Uncoupling Proteins Prevent Glucose-Induced Neuronal Oxidative Stress and Programmed Cell Death

Diabetes

Volumn 53, Issue 3, 2004, Pages 726-734

  Vincent, Andrea M ^a   Olzmann, James A ^a   Brownlee, Michael ^b   Sivitz, W I ^c   Russell, James W ^a,d  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF IOWA HOSPITALS AND CLINICS   (United States)

^d VA ANN ARBOR HEALTHCARE SYSTEM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; GLUCOSE; REACTIVE OXYGEN METABOLITE; UNCOUPLING PROTEIN; UNCOUPLING PROTEIN 1; UNCOUPLING PROTEIN 3;

ANIMAL CELL; ANIMAL MODEL; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DIABETES MELLITUS; DIABETIC NEUROPATHY; DOWN REGULATION; EMBRYO; GENE OVEREXPRESSION; HYPERGLYCEMIA; HYPERPOLARIZATION; IMMUNOCYTOCHEMISTRY; MITOCHONDRIAL MEMBRANE; NERVE CELL CULTURE; NERVE CELL DEGENERATION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RAT; SPINAL GANGLION; WESTERN BLOTTING;

ANIMALS; APOPTOSIS; CARRIER PROTEINS; DISEASE MODELS, ANIMAL; GANGLIA, SPINAL; GLUCOSE; HYPERGLYCEMIA; ION CHANNELS; MEMBRANE POTENTIALS; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; NEURONS; OXIDATIVE STRESS; RATS; RATS, SPRAGUE-DAWLEY; UNCOUPLING AGENTS;

EID: 1442349997     PISSN: 00121797     EISSN: None     Source Type: Journal    
DOI: 10.2337/diabetes.53.3.726     Document Type: Article

References (46)

