Decreased glycolytic and tricarboxylic acid cycle intermediates coincide with peripheral nervous system oxidative stress in a murine model of type 2 diabetes

Journal of Endocrinology

Volumn 216, Issue 1, 2013, Pages 1-11

  Hinder, Lucy M ^a   Vivekanandan Giri, Anuradha ^a   McLean, Lisa L ^a   Pennathur, Subramaniam ^a   Feldman, Eva L ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Diabetes; Dorsal root ganglia; Metabolomics; Neuropathy; Sciatic nerve; Sural nerve

Indexed keywords

2,3 DIPHOSPHOGLYCERIC ACID; 3 NITROTYROSINE; ACONITATE HYDRATASE; FRUCTOSE 1,6 BISPHOSPHATE; FRUCTOSE 6 PHOSPHATE; GLUCOSE 6 PHOSPHATE; LACTIC ACID; PHOSPHOENOLPYRUVATE; 3-NITROTYROSINE; DRUG DERIVATIVE; LEPTIN RECEPTOR; LEPTIN RECEPTOR, MOUSE; TYROSINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CITRIC ACID CYCLE; CONTROLLED STUDY; DISEASE MODEL; ELECTROSPRAY MASS SPECTROMETRY; ENZYME ACTIVITY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; LIPID OXIDATION; LIQUID CHROMATOGRAPHY; MALE; METABOLOME; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OXIDATIVE STRESS; PERIPHERAL NERVOUS SYSTEM; PRIORITY JOURNAL; SCIATIC NERVE; SPINAL GANGLION; SURAL NERVE; TANDEM MASS SPECTROMETRY; ANIMAL; DIABETIC NEUROPATHY; DOWN REGULATION; ENZYMOLOGY; GENETICS; GLYCOLYSIS; LIPID PEROXIDATION; METABOLISM; MOUSE MUTANT; NERVE CELL;

ACONITATE HYDRATASE; ANIMALS; CITRIC ACID CYCLE; DIABETES MELLITUS, TYPE 2; DIABETIC NEUROPATHIES; DISEASE MODELS, ANIMAL; DOWN-REGULATION; GANGLIA, SPINAL; GLYCOLYSIS; LIPID PEROXIDATION; MALE; MICE; MICE, MUTANT STRAINS; NEURONS; OXIDATIVE STRESS; PERIPHERAL NERVOUS SYSTEM; RECEPTORS, LEPTIN; SCIATIC NERVE; SURAL NERVE; TYROSINE;

MLCS; MLOWN;

EID: 84874405179     PISSN: 00220795     EISSN: 14796805     Source Type: Journal    
DOI: 10.1530/JOE-12-0356     Document Type: Article

References (55)

