Novel pathogenic pathways in diabetic neuropathy

Trends in Neurosciences

Volumn 36, Issue 8, 2013, Pages 439-449

  Zenker, Jennifer ^a   Ziegler, Dan ^b   Chrast, Roman ^a  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

^b UNIVERSITY HOSPITAL DÜSSELDORF   (Germany)

Author keywords

Axon; Diabetic neuropathy; Insulin resistance; Ion channels; Mitochondria; Schwann cell

Indexed keywords

ACTOVEGIN; ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); ADENOSINE TRIPHOSPHATE; BENFOTIAMINE; EPALRESTAT; GLUCOSE; GLUCOSE TRANSPORTER; ILOPROST; INOSITOL; INSULIN; INSULIN RECEPTOR; ION CHANNEL; LACTIC ACID; MYELIN; NICOTINIC ACID; PEROXYNITRITE; POTASSIUM CHANNEL; RIBOFLAVIN; RUBOXISTAURIN; SODIUM CHANNEL; TAURINE; TRANDOLAPRIL; UBIDECARENONE; VITAMIN B GROUP;

ADIPOCYTE; CELL INTERACTION; CELL RESPIRATION; DEMYELINATION; DIABETIC NEUROPATHY; ENERGY METABOLISM; GENE EXPRESSION; GLIA; GLUCOSE METABOLISM; HUMAN; HYPERGLYCEMIA; INSULIN DEPENDENT DIABETES MELLITUS; ION CONDUCTANCE; LIPID METABOLISM; MECHANICAL STIMULATION; MEMBRANE STEADY POTENTIAL; MITOCHONDRION; MYELIN SHEATH; NERVE FIBER; NERVE FIBER DEGENERATION; NEUROPATHOLOGY; NEUROTOXICITY; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PERIPHERAL NERVE; PERIPHERAL NEUROPATHY; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REINFORCEMENT; REPOLARIZATION; REVIEW; SCHWANN CELL; SPINAL GANGLION;

AXON; DIABETIC NEUROPATHY; INSULIN RESISTANCE; ION CHANNELS; MITOCHONDRIA; SCHWANN CELL;

AXONS; DIABETIC NEUROPATHIES; GLUCOSE; HUMANS; INSULIN; ION CHANNELS; PERIPHERAL NERVES; SCHWANN CELLS; SIGNAL TRANSDUCTION;

EID: 84881023484     PISSN: 01662236     EISSN: 1878108X     Source Type: Journal    
DOI: 10.1016/j.tins.2013.04.008     Document Type: Review

References (104)