1. Russell JW, Sullivan KA, Windebank AJ, Herrmann DN, Feldman EL: Neurons undergo apoptosis in animal and cell culture models of diabetes. Neurobiol Dis 6:347-363, 1999
2. Russell JW, Golovoy D, Vincent AM, Mahendru P, Olzmann JA, Mentzer A, Feldman EL: High glucose-induced oxidative stress and mitochondrial dysfunction in neurons. FASEB J 16:1738-1748, 2002
3. Russell JW, Feldman EL: Insulin-like growth factor-I prevents apoptosis in sympathetic neurons exposed to high glucose. Horm Metab Res 31:90-96, 1999
4. Srinivasan S, Stevens MJ, Wiley JW: Diabetic peripheral neuropathy: evidence for apoptosis and associated mitochondrial dysfunction. Diabetes 49:1932-1938, 2000
5. Schmeichel AM, Schmelzer JD, Low PA: Oxidative injury and apoptosis of dorsal root ganglion neurons in chronic experimental diabetic neuropathy. Diabetes 52:165-171, 2003
6. Cheng C, Zochodne DW: Sensory neurons with activated caspase-3 survive long-term experimental diabetes. Diabetes 52:2363-2371, 2003
7. Low PA, Nickander KK, Trischler HJ: The roles of oxidative stress and antioxidant treatment in experimental diabetic neuropathy. Diabetes 46 (Suppl. 2):S38-S42, 1997
8. Tomlinson DR: Future prevention and treatment of diabetic neuropathy. Diabete Metab 24 (Suppl. 3):79-83, 1998
9. Zochodne DW: Diabetic neuropathies: features and mechanisms. Brain Pathol 9:369-391, 1999
10. Cameron NE, Cotter MA: Metabolic and vascular factors in the pathogenesis of diabetic neuropathy. Diabetes 46 (Suppl. 2):S31-S37, 1997
11. Stevens MJ, Obrosova I, Cao X, Van Huysen C, Greene DA: Effects of DL-α-lipoic acid on peripheral nerve conduction, blood flow, energy metabolism, and oxidative stress in experimental diabetic neuropathy. Diabetes 49:1006-1015, 2000
12. Coppey LJ, Gellett JS, Davidson EP, Dunlap JA, Lund DD, Yorek MA: Effect of antioxidant treatment of streptozotocin-induced diabetic rats on endoneurial blood flow, motor nerve conduction velocity, and vascular reactivity of epineurial arterioles of the sciatic nerve. Diabetes 50:1927-1937, 2001
13. Brownlee M: Biochemistry and molecular cell biology of diabetic complications. Nature 414:813-820, 2001
14. Echtay KS, Roussel D, St-Pierre J, Jekabsons MB, Cadenas S, Stuart JA, Harper JA, Roebuck SJ, Morrison A, Pickering S, Clapham JC, Brand MD: Superoxide activates mitochondrial uncoupling proteins. Nature 415:96-99, 2002
15. Budd SL, Tenneti L, Lishnak T, Lipton SA: Mitochondrial and extramitochondrial apoptotic signaling pathways in cerebrocortical neurons. Proc Natl Acad Sci U S A 97:6161-6166, 2000
16. Vincent AM, Brownlee M, Russell JW: Oxidative stress and programmed cell death in diabetic neuropathy. Ann N Y Acad Sci 959:368-383, 2002
17. Deshmukh M, Johnson EM Jr: Evidence of a novel event during neuronal death: development of competence-to-die in response to cytoplasmic cytochrome c. Neuron 21:695-705, 1998
18. Luetjens CM, Bui NT, Sengpiel B, Munstermann G, Poppe M, Krohn AJ, Bauerbach E, Krieglstein J, Prehn JH: Delayed mitochondrial dysfunction in excitotoxic neuron death: cytochrome c release and a secondary increase in superoxide production. J Neurosci 20:5715-5723, 2000
19. Boss O, Muzzin P, Giacobino JP: The uncoupling proteins, a review. Eur J Endocrinol 139:1-9, 1998
20. Clapham JC, Arch JR, Chapman H, Haynes A, Lister C, Moore GB, Piercy V, Carter SA, Lehner I, Smith SA, Beeley LJ, Godden RJ, Herrity N, Skehel M, Changani KK, Hockings PD, Reid DG, Squires SM, Hatcher J, Trail B, Latcham J, Rastan S, Harper AJ, Cadenas S, Buckingham JA, Brand MD: Mice overexpressing human uncoupling protein-3 in skeletal muscle are hyperphagic and lean. Nature 406:415-418, 2000
21. Kim-Han JS, Reichert SA, Quick KL, Dugan LL: BMCP1: a mitochondrial uncoupling protein in neurons which regulates mitochondrial function and oxidant production. J Neurochem 79:658-668, 2001
22. Horvath TL, Warden CH, Hajos M, Lombardi A, Goglia F, Diano S: Brain uncoupling protein 2: uncoupled neuronal mitochondria predict thermal synapses in homeostatic centers. J Neurosci 19:10417-10427, 1999
23. Havel PJ, Hahn TM, Sindelar DK, Baskin DG, Dallman MF, Weigle DS, Schwartz MW: Effects of streptozotocin-induced diabetes and insulin treatment on the hypothalamic melanocortin system and muscle uncoupling protein 3 expression in rats. Diabetes 49:244-252, 2000
24. Warden C: Genetics of uncoupling proteins in humans. Int J Obes Relat Metab Disord 23 (Suppl. 6):S46-S48, 1999
25. Krook A, Digby J, O'Rahilly S, Zierath JR, Wallberg-Henriksson H: Uncoupling protein 3 is reduced in skeletal muscle of NIDDM patients. Diabetes 47:1528-1531, 1998
