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Diabetes & C-Peptide pp 79–92Cite as

The Mechanisms Underlying the Effects of C-Peptide on Type 1 Diabetic Neuropathy

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Part of the book series: Contemporary Diabetes ((CDI))

Abstract

Diabetic polyneuropathy (DPN) is the most ­common chronic complication of diabetes occurring in approximately 60% of diabetic patients [1–3]. It affects somato-sensory, nociceptive and autonomic peripheral nerves. These involvements may lead to serious consequences such as sensory loss and foot ulcerations, sometimes necessitating limb amputation. A common bothersome symptom is neuropathic pain. Autonomic neuropathy may impact on cardiac and gastrointestinal functions [2, 3].

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References

  1. Greene DA, Sima AAF, Feldman EL, Stevens MJ. Diabetic neuropathy. In: Porte Jr D, Sherwin RS, editors. Ellenberg and rifkin diabetes mellitus. 5th ed. Stanford: Appleton & Lange; 1997. p. 1009–76.

    Google Scholar 

  2. Feldman EL, Stevens MJ, Russell JW, et al. Somatosensory neuropathy. In: Porte DS, Sherwin RS, Baron A, editors. The diabetes mellitus manual. New York: McGraw-Hill; 2005. p. 366–84.

    Google Scholar 

  3. Sima AAF, Kamiya H. Diabetic neuropathy differs in type 1 and type 2 diabetes. Ann N Y Acad Sci. 2006;1084:235–49.

    Article  PubMed  Google Scholar 

  4. Thomas PK, Lascelles RG. Schwann cell abnormalities in diabetic neuropathy. Lancet. 1965;1:1355–7.

    Article  PubMed  CAS  Google Scholar 

  5. Thomas PK, Lascelles RG. The pathology of diabetic neuropathy. Q J Med. 1966;35:489–509.

    Google Scholar 

  6. Thomas PK, Eliasson SG. Diabetic neuropathy. In: Dyck PJ, Thomas PK, Lambert EH, editors. Peripheral neuropathy. Philadelphia: WB Saunders Co.; 1975. p. 956–81.

    Google Scholar 

  7. Sima AAF, Robertson DM. Peripheral neuropathy in mutant diabetic mouse [C57/B1/KS(db/db)]. Acta Neuropathol (Berl). 1978;41:85–9.

    Article  CAS  Google Scholar 

  8. Sima AAF, Bouchier M, Christensen H. Axonal atrophy in sensory nerves of the diabetic BB-Wistar rat, a possible early correlate of human diabetic neuropathy. Ann Neurol. 1983;13:264–72.

    Article  PubMed  CAS  Google Scholar 

  9. Sima AAF, Yagihashi S. Central-peripheral distal axonopathy in the spontaneously diabetic BB-rat: ultrastructural and morphometric findings. Diabetes Res Clin Pract. 1986;1:289–98.

    Article  CAS  Google Scholar 

  10. Sima AAF, Nathaniel V, Bril V, McEwen TAJ, Greene DA. Histopathological heterogeneity of neuropathy in insulin-dependent and non-insulin-dependent diabetes, and demonstration of axo-glial dysjunction in human diabetic neuropathy. J Clin Invest. 1988;81:349–64.

    Article  PubMed  CAS  Google Scholar 

  11. Greene DA, Sima AAF, Pfeifer MA, Albers JW. Diabetic neuropathy. Annu Rev Med. 1990;41:303–17.

    Article  PubMed  CAS  Google Scholar 

  12. Reichard P, Pihl M, Rosenquist U, Sule J. Complications in IDDM are caused by elevated blood glucose level: the Stockholm Diabetes Intervention Study (SDIS) at 10-year follow-up. Diabetologia. 1996;39:1483–8.

    Article  PubMed  CAS  Google Scholar 

  13. The Diabetes Control Complications Trial Research Group. The effect of intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependent diabetes mellitus. N Engl J Med. 1993;329:977–86.

