Metabolic dysfunction is restricted to the sciatic nerve in experimental diabetic neuropathy

Diabetes

Volumn 65, Issue 1, 2016, Pages 228-238

  Freeman, Oliver J ^a,b   Unwin, Richard D ^b,c   Dowsey, Andrew W ^b,c   Begley, Paul ^b,c   Ali, Sumia ^a   Hollywood, Katherine A ^b,c   Rustogi, Nitin ^b,c   Petersen, Rasmus S ^a   Dunn, Warwick B ^b,c   Cooper, Garth J S ^b,c,d,e   Gardiner, Natalie J ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b MANCHESTER UNIVERSITY NHS FOUNDATION TRUST   (United Kingdom)

^c UNIVERSITY OF MANCHESTER   (United Kingdom)

^d UNIVERSITY OF AUCKLAND   (New Zealand)

^e UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

POLYOL; ACYLCARNITINE; CARNITINE; FRUCTOSE; GLUCOSE; INOSITOL; POLYMER; SCYLLITOL; SORBITOL;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL BODY; CONTROLLED STUDY; LIPID METABOLISM; MALE; METABOLIC DISORDER; METABOLOMICS; NONHUMAN; OXIDATIVE PHOSPHORYLATION; OXIDATIVE STRESS; PATHOGENESIS; PERIPHERAL NERVOUS SYSTEM; PRIORITY JOURNAL; PROTEOMICS; RAT; SCHWANN CELL; SCIATIC NERVE; SPINAL GANGLION; STREPTOZOTOCIN-INDUCED DIABETIC NEUROPATHY; TRIGEMINUS GANGLION; UPREGULATION; ANALOGS AND DERIVATIVES; ANIMAL; COMPLICATION; DIABETIC NEUROPATHIES; DISEASE MODEL; ENERGY METABOLISM; EXPERIMENTAL DIABETES MELLITUS; HOMEOSTASIS; LUMBAR VERTEBRA; METABOLISM; MITOCHONDRION; NERVE CONDUCTION; SPRAGUE DAWLEY RAT;

ANIMALS; CARNITINE; DIABETES MELLITUS, EXPERIMENTAL; DIABETIC NEUROPATHIES; DISEASE MODELS, ANIMAL; ENERGY METABOLISM; FRUCTOSE; GANGLIA, SPINAL; GLUCOSE; HOMEOSTASIS; INOSITOL; LIPID METABOLISM; LUMBAR VERTEBRAE; METABOLOMICS; MITOCHONDRIA; NEURAL CONDUCTION; OXIDATIVE PHOSPHORYLATION; OXIDATIVE STRESS; POLYMERS; RATS; RATS, SPRAGUE-DAWLEY; SCIATIC NERVE; SORBITOL; TRIGEMINAL GANGLION;

EID: 84962182345     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db15-0835     Document Type: Article

References (34)