1. Forbes J.M., Cooper M.E. Mechanisms of diabetic complications. Physiol. Rev. 2013, 93:137-188.
2. Zochodne D.W. Diabetes mellitus and the peripheral nervous system: manifestations and mechanisms. Muscle Nerve 2007, 36:144-166.
3. Callaghan B.C., et al. Diabetic neuropathy: clinical manifestations and current treatments. Lancet Neurol. 2012, 11:521-534.
4. Tesfaye S., et al. Diabetic neuropathies: update on definitions, diagnostic criteria, estimation of severity, and treatments. Diabetes Care 2010, 33:2285-2293.
5. Ziegler D. Current concepts in the management of diabetic polyneuropathy. Curr. Diabetes Rev. 2011, 7:208-220.
6. Papanas N., et al. Neuropathy in prediabetes: does the clock start ticking early?. Nat. Rev. Endocrinol. 2011, 7:682-690.
7. Chao C.Y., Cheing G.L. Microvascular dysfunction in diabetic foot disease and ulceration. Diabetes Metab. Res. Rev. 2009, 25:604-614.
8. Nukada H., et al. Increased susceptibility to ischemia and macrophage activation in STZ-diabetic rat nerve. Brain Res. 2011, 1373:172-182.
9. Chrast R., et al. Lipid metabolism in myelinating glial cells: lessons from human inherited disorders and mouse models. J. Lipid Res. 2011, 52:419-434.
10. Michailov G.V., et al. Axonal neuregulin-1 regulates myelin sheath thickness. Science 2004, 304:700-703.
11. Salzer J.L., et al. Molecular domains of myelinated axons in the peripheral nervous system. Glia 2008, 56:1532-1540.
12. Zenker J., et al. Altered distribution of juxtaparanodal kv1.2 subunits mediates peripheral nerve hyperexcitability in type 2 diabetes mellitus. J. Neurosci. 2012, 32:7493-7498.
13. Sima A.A. The heterogeneity of diabetic neuropathy. Front. Biosci. 2008, 13:4809-4816.
14. Funfschilling U., et al. Glycolytic oligodendrocytes maintain myelin and long-term axonal integrity. Nature 2012, 485:517-521.
15. Lee Y.J., et al. Oligodendroglia metabolically support axons and contribute to neurodegeneration. Nature 2012, 487:443-448.
16. Viader A., et al. Schwann cell mitochondrial metabolism supports long-term axonal survival and peripheral nerve function. J. Neurosci. 2011, 31:10128-10140.
17. Kim B., Feldman E.L. Insulin resistance in the nervous system. Trends Endocrinol. Metab. 2012, 23:133-141.
18. Sugimoto K., et al. Expression and localization of insulin receptor in rat dorsal root ganglion and spinal cord. J. Peripher. Nerv. Syst. 2002, 7:44-53.
19. Shettar A., Muttagi G. Developmental regulation of insulin receptor gene in sciatic nerves and role of insulin on glycoprotein P0 in the Schwann cells. Peptides 2012, 36:46-53.
20. Fernandez A.M., Torres-Aleman I. The many faces of insulin-like peptide signalling in the brain. Nat. Rev. Neurosci. 2012, 13:225-239.
21. Singh B., et al. Resistance to trophic neurite outgrowth of sensory neurons exposed to insulin. J. Neurochem. 2012, 121:263-276.
22. Calcutt N.A., et al. Growth factors as therapeutics for diabetic neuropathy. Curr. Drug Targets 2008, 9:47-59.
23. Kim B., et al. Hyperinsulinemia induces insulin resistance in dorsal root ganglion neurons. Endocrinology 2011, 152:3638-3647.
24. de Preux A.S., et al. SREBP-1c expression in Schwann cells is affected by diabetes and nutritional status. Mol. Cell. Neurosci. 2007, 35:525-534.
25. Tomlinson D.R., Gardiner N.J. Glucose neurotoxicity. Nat. Rev. Neurosci. 2008, 9:36-45.
26. Thorens B., Mueckler M. Glucose transporters in the 21st Century. Am. J. Physiol. Endocrinol. Metab. 2010, 298:E141-E145.
27. Gomez O., et al. Developmental regulation of glucose transporters GLUT3, GLUT4 and GLUT8 in the mouse cerebellar cortex. J. Anat. 2010, 217:616-623.
28. + (MCTs) transporters in rat olfactory epithelia. Chem. Senses 2011, 36:771-780.