    Article  Google Scholar 

  14. Dyck PJ, Zimmerman BR, Vileu TH, et al. Nerve glucose, fructose, sorbitol, myoinositol, and fiber degeneration and regeneration in diabetic neuropathy. N Engl J Med. 1988;319:542–8.

    Article  PubMed  CAS  Google Scholar 

  15. Hale PJ, Nattrass M, Silverman SH, et al. Peripheral nerve concentrations of glucose, fructose, sorbitol and myoinositol in diabetic and non-diabetic patients. Diabetologia. 1987;30:464–7.

    Article  PubMed  CAS  Google Scholar 

  16. Sima AAF. New insights into the metabolic and molecular basis for diabetic neuropathy. Cell Mol Life Sci. 2003;60:2445–64.

    Article  PubMed  CAS  Google Scholar 

  17. Sima AAF, Bril V, Nathaniel V, et al. Regeneration and repair of myelinated fibers in sural nerve biopsies from patients with diabetic neuropathy treated with an aldose reductase inhibitor. N Engl J Med. 1988;319:548–55.

    Article  PubMed  CAS  Google Scholar 

  18. O’Hare JP, Morgan MH, Alden P, et al. Clinical and neuropsychological studies of one year’s treatment with sorbinil. Diabet Med. 1988;5:537–42.

    Article  PubMed  Google Scholar 

  19. Boulton AJM, Levin S, Comstock J. A multicentre trial of the aldose reductase inhibitor tolrestat, in patients with symptomatic diabetic neuropathy. Diabetologia. 1990;33:431–7.

    Article  PubMed  CAS  Google Scholar 

  20. Sima AAF, Greene DA, Brown MB, et al. Effect of hyperglycemia and the aldose reductase inhibitor tolrestat on sural nerve biochemistry and morphometry in advanced diabetic peripheral polyneuropathy. J Diabetes Complications. 1993;7:157–69.

    Article  PubMed  CAS  Google Scholar 

  21. Greene DA, Arezzo J, Brown M. Effects of aldose reductase inhibition on nerve conduction and morphometry in diabetic neuropathy. Neurology. 1999;53:580–91.

    PubMed  CAS  Google Scholar 

  22. Veves A. Aldose reductase inhibitors for the treatment of diabetic neuropathy. In: Veves A, Malik RA, editors. Diabetic neuropathy. Clinical management. Totowa: Humana Press; 2007. p. 309–20.

    Chapter  Google Scholar 

  23. Ziegler D, Gries FA. Alpha-lipoic acid in the treatment of diabetic peripheral and cardiac autonomic neuropathy. Diabetes. 1997;46 Suppl 2:562–6.

    Google Scholar 

  24. Ziegler D, Schatz H, Conrad F, et al. Effects of treatment with the antioxidant alpha-lipoic acid on cardiac autonomic neuropathy in NIDDM patients. A 4-month randomized controlled multicenter trial (DEKAN Study). Deutsche Kardiale Autonome Neuropathie. Diabetes Care. 1997;20:369–73.

    Article  PubMed  CAS  Google Scholar 

  25. Keen H, Payan J, Allawi J, et al. Treatment of diabetic neuropathy with gamma-linolenic acid. The gamma linolenic acid multicenter trial group. Diabetes Care. 1993;16:8–15.

    Article  PubMed  CAS  Google Scholar 

  26. Stevens MJ, Lattimer SA, Feldman EL, et al. Acetyl-L-carnitine deficiency as a cause of altered nerve myo-inositol content, Na+ K+-ATPase activity and motor conduction velocity in the streptozotocin diabetic rat. Metabolism. 1996;45:865–72.

    Article  PubMed  CAS  Google Scholar 

  27. Sima AAF, Calvani M, Mehra M, Amato A. Acetyl-L-carnitine improves pain, vibratory perception and nerve morphology in patients with chronic diabetic peripheral neuropathy: an analysis of two randomized, placebo-controlled trials. Diabetes Care. 2005;28:96–101.

