left ventricular diastolic function in healthy subjects. Diabetes 2007, 56:2849-2853.
207. van der Meer R.W., Rijzewijk L.J., de Jong H.W., et al. Pioglitazone improves cardiac function and alters myocardial substrate metabolism without affecting cardiac triglyceride accumulation and high-energy phosphate metabolism in patients with well-controlled type 2 diabetes mellitus. Circulation 2009, 119:2069-2077.
208. Vincent A.M., Russell J.W., Low P., et al. Oxidative stress in the pathogenesis of diabetic neuropathy. Endocr Rev 2004, 25:612-628.
209. Vincent A.M., Olzmann J.A., Brownlee M., et al. Uncoupling proteins prevent glucose-induced neuronal oxidative stress and programmed cell death. Diabetes 2004, 53:726-734.
210. Vinik A.I., Maser R.E., Mitchell B.D., et al. Diabetic autonomic neuropathy. Diabetes Care 2003, 26:1553-1579.
211. Voitenko N.V., Kostyuk E.P., Kruglikov I.A., et al. Changes in calcium signalling in dorsal horn neurons in rats with streptozotocin-induced diabetes. Neuroscience 1999, 94:887-890.
212. Voitenko N.V., Kruglikov I.A., Kostyuk E.P., et al. Effect of streptozotocin-induced diabetes on the activity of calcium channels in rat dorsal horn neurons. Neuroscience 2000, 95:519-524.
213. Wang P., Lloyd S.G., Zeng H., et al. Impact of altered substrate utilization on cardiac function in isolated hearts from Zucker diabetic fatty rats. Am J Physiol Heart Circ Physiol 2005, 288:H2102-H2110.
214. Wang Y., Ebermann L., Sterner-Kock A., et al. Myocardial overexpression of adenine nucleotide translocase 1 ameliorates diabetic cardiomyopathy in mice. Exp Physiol 2009, 94:220-227.
215. Wei M., Gibbons L.W., Kampert J.B., et al. Low cardiorespiratory fitness and physical inactivity as predictors of mortality in men with type 2 diabetes. Ann Intern Med 2000, 132:605-611.
216. Weis B.C., Esser V., Foster D.W., et al. Rat heart expresses two forms of mitochondrial carnitine palmitoyltransferase I. The minor component is identical to the liver enzyme. J Biol Chem 1994, 269:18712-18715.
217. Wilson T.M., Tanaka H. Meta-analysis of the age-associated decline in maximal aerobic capacity in men: relation to training status. Am J Physiol Heart Circ Physiol 2000, 278:H829-H834.
218. Wisloff U., Najjar S.M., Ellingsen O., et al. Cardiovascular risk factors emerge after artificial selection for low aerobic capacity. Science 2005, 307:418-420.
219. Wittmeier K.D., Wicklow B.A., MacIntosh A.C., et al. Hepatic steatosis and low cardiorespiratory fitness in youth with type 2 diabetes. Obesity (Silver Spring) 2012, 20:1034-1040.
220. Yagihashi S. Pathogenetic mechanisms of diabetic neuropathy: lessons from animal models. J Peripher Nerv Syst 1997, 2:113-132.
221. Yan Y., Wei C.L., Zhang W.R., et al. Cross-talk between calcium and reactive oxygen species signaling. Acta Pharmacol Sin 2006, 27:821-826.
222. Young M.E., McNulty P., Taegtmeyer H. Adaptation and maladaptation of the heart in diabetes. Part II: potential mechanisms. Circulation 2002, 105:1861-1870.
223. Young M.E., Guthrie P.H., Razeghi P., et al. Impaired long-chain fatty acid oxidation and contractile dysfunction in the obese Zucker rat heart. Diabetes 2002, 51:2587-2595.
224. Yu C., Rouen S., Dobrowsky R.T. Hyperglycemia and downregulation of caveolin-1 enhance neuregulin-induced demyelination. Glia 2008, 56:877-887.
225. Zhang L., Zhao H., Blagg B.S., et al. C-terminal heat shock protein 90 inhibitor decreases hyperglycemia-induced oxidative stress and improves mitochondrial bioenergetics in sensory neurons. J Proteome Res 2012, 11:2581-2593.
226. Zherebitskaya E., Akude E., Smith D.R., et al. Development of selective axonopathy in adult sensory neurons isolated from diabetic rats: role of glucose-induced oxidative stress. Diabetes 2009, 58:1356-1364.
227. Zherebitskaya E., Schapansky J., Akude E., et al. Sensory neurons derived from diabetic rats have diminished internal Ca2+ stores linked to impaired re-uptake by the endoplasmic reticulum. ASN Neuro 2012, 4:e00072.
228. Zhou Y.T., Grayburn P., Karim A., et al. Lipotoxic heart disease in obese rats: implications for human obesity. Proc Natl Acad Sci U S A 2000, 97:1784-1789.
229. Zib I., Jacob A.N., Lingvay I., et al. Effect of pioglitazone therapy on myocardial and hepatic steatosis in insulin-treated patients with type 2 diabetes. J Investig Med 2007, 55:230-236.