Development of selective axonopathy in adult sensory neurons isolated from diabetic rats: Role of glucose-induced oxidative stress

Diabetes

Volumn 58, Issue 6, 2009, Pages 1356-1364

  Zherebitskaya, Elena ^a   Akude, Eli ^a,b   Smith, Darrell R ^a,b   Fernyhough, Paul ^a,b  

^a ST BONIFACE GENERAL HOSPITAL   (Canada)

^b UNIVERSITY OF MANITOBA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

4 HYDROXYNONENAL; GLUCOSE; MANGANESE SUPEROXIDE DISMUTASE; MANNITOL; REACTIVE OXYGEN METABOLITE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL SURVIVAL; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DIABETIC NEUROPATHY; DISEASE PREDISPOSITION; IMMUNOFLUORESCENCE; INSULIN DEPENDENT DIABETES MELLITUS; MALE; NERVE DEGENERATION; NERVE FIBER GROWTH; NEUROPATHY; NONHUMAN; OXIDATIVE STRESS; PHENOTYPE; PRIORITY JOURNAL; RAT; SELECTIVE AXONOPATHY; SENSORY NERVE CELL; SPINAL GANGLION; STREPTOZOCIN DIABETES;

AGING; ANIMALS; AXONS; CASPASES; DIABETES MELLITUS, EXPERIMENTAL; GLUCOSE; MALE; NEUROFILAMENT PROTEINS; OXIDATIVE STRESS; RATS; RATS, SPRAGUE-DAWLEY; SENSORY RECEPTOR CELLS; SUPEROXIDE DISMUTASE;

EID: 66649095843     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db09-0034     Document Type: Article

References (43)