    Article  Google Scholar 

  28. Evan JD, Jacobs TF, Evans EV. Role of acetyl-L-carnitine in the treatment of diabetic peripheral neuropathy. Ann Pharmacother. 2008;42:1686–91.

    Article  CAS  Google Scholar 

  29. Wiggins TD, Sullivan KA, Pop-Busui R, et al. Elevated triglycerides correlate with progression of diabetic neuropathy. Diabetes. 2009;58:1634–40.

    Article  CAS  Google Scholar 

  30. UK Prospective Diabetes Study (UKPDS) Group. Intensive blood glucose control with sulphonylureas or insulin compared with conventional treatment and risk of complications in patients with type 2 diabetes. Lancet. 1998;352:S37–53.

    Article  Google Scholar 

  31. Burger AJ, Weinrauch LA, D’Elia JA, Aronson D. Effect of glycemic control on heart rate variability in type 1 diabetic patients with cardiac autonomic neuropathy. Am J Cardiol. 1999;84:687–91.

    Article  PubMed  CAS  Google Scholar 

  32. Cheatham B, Kahn R. Insulin action and the insulin signaling network. Endocr Rev. 1995;16:117–42.

    PubMed  CAS  Google Scholar 

  33. Brussee V, Cunningham FA, Zochodne DW. Direct insulin signaling of neurons reverses diabetic neuropathy. Diabetes. 2004;53:1824–30.

    Article  PubMed  CAS  Google Scholar 

  34. Sima AAF, Kamiya H. Insulin, C-peptide and diabetic neuropathy. Sci Med. 2004;10:308–19.

    Google Scholar 

  35. Pierson CR, Zhang W, Murakawa Y, Sima AAF. Early gene responses of trophic factors differ in nerve regeneration in type 1 and type 2 diabetic ­neuropathy. J Neuropathol Exp Neurol. 2002;61:857–71.

    PubMed  CAS  Google Scholar 

  36. Pant HC, Veeranna, Grant P. Regulation of axonal neurofilament phosphorylation. Curr Top Cell Regul. 2000;36:133–50.

    Article  CAS  PubMed  Google Scholar 

  37. Greene DA, Yagihashi S, Lattimer SA, Sima AAF. Nerve Na+-K+-ATPase, conduction and myo-inositol in the insulin deficient BB-rat. Am J Physiol. 1984;247:E534–9.

    PubMed  CAS  Google Scholar 

  38. Sima AAF, Brismar T. Reversible diabetic nerve dysfunction. Structural correlates to electrophysiological abnormalities. Ann Neurol. 1985;18:21–9.

    Article  PubMed  CAS  Google Scholar 

  39. Vague P, Dufayet D, Coste T, et al. Association of diabetic neuropathy with Na/K ATPase gene polymorphism. Diabetologia. 1997;40:506–11.

    Article  PubMed  CAS  Google Scholar 

  40. Stevens MJ, Dananberg J, Feldman EL, et al. The linked roles of nitric oxide, aldose reductase and (Na+, K+)-ATPase in the slowing of nerve conduction in the streptozotocin diabetic rat. Metabolism. 1996;45:865–72.

    Article  PubMed  CAS  Google Scholar 

  41. Stevens MJ, Zhang W, Li F, Sima AAF. C-peptide corrects endoneurial blood flow but not oxidative stress in type 1 BB/Wor-rats. Am J Physiol. 2004;287:E497–505.

    CAS  Google Scholar 

  42. Xu G, Sima AAF. Altered immediate early gene expression is impaired in diabetic nerve: implications in regeneration. J Neuropathol Exp Neurol. 2001;60(10):972–83.

    PubMed  CAS  Google Scholar 

  43. Pierson CR, Zhang W, Murakawa Y, Sima AAF. Insulin deficiency rather than hyperglycemia accounts for impaired neurotrophic responses and nerve fiber regeneration in type 1 diabetic neuropathy. J Neuropathol Exp Neurol. 2003;62:260–71.