29. Magnani P., et al. Glucose transporters in rat peripheral nerve: paranodal expression of GLUT1 and GLUT3. Metabolism 1996, 45:1466-1473.
30. Pande M., et al. Transcriptional profiling of diabetic neuropathy in the BKS db/db mouse: a model of type 2 diabetes. Diabetes 2011, 60:1981-1989.
31. Hur J., et al. The identification of gene expression profiles associated with progression of human diabetic neuropathy. Brain 2011, 134:3222-3235.
32. de Preux Charles A.S., et al. Global transcriptional programs in peripheral nerve endoneurium and DRG are resistant to the onset of type 1 diabetic neuropathy in Ins2 mice. PLoS ONE 2010, 5:e10832.
33. Bakirtzi K., et al. Cerebellar neurons possess a vesicular compartment structurally and functionally similar to Glut4-storage vesicles from peripheral insulin-sensitive tissues. J. Neurosci. 2009, 29:5193-5201.
34. Pierre K., et al. Linking supply to demand: the neuronal monocarboxylate transporter MCT2 and the alpha-amino-3-hydroxyl-5-methyl-4-isoxazole-propionic acid receptor GluR2/3 subunit are associated in a common trafficking process. Eur. J. Neurosci. 2009, 29:1951-1963.
35. Takebe K., et al. Histochemical demonstration of a monocarboxylate transporter in the mouse perineurium with special reference to GLUT1. Biomed. Res. 2008, 29:297-306.
36. Obrosova I.G. Diabetes and the peripheral nerve. Biochim. Biophys. Acta 2009, 1792:931-940.
37. Farmer K.L., et al. Diabetic peripheral neuropathy: should a chaperone accompany our therapeutic approach?. Pharmacol. Rev. 2012, 64:880-900.
38. Chowdhury S.K., et al. The role of aberrant mitochondrial bioenergetics in diabetic neuropathy. Neurobiol. Dis. 2013, 51:56-65.
39. Pellerin L., Magistretti P.J. How to balance the brain energy budget while spending glucose differently. J. Physiol. 2003, 546:325.
40. Perkins G.A., Ellisman M.H. Mitochondrial configurations in peripheral nerve suggest differential ATP production. J. Struct. Biol. 2011, 173:117-127.
41. Vega C., et al. Uptake of locally applied deoxyglucose, glucose and lactate by axons and Schwann cells of rat vagus nerve. J. Physiol. 2003, 546:551-564.
42. Chrast R., et al. Complement factors in adult peripheral nerve: a potential role in energy metabolism. Neurochem. Int. 2004, 45:353-359.
43. Li F., et al. Evaluation of orally active poly(ADP-ribose) polymerase inhibitor in streptozotocin-diabetic rat model of early peripheral neuropathy. Diabetologia 2004, 47:710-717.
44. Obrosova I.G., et al. Early diabetes-induced biochemical changes in the retina: comparison of rat and mouse models. Diabetologia 2006, 49:2525-2533.
45. Price S.A., et al. 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.
46. Zhang L., 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.
47. Chowdhury S.K.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.
48. Akude E., 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.
49. Feige J.N., Auwerx J. Transcriptional coregulators in the control of energy homeostasis. Trends Cell Biol. 2007, 17:292-301.
50. Hinder L.M., et al. Bioenergetics in diabetic neuropathy: what we need to know. J. Peripher. Nerv. Syst. 2012, 17(Suppl. 2):10-14.
51. Vincent A.M., et al. Mitochondrial biogenesis and fission in axons in cell culture and animal models of diabetic neuropathy. Acta Neuropathol. 2010, 120:477-489.
52. Edwards J.L., et al. Diabetes regulates mitochondrial biogenesis and fission in mouse neurons. Diabetologia 2010, 53:160-169.
53. + pump dysfunction in diabetic neuropathy. Brain 2008, 131:1209-1216.
54. Fernyhough P., Calcutt N.A. Abnormal calcium homeostasis in peripheral neuropathies. Cell Calcium 2010, 47:130-139.
55. + currents in human diabetic neuropathy. J. Peripher. Nerv. Syst. 2009, 14:279-284.