1. Malik RA, Tesfaye S, Newrick PG, Walker D, Rajbhandari SM, Siddique I, Sharma AK, Boulton AJ, King RH, Thomas PK, Ward JD. Sural nerve pathology in diabetic patients with minimal but progressive neuropathy. Diabetologia 2005;48:578-585 (Pubitemid 40487306)
2. Yagihashi S. Pathology and pathogenetic mechanisms of diabetic neuropathy. Diabetes Metab Rev 1995;11:193-225
3. Vincent AM, Brownlee M, Russell JW. Oxidative stress and programmed cell death in diabetic neuropathy. Ann N Y Acad Sci 2002;959:368-383 (Pubitemid 34457577)
4. 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 2002;16:1738-1748 (Pubitemid 35340354)
5. Vincent AM, Olzmann JA, Brownlee M, Sivitz WI, Russell JW. Uncoupling proteins prevent glucose-induced neuronal oxidative stress and programmed cell death. Diabetes 2004;53:726-734 (Pubitemid 38270643)
6. Vincent AM, McLean LL, Backus C, Feldman EL. Short-term hyperglycemia produces oxidative damage and apoptosis in neurons. FASEB J 2005;19:638-640 (Pubitemid 40471270)
7. Kennedy JM, Zochodne DW. Experimental diabetic neuropathy with spontaneous recovery: is there irreparable damage? Diabetes 2005;54:830-837
8. Cheng C, Zochodne DW. Sensory neurons with activated caspase-3 survive long-term experimental diabetes. Diabetes 2003;52:2363-2371 (Pubitemid 37059508)
9. 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 (Pubitemid 33055375)
10. Kamiya H, Zhangm W, Sima AA. 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 (Pubitemid 43334387)
11. Kamiya H, Zhang W, Sima AA. Degeneration of the Golgi and neuronal loss in dorsal root ganglia in diabetic BioBreeding/Worcester rats. Diabetologia 2006;49:2763-2774
12. Jiang Y, Zhang JS, Jakobsen J. Differential effect of p75 neurotrophin receptor on expression of pro-apoptotic proteins c-jun, p38 and caspase-3 in dorsal root ganglion cells after axotomy in experimental diabetes. Neuroscience 2005;132:1083-1092 (Pubitemid 40602542)
13. Kalichman MW, Powell HC, Mizisin AP. Reactive, degenerative, and proliferative Schwann cell responses in experimental galactose and human diabetic neuropathy. Acta Neuropathol 1998;95:47-56 (Pubitemid 28075926)
14. Schmidt RE, Dorsey D, Parvin CA, Beaudet LN, Plurad SB, Roth KA. Dystrophic axonal swellings develop as a function of age and diabetes in human dorsal root ganglia. J Neuropathol Exp Neurol 1997;56:1028-1043 (Pubitemid 27386132)
15. Schmidt RE, Beaudet LN, Plurad SB, Dorsey DA. Axonal cytoskeletal pathology in aged and diabetic human sympathetic autonomic ganglia. Brain Res 1997;769:375-383 (Pubitemid 27461476)
16. Lindsay RM. Nerve growth factors (NGF, BDNF) enhance axonal regeneration but are not required for survival of adult sensory neurons. J Neurosci 1988;8:2394-2405 (Pubitemid 18195210)
17. 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 2003;52:2129-2136 (Pubitemid 36919808)
18. Huang TJ, Sayers NM, Verkhratsky A, Fernyhough P. Neurotrophin-3 prevents mitochondrial dysfunction in sensory neurons of streptozotocin-diabetic rats. Exp Neurol 2005;194:279-283 (Pubitemid 40719762)
19. Huang TJ, Verkhratsky A, Fernyhough P. Insulin enhances mitochondrial inner membrane potential and increases ATP levels through phosphoinositide 3-kinase in adult sensory neurons. Mol Cell Neurosci 2005;28:42-54 (Pubitemid 39656010)
20. Fernyhough P, Smith DR, Schapansky J, Van Der Ploeg R, Gardiner NJ, Tweed CW, Kontos A, Freeman L, Purves-Tyson TD, Glazner GW. Activation of nuclear factor-kappaB via endogenous tumor necrosis factor alpha regulates survival of axotomized adult sensory neurons. J Neurosci 2005;25:1682-1690 (Pubitemid 40279273)
21. Mattson MP, Barger SW, Begley JG, Mark RJ. Calcium, free radicals, and excitotoxic neuronal death in primary cell culture. Methods Cell Biol 1995;46:187-216
22. Gardiner NJ, Fernyhough P, Tomlinson DR, Mayer U, von der Mark H, Streuli CH. Alpha7 integrin mediates neurite outgrowth of distinct populations of adult sensory neurons. Mol Cell Neurosci 2005;28:229-240 (Pubitemid 40202585)
23. Gumy LF, Bampton ET, Tolkovsky AM. 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
24. Purves T, Middlemas A, Agthong S, Jude EB, Boulton AJ, Fernyhough P, Tomlinson DR. A role for mitogen-activated protein kinases in the etiology of diabetic neuropathy. FASEB J 2001;15:2508-2514 (Pubitemid 33063180)
25. Yu C, Rouen S, Dobrowsky RT. Hyperglycemia and downregulation of caveolin-1 enhance neuregulin-induced demyelination. Glia 2008;56:877-887
26. Sango K, Horie H, Saito H, Ajiki K, Tokashiki A, Takeshita K, Ishigatsubo Y, Kawano H, Ishikawa Y. Diabetes is not a potent inducer of neuronal cell death in mouse sensory ganglia, but it enhances neurite regeneration in vitro. Life Sci 2002;71:2351-2368 (Pubitemid 35264610)
27. Bianchi R, Buyukakilli B, Brines M, Savino C, Cavaletti G, Oggioni N, Lauria G, Borgna M, Lombardi R, Cimen B, Comelekoglu U, Kanik A, Tataroglu C, Cerami A, Ghezzi P. Erythropoietin both protects from and reverses experimental diabetic neuropathy. Proc Natl Acad Sci U S A 2004;101:823-828 (Pubitemid 38121042)
28. Ebenezer GJ, McArthur JC, Thomas D, Murinson B, Hauer P, Polydefkis M, Griffin JW. Denervation of skin in neuropathies: the sequence of axonal and Schwann cell changes in skin biopsies. Brain 2007;130:2703-2714 (Pubitemid 47511712)
29. Kennedy WR, Wendelschafer-Crabb G, Johnson T. Quantitation of epidermal nerves in diabetic neuropathy. Neurology 1996;47:1042-1048 (Pubitemid 26362047)
30. Polydefkis M, Hauer P, Sheth S, Sirdofsky M, Griffin JW, McArthur JC. 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 (Pubitemid 38899413)
31. Sima AA, Kamiya H. Diabetic neuropathy differs in type 1 and type 2 diabetes. Ann N Y Acad Sci 2006;1084:235-249 (Pubitemid 47091939)
32. Akkina SK, Patterson CL, Wright DE. GDNF rescues nonpeptidergic unmyelinated primary afferents in streptozotocin-treated diabetic mice. Exp Neurol 2001;167:173-182
33. Calcutt NA, Jolivalt CG, Fernyhough P. Growth factors as therapeutics for diabetic neuropathy. Curr Drug Targets 2008;9:47-59
34. Christianson JA, Riekhof JT, Wright DE. Restorative effects of neurotrophin treatment on diabetes-induced cutaneous axon loss in mice. Exp Neurol 2003;179:188-199
35. Toth C, Brussee V, Zochodne DW. Remote neurotrophic support of epidermal nerve fibres in experimental diabetes. Diabetologia 2006;49:1081-1088
36. Huang TJ, Sayers NM, Fernyhough P, Verkhratsky A. 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 (Pubitemid 34533836)
37. Verkhratsky A, Fernyhough P. Mitochondrial malfunction and Ca2+ dyshomeostasis drive neuronal pathology in diabetes. Cell Calcium 2008;44:112-122
38. Vetter R, Rehfeld U, Reissfelder C, Weiss W, Wagner KD, Gunther J, Hammes A, Tschope C, Dillmann W, Paul M. Transgenic overexpression of the sarcoplasmic reticulum Ca2+ATPase improves reticular Ca2+ handling in normal and diabetic rat hearts. FASEB J 2002;16:1657-1659
39. Price SA, Gardiner NJ, Duran-Jimenez B, Zeef LA, Obrosova IG, Tomlinson DR. Thioredoxin interacting protein is increased in sensory neurons in experimental diabetes. Brain Res 2006;1116:206-214 (Pubitemid 44488597)
40. Delcroix JD, Michael GJ, Priestley JV, Tomlinson DR, Fernyhough P. Effect of nerve growth factor treatment on p75NTR gene expression in lumbar dorsal root ganglia of streptozocin-induced diabetic rats. Diabetes 1998;47:1779-1785 (Pubitemid 28476253)
41. Gardiner NJ, Moffatt S, Fernyhough P, Humphries MJ, Streuli CH, Tomlinson DR. Preconditioning injury-induced neurite outgrowth of adult rat sensory neurons on fibronectin is mediated by mobilisation of axonal alpha5 integrin. Mol Cell Neurosci 2007;35:249-260 (Pubitemid 46843563)
42. Lauria G, Morbin M, Lombardi R, Borgna M, Mazzoleni G, Sghirlanzoni A, Pareyson D. Axonal swellings predict the degeneration of epidermal nerve fibers in painful neuropathies. Neurology 2003;61:631-636 (Pubitemid 37082599)
43. Bernstein BW, Bamburg JR. Actin-ATP hydrolysis is a major energy drain for neurons. J Neurosci 2003;23:1-6 (Pubitemid 36050396)