    PubMed  CAS  Google Scholar 

  44. Pierson CR, Zhang W, Sima AAF. Proinsulin C-peptide replacement in type 1 diabetic BB/Wor-rats prevents deficits in nerve fiber regeneration. J Neuropathol Exp Neurol. 2003;62:765–79.

    PubMed  CAS  Google Scholar 

  45. Sima AAF, Zhang W, Li Z-G, Murakawa Y, Pierson CR. Molecular alterations underlie nodal and paranodal degeneration in type 1 diabetic neuropathy and are prevented by C-peptide. Diabetes. 2004;53:1556–63.

    Article  PubMed  CAS  Google Scholar 

  46. Bierhaus A, Schiekofer S, Schwarninger M, et al. Diabetes associated sustained activation of the transcription factor nuclear factor-kappa B. Diabetes. 2001;50:2792–806.

    Article  PubMed  CAS  Google Scholar 

  47. Ramasamy R, Vanucci SJ, Yau SO, et al. Advanced glycation end product and RAGE: a common thread in aging, diabetes, neurodegeneration and inflammation. Glycobiology. 2004;15:16R–28.

    Article  CAS  Google Scholar 

  48. Cifarelli V, Luppi P, Tse HM, et al. Human proinsulin C-peptide reduces high glucose induced proliferation and NF-kappaB activation in smooth muscle cells. Atherosclerosis. 2008;201:248–57.

    Article  PubMed  CAS  Google Scholar 

  49. McGuire JF, Rouen S, Siegfreid E, Wright DE, Dobrowsky RT. Caveolin-1 and altered neuroregulin signaling contribute to the pathophysiological progression of diabetic peripheral neuropathy. Diabetes. 2009;58:2677–86.

    Article  PubMed  CAS  Google Scholar 

  50. Steiner DF, Cunningham L, Spigelman L, Aben B. Insulin biosynthesis: evidence for a precursor. Science. 1967;157:697–700.

    Article  PubMed  CAS  Google Scholar 

  51. Johansson B-L, Linde B, Wahren J. Effect of C-peptide on blood flow, capillary diffusion capacity and glucose utilization in the exercising forms of type 1 (insulin-dependent) diabetic patients. Diabetologia. 1992;35:1151–8.

    Article  PubMed  CAS  Google Scholar 

  52. Johansson B-L, Borg K, Fernquist-Forbes E, et al. Beneficial effects of C-peptide on incipient nephropathy and neuropathy in patients with type 1 diabetes mellitus. Diabet Med. 2000;17:181–9.

    Article  PubMed  CAS  Google Scholar 

  53. Rigler R, Pramanik A, Jonasson P, et al. Specific binding of the proinsulin C-peptide to human cell membranes. Proc Natl Acad Sci USA. 1999;46:13318–23.

    Article  Google Scholar 

  54. Grunberger G, Qiang X, Li Z-G, et al. Molecular basis for the insulinomimetic effects of C-peptide. Diabetologia. 2001;44:1247–57.

    Article  PubMed  CAS  Google Scholar 

  55. Li Z-G, Qiang X, Sima AAF, Grunberger G. C-peptide attenuates protein tyrosine phosphatase activity and enhances glycogen synthesis in L6 myoblasts. Biochem Biophys Res Commun. 2001;26:615–9.

    Article  CAS  Google Scholar 

  56. Othomo Y, Aperia A, Sahlgren B, Johansson B-L, Wahren J. C-peptide stimulates rat renal tubular Na+, K+-ATPase activity in synergism with neuropeptide Y. Diabetologia. 1996;39:199–205.

    Article  Google Scholar 

  57. Zhang W, Yorek M, Pierson CR, et al. Human C-peptide dose dependently prevents early neuropathy in the BB/Wor-rat. Int J Exp Diabetes Res. 2001;2(3):187–94.