1. Akude E, Zherebitskaya E, Chowdhury SK, Smith DR, Dobrowsky RT & Fernyhough P 2011 Diminished superoxide generation is associated with respiratory chain dysfunction and changes in the mitochondrial proteome of sensory neurons from diabetic rats. Diabetes 60 288-297
2. Brownlee M 2001 Biochemistry and molecular cell biology of diabetic complications. Nature 414 813-820
3. Callaghan BC, Hur J & Feldman EL 2012 Diabetic neuropathy: one disease or two? Current Opinion in Neurology 25 536-541
4. CDCP 2011 National diabetes fact sheet: national estimates and general information on diabetes and prediabetes in the United States. U.S. Department of Health and Human Services, Centers for Disease Control and Prevention, Atlanta, GA.
5. Cheng HT, Dauch JR, Hayes JM, Hong Y & Feldman EL 2009 Nerve growth factor mediates mechanical allodynia in a mouse model of type 2 diabetes. Journal of Neuropathology and Experimental Neurology 68 1229-1243
6. Chowdhury SK, Zherebitskaya E, Smith DR, Akude E, Chattopadhyay S, Jolivalt CG, Calcutt NA & Fernyhough P 2010 Mitochondrial respiratory chain dysfunction in dorsal root ganglia of streptozotocininduced diabetic rats and its correction by insulin treatment. Diabetes 59 1082-1091
7. Corbett JA, Tilton RG, Chang K, Hasan KS, Ido Y, Wang JL, Sweetland MA, Lancaster JR Jr, Williamson JR & McDaniel ML 1992 Aminoguanidine, a novel inhibitor of nitric oxide formation, prevents diabetic vascular dysfunction. Diabetes 41 552-556
8. Du XL, Edelstein D, Rossetti L, Fantus IG, Goldberg H, Ziyadeh F, Wu J & Brownlee M 2000 Hyperglycemia-induced mitochondrial superoxide overproduction activates the hexosamine pathway and induces plasminogen activator inhibitor-1 expression by increasing Sp1 glycosylation. PNAS 97 12222-12226
9. Du Y, Smith MA, Miller CM & Kern TS 2002 Diabetes-induced nitrative stress in the retina, and correction by aminoguanidine. Journal of Neurochemistry 80 771-779
10. Edwards JL, Vincent AM, Cheng HT & Feldman EL 2008 Diabetic neuropathy: mechanisms to management. Pharmacology & Therapeutics 120 1-34
11. Erecinska M, Nelson D, Deas J & Silver IA 1996 Limitation of glycolysis by hexokinase in rat brain synaptosomes during intense ion pumping. Brain Research 726 153-159
12. Feldman EL 2008 Diabetic neuropathy. Current Drug Targets 9 1-2
13. Gardiner NJ, Wang Z, Luke C, Gott A, Price SA & Fernyhough P 2007 Expression of hexokinase isoforms in the dorsal root ganglion of the adult rat and effect of experimental diabetes. Brain Research 1175 143-154
14. Gardner PR & Fridovich I 1992 Inactivation-reactivation of aconitase in Escherichia coli. A sensitive measure of superoxide radical. Journal of Biological Chemistry 267 8757-8763.
15. Gardner PR, Raineri I, Epstein LB&WhiteCW 1995 Superoxide radical and iron modulate aconitase activity in mammalian cells. Journal of Biological Chemistry 270 13399-13405
16. Gibson GE, Starkov A, Blass JP, Ratan RR & Beal MF 2010 Cause and consequence: mitochondrial dysfunction initiates and propagates neuronal dysfunction, neuronal death and behavioral abnormalities in age-associated neurodegenerative diseases. Biochimica et Biophysica Acta 1802 122-134
17. Greene DA & Winegrad AI 1979 In vitro studies of the substrates for energy production and the effects of insulin on glucose utilization in the neural components of peripheral nerve. Diabetes 28 878-887
18. Kishi Y, Schmelzer JD, Yao JK, Zollman PJ, Nickander KK, Tritschler HJ & Low PA 1999 a-Lipoic acid: effect on glucose uptake, sorbitol pathway, and energy metabolism in experimental diabetic neuropathy. Diabetes 48 2045-2051