56. Krishnan A.V., Kiernan M.C. Altered nerve excitability properties in established diabetic neuropathy. Brain 2005, 128:1178-1187.
57. Sun W., et al. Gastrodin inhibits allodynia and hyperalgesia in painful diabetic neuropathy rats by decreasing excitability of nociceptive primary sensory neurons. PLoS ONE 2012, 7:e39647.
58. Court F.A., Coleman M.P. Mitochondria as a central sensor for axonal degenerative stimuli. Trends Neurosci. 2012, 35:364-372.
59. Calcutt N.A., Backonja M.M. Pathogenesis of pain in peripheral diabetic neuropathy. Curr. Diab. Rep. 2007, 7:429-434.
60. Veves A., et al. Painful diabetic neuropathy: epidemiology, natural history, early diagnosis, and treatment options. Pain Med. 2008, 9:660-674.
61. Rush A.M., et al. Multiple sodium channels and their roles in electrogenesis within dorsal root ganglion neurons. J. Physiol. 2007, 579:1-14.
62. Hong S., et al. Early painful diabetic neuropathy is associated with differential changes in tetrodotoxin-sensitive and -resistant sodium channels in dorsal root ganglion neurons in the rat. J. Biol. Chem. 2004, 279:29341-29350.
63. Hong S., Wiley J.W. Altered expression and function of sodium channels in large DRG neurons and myelinated A-fibers in early diabetic neuropathy in the rat. Biochem. Biophys. Res. Commun. 2006, 339:652-660.
64. Craner M.J., et al. Changes of sodium channel expression in experimental painful diabetic neuropathy. Ann. Neurol. 2002, 52:786-792.
65. Chattopadhyay M., et al. Continuous delta-opioid receptor activation reduces neuronal voltage-gated sodium channel (NaV1.7) levels through activation of protein kinase C in painful diabetic neuropathy. J. Neurosci. 2008, 28:6652-6658.
66. Ren Y.S., et al. Sodium channel Nav1.6 is up-regulated in the dorsal root ganglia in a mouse model of type 2 diabetes. Brain Res. Bull. 2012, 87:244-249.
67. + currents following axotomy of dorsal root ganglion neurons. J. Neurophysiol. 2002, 88:650-658.
68. Debanne D., et al. Axon physiology. Physiol. Rev. 2011, 91:555-602.
69. + channels during the formation of nodes of Ranvier. Neuron 2010, 65:490-502.
70. Bierhaus A., et al. Methylglyoxal modification of Na(v)1.8 facilitates nociceptive neuron firing and causes hyperalgesia in diabetic neuropathy. Nat. Med. 2012, 18:926-933.
71. Jack M.M., et al. Characterisation of glyoxalase I in a streptozocin-induced mouse model of diabetes with painful and insensate neuropathy. Diabetologia 2011, 54:2174-2182.
72. Jack M.M., et al. Protection from diabetes-induced peripheral sensory neuropathy - a role for elevated glyoxalase I?. Exp. Neurol. 2012, 234:62-69.
73. Tomlinson S.E., et al. Nerve excitability studies characterize Kv1.1 fast potassium channel dysfunction in patients with episodic ataxia type 1. Brain 2010, 133:3530-3540.
74. + channel. J. Neurosci. 2004, 24:1236-1244.
75. + channel activity in primary sensory neurons in painful diabetic neuropathy: role of brain-derived neurotrophic factor. J. Neurochem. 2010, 114:1460-1475.
76. + channels in rat coronary microvessels exposed to high glucose. Diabetes 2004, 53:2436-2442.
77. Verkhratsky A., Steinhauser C. Ion channels in glial cells. Brain Res. Brain Res. Rev. 2000, 32:380-412.
78. Pop-Busui R., et al. Effects of prior intensive insulin therapy on cardiac autonomic nervous system function in type 1 diabetes mellitus: the Diabetes Control and Complications Trial/Epidemiology of Diabetes Interventions and Complications study (DCCT/EDIC). Circulation 2009, 119:2886-2893.
79. Ziegler D., et al. Treatment of symptomatic polyneuropathy with actovegin in type 2 diabetic patients. Diabetes Care 2009, 32:1479-1484.