    Article  PubMed  CAS  Google Scholar 

  58. Cotter MA, Ekberg K, Wahren J, Cameron NE. Effects of proinsulin C-peptide in experimental diabetic neuropathy: vascular actions and modulation by nitric oxide synthase inhibition. Diabetes. 2003;52:1812–7.

    Article  PubMed  CAS  Google Scholar 

  59. Jägerbrink T, Landahl E, Shafqat J, Jörnvall H. Proinsulin C-peptide interaction with protein tyrosine phosphatase 1B demonstrated with a labeling reaction. Biochem Biophys Res Commun. 2009;387:31–5.

    Article  PubMed  CAS  Google Scholar 

  60. Sima AAF. Diabetic neuropathy in type 1 and type 2 diabetes and the effects of C-peptide. Neurol Sci. 2004;220:133–6.

    Article  Google Scholar 

  61. Shafqat J, Melles E, Sigmudsson K, et al. Proinsulin C-peptide elicits disaggregation of insulin resulting in enhanced physiological insulin effects. Cell Mol Life Sci. 2006;63:1805–11.

    Article  PubMed  CAS  Google Scholar 

  62. Medawala W, McCahill P, Giebink A, et al. A molecular level understanding of zinc activation of C-peptide and its effects on cellular communications in the bloodstream. Rev Diabet Stud. 2009;6:148–58.

    Article  PubMed  Google Scholar 

  63. Jörnvall H, Lindahl E, Astorga-Wells J, et al. Oligomerization and insulin interactions of proinsulin C-peptide: threefold relationships to properties of insulin. Biochem Biophys Res Commun. 2010;391:1561–6.

    Article  PubMed  CAS  Google Scholar 

  64. Lindahl E, Nyman U, Melles E, et al. Cellular internalization of proinsulin C-peptide. Cell Mol Life Sci. 2007;64:479–86.

    Article  PubMed  CAS  Google Scholar 

  65. Luppi P, Geng X, Cifarelli V, Drain P, Trucco M. C-peptide is internalized in human endothelial and vascular smooth muscle cells via early endosomes. Diabetologia. 2009;52:2218–28.

    Article  PubMed  CAS  Google Scholar 

  66. Lindahl E, Nyman U, Zaman F, et al. Proinsulin C-peptide regulates ribosomal RNA expression. J Biol Chem. 2010;285:3462–9.

    Article  PubMed  CAS  Google Scholar 

  67. Xu G, Murakawa Y, Pierson CR, Sima AAF. Altered β-tubulin and neurofilament expression and impaired axonal growth in diabetic nerve regeneration. J Neuropathol Exp Neurol. 2002;61:164–75.

    PubMed  CAS  Google Scholar 

  68. Li Z-G, Zhang W, Sima AAF. C-peptide enhances insulin-mediated cell growth and protection against high glucose induced apoptosis in SH-SY5Y cells. Diabetes Metab Res Rev. 2003;19:375–85.

    Article  PubMed  CAS  Google Scholar 

  69. Sima AAF, Li Z-G. The effect of C-peptide on ­cognitive dysfunction and hippocampal apoptosis in type 1 diabetes. Diabetes. 2005;54:1497–505.

    Article  PubMed  CAS  Google Scholar 

  70. Luppi P, Cifarelli V, Tse H, Piganelli J, Trucco M. Human C-peptide antagonizes high glucose-induced endothelial dysfunction through the nuclear factor-κB pathway. Diabetologia. 2008;51:1534–43.

    Article  PubMed  CAS  Google Scholar 

  71. Sima AAF, Zhang W, Kreipke CW, Rafols JA, Hoffman WH. Inflammation in diabetic encephalopathy is prevented by C-peptide. Rev Diabet Stud. 2009;6:37–42.

    Article  PubMed  Google Scholar 

  72. Sima AAF. Can the BB-rat help to unravel diabetic neuropathy? Annotation. Neuropathol Appl Neurobiol. 1985;11:253–64.