26. Vidal-Puig AJ, Grujic D, Zhang CY, Hagen T, Boss O, Ido Y, Szczepanik A, Wade J, Mootha V, Cortright R, Muoio DM, Lowell BB: Energy metabolism in uncoupling protein 3 gene knockout mice. J Biol Chem 275:16258-16266, 2000
27. Hong Y, Fink BD, Dillon JS, Sivitz WI: Effects of adenoviral overexpression of uncoupling protein-2 and -3 on mitochondrial respiration in insulinoma cells. Endocrinology 142:249-256, 2001
28. Fink BD, Hong YS, Mathahs MM, Scholz TD, Dillon JS, Sivitz WI: UCP2-dependent proton leak in isolated mammalian mitochondria. J Biol Chem 277:3918-3925, 2002
29. Ward MW, Rego AC, Frenguelli BG, Nicholls DG: Mitochondrial membrane potential and glutamate excitotoxicity in cultured cerebellar granule cells. J Neurosci 20:7208-7219, 2000
30. Vidal-Puig A, Solanes G, Grujic D, Flier JS, Lowell BB: UCP3: an uncoupling protein homologue expressed preferentially and abundantly in skeletal muscle and brown adipose tissue. Biochem Biophys Res Commun 235:79-82, 1997
31. Muzzin P, Boss O, Giacobino JP: Uncoupling protein 3: its possible biological role and mode of regulation in rodents and humans. J Bioenerg Biomembr 31:467-473, 1999
32. Du XL, Edelstein D, Dimmeler S, Ju Q, Sui C, Brownlee M: Hyperglycemia inhibits endothelial nitric oxide synthase activity by posttranslational modification at the Akt site. J Clin Invest 108:1341-1348, 2001
33. Huang TJ, Price SA, Chilton L, Calcutt NA, Tomlinson DR, Verkhratsky A, Fernyhough P: Insulin prevents depolarization of the mitochondrial inner membrane in sensory neurons of type 1 diabetic rats in the presence of sustained hyperglycemia. Diabetes 52:2129-2136, 2003
34. Berent-Spillson A, Russell JW: Metabotropic glutamate receptor regulation of neuronal injury. Exp Neurol 184:97-105, 2003
35. Sayers NM, Beswick LJ, Middlemas A, Calcutt NA, Mizisin AP, Tomlinson DR, Fernyhough P: Neurotrophin-3 prevents the proximal accumulation of neurofilament proteins in sensory neurons of streptozocin-induced diabetic rats. Diabetes 52:2372-2380, 2003
36. Kishi M, Tanabe J, Schmelzer JD, Low PA: Morphometry of dorsal root ganglion in chronic experimental diabetic neuropathy. Diabetes 51:819-824, 2002
37. Zochodne DW, Verge VM, Cheng C, Sun H, Johnston J: Does diabetes target ganglion neurones? Progressive sensory neuron involvement in long-term experimental diabetes. Brain 124:2319-2334, 2001
38. Virag L, Szabo C: The therapeutic potential of poly(ADP-ribose) polymerase inhibitors. Pharmacol Rev 54:375-429, 2002
39. Murphy AN, Fiskum G, Beal MF: Mitochondria in neurodegeneration: bioenergetic function in cell life and death. J Cereb Blood Flow Metab 19:231-245, 1999
40. Pedraza N, Solanes G, Carmona MC, Iglesias R, Vinas O, Mampel T, Vazquez M, Giralt M, Villarroya F: Impaired expression of the uncoupling protein-3 gene in skeletal muscle during lactation: fibrates and troglitazone reverse lactation-induced downregulation of the uncoupling protein-3 gene. Diabetes 49:1224-1230, 2000
41. Schrauwen P, Hesselink MK, Blaak EE, Borghouts LB, Schaart G, Saris WH, Keizer HA: Uncoupling protein 3 content is decreased in skeletal muscle of patients with type 2 diabetes. Diabetes 50:2870-2873, 2001
42. Chan CB, De Leo D, Joseph JW, McQuaid TS, Ha XF, Xu F, Tsushima RG, Pennefather PS, Salapatek AM, Wheeler MB: Increased uncoupling protein-2 levels in β-cells are associated with impaired glucose-stimulated insulin secretion: mechanism of action. Diabetes 50:1302-1310, 2001
43. Dalgaard LT, Pedersen O: Uncoupling proteins: functional characteristics and role in the pathogenesis of obesity and type II diabetes. Diabetologia 44:946-965, 2001
44. Zhang CY, Baffy G, Perret P, Krauss S, Peroni O, Grujic D, Hagen T, Vidal-Puig AJ, Boss O, Kim YB, Zheng XX, Wheeler MB, Shulman GI, Chan CB, Lowell BB: Uncoupling protein-2 negatively regulates insulin secretion and is a major link between obesity, beta cell dysfunction, and type 2 diabetes. Cell 105:745-755, 2001
45. Esterbauer H, Schneitler C, Oberkofler H, Ebenbichler C, Paulweber B, Sandhofer F, Ladurner G, Hell E, Strosberg AD, Patsch JR, Krempler F, Patsch W: A common polymorphism in the promoter of UCP2 is associated with decreased risk of obesity in middle-aged humans. Nat Genet 28:178-183, 2001
46. Harper JA, Stuart JA, Jekabsons MB, Roussel D, Brindle KM, Dickinson K, Jones RB, Brand MD: Artifactual uncoupling by uncoupling protein 3 in yeast mitochondria at the concentrations found in mouse and rat skeletal-muscle mitochondria. Biochem J 361:49-56, 2002