80. Elmlinger M.W., et al. Neuroprotective and anti-oxidative effects of the hemodialysate actovegin on primary rat neurons in vitro. Neuromol. Med. 2011, 13:266-274.
81. Dyck P.J., et al. Challenges in design of multicenter trials: end points assessed longitudinally for change and monotonicity. Diabetes Care 2007, 30:2619-2625.
82. Ziegler D., et al. Efficacy and safety of antioxidant treatment with alpha-lipoic acid over 4 years in diabetic polyneuropathy: the NATHAN 1 trial. Diabetes Care 2011, 34:2054-2060.
83. Perry C.G., et al. Methods for assessing mitochondrial function in diabetes. Diabetes 2013, 62:1041-1053.
84. Chowdhury S.K.R., 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.
85. Urban M.J., et al. Heat shock response and insulin-associated neurodegeneration. Trends Pharmacol. Sci. 2012, 33:129-137.
86. Korngut L., et al. Overexpression of human HSP27 protects sensory neurons from diabetes. Neurobiol. Dis. 2012, 47:436-443.
87. Wilson L., et al. Pyruvate induces mitochondrial biogenesis by a PGC-1 alpha-independent mechanism. Am. J. Physiol. Cell Physiol. 2007, 292:C1599-C1605.
88. Perumal S.S., et al. Energy-modulating vitamins - a new combinatorial therapy prevents cancer cachexia in rat mammary carcinoma. Br. J. Nutr. 2005, 93:901-909.
89. Oron U., et al. Ga-As (808nm) laser irradiation enhances ATP production in human neuronal cells in culture. Photomed. Laser Surg. 2007, 25:180-182.
90. Yazdani S.O., et al. Effects of low level laser therapy on proliferation and neurotrophic factor gene expression of human schwann cells in vitro. J. Photochem. Photobiol. B 2012, 107:9-13.
91. Saleh A., et al. Ciliary neurotrophic factor activates NF-kappa B to enhance mitochondrial bioenergetics and prevent neuropathy in sensory neurons of streptozotocin-induced diabetic rodents. Neuropharmacology 2013, 65:65-73.
92. Wang S.S., et al. Functional trade-offs in white matter axonal scaling. J. Neurosci. 2008, 28:4047-4056.
93. Perge J.A., et al. Why do axons differ in caliber?. J. Neurosci. 2012, 32:626-638.
94. Shevalye H., et al. Metanx alleviates multiple manifestations of peripheral neuropathy and increases intraepidermal nerve fiber density in Zucker diabetic fatty rats. Diabetes 2012, 61:2126-2133.
95. Askwith T., et al. Taurine reduces nitrosative stress and nitric oxide synthase expression in high glucose-exposed human Schwann cells. Exp. Neurol. 2012, 233:154-162.
96. Rosker C., et al. The TTX metabolite 4,9-anhydro-TTX is a highly specific blocker of the Na(v1.6) voltage-dependent sodium channel. Am. J. Physiol. Cell Physiol. 2007, 293:C783-C789.
97. Wallace C.H., et al. Inhibition of cardiac voltage-gated sodium channels by grape polyphenols. Br. J. Pharmacol. 2006, 149:657-665.
98. Lagouge M., et al. Resveratrol improves mitochondrial function and protects against metabolic disease by activating SIRT1 and PGC-1alpha. Cell 2006, 127:1109-1122.
99. Cheng A.S., et al. Resveratrol upregulates Nrf2 expression to attenuate methylglyoxal-induced insulin resistance in Hep G2 cells. J. Agric. Food Chem. 2012, 60:9180-9187.
100. Melstrom L.G., et al. Apigenin inhibits the GLUT-1 glucose transporter and the phosphoinositide 3-kinase/Akt pathway in human pancreatic cancer cells. Pancreas 2008, 37:426-431.
101. Wood T.E., et al. A novel inhibitor of glucose uptake sensitizes cells to FAS-induced cell death. Mol. Cancer Ther. 2008, 7:3546-3555.
102. Sullivan K.A., et al. Mouse models of diabetic neuropathy. Neurobiol. Dis. 2007, 28:276-285.
103. Homs J., et al. Comparative study of peripheral neuropathy and nerve regeneration in NOD and ICR diabetic mice. J. Peripher. Nerv. Syst. 2011, 16:213-227.
104. Sima A.A. New insights into the metabolic and molecular basis for diabetic neuropathy. Cell. Mol. Life Sci. 2003, 60:2445-2464.