    Article  PubMed  CAS  Google Scholar 

  73. Sima AAF, Kamiya H. Is C-peptide replacement the missing link for successful treatment of neurological complications in type 1 diabetes? Curr Drug Targets. 2008;9:37–46.

    Article  PubMed  CAS  Google Scholar 

  74. Cameron NE, Cotter MA. Metabolic and vascular factors in the pathogenesis of diabetic neuropathy. Diabetes. 1997;46 Suppl 2:S31–7.

    PubMed  CAS  Google Scholar 

  75. Brismar T, Sima AAF. Changes in nodal function in nerve fibres of the spontaneously diabetic BB-Wistar rat. Potential clamp analysis. Acta Physiol Scand. 1981;113:499–506.

    Article  PubMed  CAS  Google Scholar 

  76. Greene DA, Lattimer SA, Sima AAF. Sorbitol, phosphoinositides and sodium-potassium ATPase in the pathogenesis of diabetic complications. N Engl J Med. 1987;316:599–606.

    Article  PubMed  CAS  Google Scholar 

  77. Sugimoto K, Murakawa Y, Zhang W-X, Xu G, Sima AAF. Insulin receptor in rat peripheral nerve: its localization and alternatively spliced isoforms. Diabetes Metab Res Rev. 2000;16(5):354–63.

    Article  PubMed  CAS  Google Scholar 

  78. Kutanyra T, Kimura K, Makondo K, et al. Proinsulin C-peptide increases nitric oxide production by enhancing mitogen-activated protein-kinase-dependent transcription of endothelial nitric oxide synthase in aortic enothelial cells of Wistar-rats. Diabetologia. 2003;46:1698–705.

    Article  CAS  Google Scholar 

  79. Sima AAF. Heterogeneity of diabetic neuropathy. Front Biosci. 2008;13:4809–16.

    Article  PubMed  CAS  Google Scholar 

  80. Sima AAF, Zhang W-X, Tai J, Tze WJ, Nathaniel V. Diabetic neuropathy in STZ-induced diabetic rat and effect of allogenic islet cell transplantation. Morphometric analysis. Diabetes. 1988;37:1129–36.

    Article  PubMed  CAS  Google Scholar 

  81. Sima AAF, Lattimer SA, Yagihashi S, Greene DA. “Axo-glial dysjunction”: a novel structural lesion that accounts for poorly reversible slowing of nerve conduction in the spontaneously diabetic BB-rat. J Clin Invest. 1986;77:474–84.

    Article  PubMed  CAS  Google Scholar 

  82. Cherian PV, Kamijo M, Angelides KJ, Sima AAF. Nodal Na+-channel displacement is associated with nerve conduction slowing in the chronically diabetic BB/W-rat. Prevention by an aldose reductase inhibitor. J Diabetes Complications. 1996;10:192–200.

    Article  PubMed  CAS  Google Scholar 

  83. Brismar T, Sima AAF, Greene DA. Reversible and irreversible nodal dysfunction in diabetic neuropathy. Ann Neurol. 1987;21:504–7.

    Article  PubMed  CAS  Google Scholar 

  84. Peles E, Nativ M, Lustig M, et al. Identification of a novel contactin-associated transmembrane receptor with multiple domains implicated in protein-protein interactions. EMBO J. 1997;16:978–88.

    Article  PubMed  CAS  Google Scholar 

  85. Ratcliffe CF, Qu V, McCormick KA, et al. A sodium channel signaling complex: modulation by associated receptor protein tyrosine phosphatase β. Nat Neurosci. 2000;3:437–44.

    Article  PubMed  CAS  Google Scholar 

  86. Peles E, Nativ M, Campbell PL, et al. The carbonic anhydrase domain of receptor tyrosine phosphatase beta is a functional ligand for the axonal recognition molecule contactin. Cell. 1995;82:251–60.

    Article  PubMed  CAS  Google Scholar 

  87. Johnson KG, Van Vactor D. Receptor protein tyrosine phosphases in nervous system development. Physiol Rev. 2003;83:1–24.