1. Callaghan BC, Cheng HT, Stables CL, Smith AL, Feldman EL. Diabetic neuropathy: clinical manifestations and current treatments. Lancet Neurol 2012; 11:521-534
2. Said G. Diabetic neuropathy-a review. Nat Clin Pract Neurol 2007;3:331-340
3. Boulton AJ, Kempler P, Ametov A, Ziegler D. Whither pathogenetic treatments for diabetic polyneuropathy? Diabetes Metab Res Rev 2013;29:327-333
4. Tomlinson DR, Gardiner NJ. Glucose neurotoxicity. Nat Rev Neurosci 2008; 9:36-45
5. Zenker J, Ziegler D, Chrast R. Novel pathogenic pathways in diabetic neuropathy. Trends Neurosci 2013;36:439-449
6. Price SA, Zeef LA, Wardleworth L, Hayes A, Tomlinson DR. Identification of changes in gene expression in dorsal root ganglia in diabetic neuropathy: correlation with functional deficits. J Neuropathol Exp Neurol 2006;65:722-732
7. Pande M, Hur J, Hong Y, et al. Transcriptional profiling of diabetic neuropathy in the BKS db/db mouse: a model of type 2 diabetes. Diabetes 2011;60:1981-1989
8. Hur J, Sullivan KA, Pande M, et al. The identification of gene expression profiles associated with progression of human diabetic neuropathy. Brain 2011;134:3222-3235
9. Akude E, Zherebitskaya E, Chowdhury SK, Smith DR, Dobrowsky RT, Fernyhough P. 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
10. Zhang L, Yu C, Vasquez FE, et al. Hyperglycemia alters the Schwann cell mitochondrial proteome and decreases coupled respiration in the absence of superoxide production. J Proteome Res 2010;9:458-471
11. Hinder LM, Vivekanandan-Giri A, McLean LL, Pennathur S, Feldman EL. Decreased glycolytic and tricarboxylic acid cycle intermediates coincide with peripheral nervous system oxidative stress in a murine model of type 2 diabetes. J Endocrinol 2013;216:1-11
12. Ali S, Driscoll HE, Newton VL, Gardiner NJ. Matrix metalloproteinase-2 is downregulated in sciatic nerve by streptozotocin induced diabetes and/or treatment with minocycline: implications for nerve regeneration. Exp Neurol 2014;261:654-665
13. Begley P, Francis-McIntyre S, Dunn WB, et al.; HUSERMET Consortium. Development and performance of a gas chromatography-time-of-flight mass spectrometry analysis for large-scale nontargeted metabolomic studies of human serum. Anal Chem 2009;81:7038-7046
14. Dunn WB, Broadhurst D, Begley P, et al.; Human Serum Metabolome (HUSERMET) Consortium. Procedures for large-scale metabolic profiling of serum and plasma using gas chromatography and liquid chromatography coupled to mass spectrometry. Nat Protoc 2011;6:1060-1083
15. Unwin RD, Griffiths JR, Whetton AD. Simultaneous analysis of relative protein expression levels across multiple samples using iTRAQ isobaric tags with 2D nano LC-MS/MS. Nat Protoc 2010;5:1574-1582
16. Hadfield JD. MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R package. J Stat Softw 2010;33:1-22
17. Morris JS, Brown PJ, Herrick RC, Baggerly KA, Coombes KR. Bayesian analysis of mass spectrometry proteomic data using wavelet-based functional mixed models. Biometrics 2008;64:479-489
18. Biessels GJ, Bril V, Calcutt NA, et al. Phenotyping animal models of diabetic neuropathy: a consensus statement of the diabetic neuropathy study group of the EASD (NeuroDiab). J Peripher Nerv Syst 2014;19:77-87
19. Finegold D, Lattimer SA, Nolle S, Bernstein M, Greene DA. Polyol pathway activity and myo-inositol metabolism. A suggested relationship in the patho-genesis of diabetic neuropathy. Diabetes 1983;32:988-992
20. Wang X, Schwarz TL. The mechanism of Ca2+ -dependent regulation of kinesin-mediated mitochondrial motility. Cell 2009;136:163-174
21. Brownlee M. Biochemistry and molecular cell biology of diabetic complications. Nature 2001;414:813-820
22. Hamid HS, Mervak CM, Münch AE, et al. Hyperglycemia- and neuropathy-induced changes in mitochondria within sensory nerves. Ann Clin Transl Neurol 2014;1:799-812
23. Viader A, Golden JP, Baloh RH, Schmidt RE, Hunter DA, Milbrandt J. Schwann cell mitochondrial metabolism supports long-term axonal survival and peripheral nerve function. J Neurosci 2011;31:10128-10140
24. Beirowski B, Babetto E, Golden JP, et al. Metabolic regulator LKB1 is crucial for Schwann cell-mediated axon maintenance. Nat Neurosci 2014;17:1351-1361
25. Véga C, Martiel JL, Drouhault D, Burckhart MF, Coles JA. Uptake of locally applied deoxyglucose, glucose and lactate by axons and Schwann cells of rat vagus nerve. J Physiol 2003;546:551-564
26. Jiang Y, Calcutt NA, Ramos KM, Mizisin AP. Novel sites of aldose reductase immunolocalization in normal and streptozotocin-diabetic rats [published correction appears in J Peripher Nerv Syst 2007;12:64]. J Peripher Nerv Syst 2006; 11:274-285
27. Ludvigson MA, Sorenson RL. Immunohistochemical localization of aldose reductase. I. Enzyme purification and antibody preparation-localization in peripheral nerve, artery, and testis. Diabetes 1980;29:438-449
28. Fünfschilling U, Supplie LM, Mahad D, et al. Glycolytic oligodendrocytes maintain myelin and long-term axonal integrity. Nature 2012;485:517-521
29. Morrison BM, Tsingalia A, Vidensky S, et al. Deficiency in monocarboxylate transporter 1 (MCT1) in mice delays regeneration of peripheral nerves following sciatic nerve crush. Exp Neurol 2015;263:325-338
30. Viader A, Sasaki Y, Kim S, et al. Aberrant Schwann cell lipid metabolism linked to mitochondrial deficits leads to axon degeneration and neuropathy. Neuron 2013;77:886-898
31. Zochodne DW, Verge VM, Cheng C, Sun H, Johnston J. Does diabetes target ganglion neurones? Progressive sensory neurone involvement in long-term experimental diabetes. Brain 2001;124:2319-2334
32. Cheng C, Zochodne DW. Sensory neurons with activated caspase-3 survive long-term experimental diabetes. Diabetes 2003;52:2363-2371
33. Toth C, Brussee V, Zochodne DW. Remote neurotrophic support of epidermal nerve fibres in experimental diabetes. Diabetologia 2006;49:1081-1088
34. Brussee V, Cunningham FA, Zochodne DW. Direct insulin signaling of neurons reverses diabetic neuropathy. Diabetes 2004;53:1824-1830