19. Lorenz MA, Burant CF & Kennedy RT 2011 Reducing time and increasing sensitivity in sample preparation for adherent mammalian cell metabolomics. Analytical Chemistry 83 3406-3414
20. Obrosova IG & Stevens MJ 1999 Effect of dietary taurine supplementation on GSH and NAD(P)-redox status, lipid peroxidation, and energy metabolism in diabetic precataractous lens. Investigative Ophthalmology & Visual Science 40 680-688
21. Obrosova I, Cao X, Greene DA & Stevens MJ 1998 Diabetes-induced changes in lens antioxidant status, glucose utilization and energy metabolism: effect of DL-a-lipoic acid. Diabetologia 41 1442-1450
22. Obrosova IG, Fathallah L, Lang HJ & Greene DA 1999 Evaluation of a sorbitol dehydrogenase inhibitor on diabetic peripheral nerve metabolism: a prevention study. Diabetologia 42 1187-1194
23. Obrosova IG, Mabley JG, Zsengeller Z, Charniauskaya T, Abatan OI, Groves JT & Szabo C 2005a Role for nitrosative stress in diabetic neuropathy: evidence from studies with a peroxynitrite decomposition catalyst. FASEB Journal 19 401-403
24. Obrosova IG, Pacher P, Szabo C, Zsengeller Z, Hirooka H, Stevens MJ & Yorek MA 2005b Aldose reductase inhibition counteracts oxidative- nitrosative stress and poly(ADP-ribose) polymerase activation in tissue sites for diabetes complications. Diabetes 54 234-242
25. Ola MS, Berkich DA, Xu Y, King MT, Gardner TW, Simpson I & LaNoue KF 2006 Analysis of glucose metabolism in diabetic rat retinas. American Journal of Physiology. Endocrinology and Metabolism 290 E1057-E1067
26. Pande M, Hur J, Hong Y, Backus C, Hayes JM, Oh SS, Kretzler M & Feldman EL 2011 Transcriptional profiling of diabetic neuropathy in the BKS db/db mouse: a model of type 2 diabetes. Diabetes 60 1981-1989
27. Pennathur S, Bergt C, Shao B, Byun J, Kassim SY, Singh P, Green PS, McDonald TO, Brunzell J, Chait A et al. 2004 Human atherosclerotic intima and blood of patients with established coronary artery disease contain high density lipoprotein damaged by reactive nitrogen species. Journal of Biological Chemistry 279 42977-42983
28. Pennathur S, Ido Y, Heller JI, Byun J, Danda R, Pergola P, Williamson JR & Heinecke JW 2005 Reactive carbonyls and polyunsaturated fatty acids produce a hydroxyl radical-like species: a potential pathway for oxidative damage of retinal proteins in diabetes. Journal of Biological Chemistry 280 22706-22714
29. Russell JW, Sullivan KA, Windebank AJ, Herrmann DN & Feldman EL 1999 Neurons undergo apoptosis in animal and cell culture models of diabetes. Neurobiology of Disease 6 347-363
30. Said G 2007 Diabetic neuropathy - a review. Nature Clinical Practice. Neurology 3 331-340
31. Shun CT, Chang YC, Wu HP, Hsieh SC, Lin WM, Lin YH, Tai TY & Hsieh ST 2004 Skin denervation in type 2 diabetes: correlations with diabetic duration and functional impairments. Brain 127 1593-1605
32. Stevens MJ, Obrosova I, Cao X, Van Huysen C & Greene DA 2000 Effects of DL-a-lipoic acid on peripheral nerve conduction, blood flow, energy metabolism, and oxidative stress in experimental diabetic neuropathy. Diabetes 49 1006-1015
33. Sullivan KA, Brown MS, Harmon L & Greene DA 2003 Digital electron microscopic examination of human sural nerve biopsies. Journal of the Peripheral Nervous System 8 260-270
34. Sullivan KA, Hayes JM, Wiggin TD, Backus C, Su Oh S, Lentz SI, Brosius F III & Feldman EL 2007 Mouse models of diabetic neuropathy. Neurobiology of Disease 28 276-285
35. Suzuki J, Akahane K, Nakamura J, Naruse K, Kamiya H, Himeno T, Nakamura N, Shibata T, Kondo M, Nagasaki H et al. 2011 Palmitate induces apoptosis in Schwann cells via both ceramide-dependent and independent pathways. Neuroscience 176 188-198
36. Thurston JH, McDougal DB Jr, Hauhart RE, SchulzDW 1995 Effects of acute, subacute, and chronic diabetes on carbohydrate and energy metabolism in rat sciatic nerve. Relation to mechanisms of peripheral neuropathy. Diabetes 44 190-195
37. Tomlinson DR & Gardiner NJ 2008 Glucose neurotoxicity. Nature Reviews. Neuroscience 9 36-45
38. Tretter L & Adam-Vizi V 2000 Inhibition of Krebs cycle enzymes by hydrogen peroxide: a key role of [a]-ketoglutarate dehydrogenase in limiting NADH production under oxidative stress. Journal of Neuroscience 20 8972-8979.
39. Tretter L & Adam-Vizi V 2004 Generation of reactive oxygen species in the reaction catalyzed by a-ketoglutarate dehydrogenase. Journal of Neuroscience 24 7771-7778
40. Tretter L & Adam-Vizi V 2005 a-Ketoglutarate dehydrogenase: a target and generator of oxidative stress. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 360 2335-2345
41. van der Veen RC & Roberts LJ 1999 Contrasting roles for nitric oxide and peroxynitrite in the peroxidation of myelin lipids. Journal of Neuroimmunology 95 1-7
42. Vincent AM & Feldman EL 2004 New insights into the mechanisms of diabetic neuropathy. Reviews in Endocrine & Metabolic Disorders 5 227-236
43. Vincent AM, Russell JW, Low P & Feldman EL 2004 Oxidative stress in the pathogenesis of diabetic neuropathy. Endocrine Reviews 25 612-628
44. Vincent AM, McLean LL, Backus C & Feldman EL 2005 Short-term hyperglycemia produces oxidative damage and apoptosis in neurons. FASEB Journal 19 638-640
45. Vincent AM, Hayes JM, McLean LL, Vivekanandan-Giri A, Pennathur S & Feldman EL 2009a Dyslipidemia-induced neuropathy in mice: the role of oxLDL/LOX-1. Diabetes 58 2376-2385
46. Vincent AM, Hinder LM, Pop-Busui R & Feldman EL 2009b Hyperlipidemia: a new therapeutic target for diabetic neuropathy. Journal of the Peripheral Nervous System 14 257-267
47. Vincent AM, Kato K, McLean LL, Soules ME & Feldman EL 2009c Sensory neurons and Schwann cells respond to oxidative stress by increasing antioxidant defense mechanisms. Antioxidants & Redox Signaling 11 425-438
48. Vincent AM, Callaghan BC, Smith AL & Feldman EL 2011 Diabetic neuropathy: cellularmechanisms as therapeutic targets. Nature Reviews. Neurology 7 573-583
49. Vitadello M, Couraud JY, Hassig R, Gorio A & Di Giamberardino L 1983 Axonal transport of acetylcholinesterase in the diabetic mutant mouse. Experimental Neurology 82 143-147
50. Vitadello M, Filliatreau G, Dupont JL, Hassig R, Gorio A & Di Giamberardino L 1985 Altered axonal transport of cytoskeletal proteins in the mutant diabetic mouse. Journal of Neurochemistry 45 860-868
51. Vivekanandan-Giri A, Byun J & Pennathur S 2011 Quantitative analysis of amino acid oxidation markers by tandem mass spectrometry. Methods in Enzymology 491 73-89
52. Wiggin TD, Kretzler M, Pennathur S, Sullivan KA, Brosius FC & Feldman EL 2008 Rosiglitazone treatment reduces diabetic neuropathy in streptozotocin-treated DBA/2J mice. Endocrinology 149 4928-4937
53. Young MJ, Boulton AJ, MacLeod AF, Williams DR & Sonksen PH 1993 A multicentre study of the prevalence of diabetic peripheral neuropathy in the United Kingdom hospital clinic population. Diabetologia 36 150-154
54. Yudkoff M, Nelson D, Daikhin Y & Erecinska M 1994 Tricarboxylic acid cycle in rat brain synaptosomes. Fluxes and interactions with aspartate aminotransferase and malate/aspartate shuttle. Journal of Biological Chemistry 269 27414-27420.
55. Zhang L, YuC, Vasquez FE, Galeva N, Onyango I, Swerdlow RH&Dobrowsky RT 2010 Hyperglycemia alters the Schwann cellmitochondrial proteome and decreases coupled respiration in the absence of superoxide production. Journal of Proteome Research 9 458-471