    PubMed  CAS  Google Scholar 

  88. Purves T, Middlemas A, Agthong S, et al. A role for mitogen-activated protein kinases in the etiology of diabetic neuropathy. FASEB J. 2001;15:2508–14.

    Article  PubMed  CAS  Google Scholar 

  89. Sugimoto K, Murakawa Y, Sima AAF. Expression and localization of insulin receptor in rat dorsal root ganglion and spinal cord. J Pheripher Nerve Syst. 2002;7:44–53.

    Article  CAS  Google Scholar 

  90. Kamiya H, Murakawa Y, Zhang W, Sima AAF. Unmyelinated fiber sensory neuropathy differs in type 1 and type 2 diabetes. Diabetes Metab Res Rev. 2005;21:448–58.

    Article  PubMed  CAS  Google Scholar 

  91. Sima AAF, Zhang W-X, Sugimoto K, et al. C-peptide prevents and improves chronic type 1 diabetic neuropathy in the BB/Wor-rat. Diabetologia. 2001;44:889–97.

    Article  PubMed  CAS  Google Scholar 

  92. Terada M, Yasuda H, Kikkawa R. Delayed Wallerian degeneration and increased neurofilament phosphorylation in sciatic nerves of rats with streptozotocin-induced diabetes. J Neurol Sci. 1998;155:23–30.

    Article  PubMed  CAS  Google Scholar 

  93. Brownlees J, Yates A, Bajaj NP, et al. Phosphorylation of neurofilament heavy chain side-arms by stress activated protein kinase – 1b/Jun N-terminal kinase-3. J Cell Sci. 2000;113:401–7.

    PubMed  CAS  Google Scholar 

  94. Kamiya H, Zhang W, Sima AAF. Dynamic changes of neuroskeletal proteins underlie impaired axonal maturation and progressive degeneration in type 1 diabetes. Exp Diabetes Res. 2009;2009:793281.

    PubMed  Google Scholar 

  95. Fernyhough P, Mill JF, Roberts JL, Ishii DN. Stabilization of tubulin mRNA’s by insulin and insulin-like growth factor-1 during neurite formation. Mol Brain Res. 1989;6:109–20.

    Article  PubMed  CAS  Google Scholar 

  96. Verge VNK, Tetzlatt W, Bisby MA, Richardson PM. Influence of nerve growth factor on neurofilament gene expression in mature primary sensory neurons. J Neurosci. 1990;10:2018–25.

    PubMed  CAS  Google Scholar 

  97. Fernyhough P, Willars GB, Lindsay RM, Tomlinson DR. Insulin and insulin-like growth factor I enhance regeneration in cultured adult rat sensory neurons. Brain. 1993;607:117–24.

    Article  CAS  Google Scholar 

  98. Gilron I, Flatters SJ. Gabapentin and pregabalin for the treatment of neuropathic pain: a review of laboratory and clinical evidence. Pain Res Manag. 2006;11(Suppl A):16–29.

    Google Scholar 

  99. Ramos KM, Jiang Y, Svensson CI, Calcutt NA. Pathogenesis of spinally mediated hyperalgesia in diabetes. Diabetes. 2007;56:1569–76.

    Article  PubMed  CAS  Google Scholar 

  100. Burchiel KJ, Russel LC, Lee RP, Sima AAF. Spontaneous activity of primary afferent neurons in diabetic BB-Wistar rats. A possible mechanism of chronic diabetic pain. Diabetes. 1985;34:1210–3.

    Article  PubMed  CAS  Google Scholar 

  101. Hirade M, Yasuda H, Omatsu-Kanbe M, Kikkawa R, Kitasato H. Tetrodotoxin-resistant sodium channels of dorsal root ganglion neurons are readily activated in diabetic rats. Neuroscience. 1999;90:933–7.

    Article  PubMed  CAS  Google Scholar 

  102. Bachouja M-M. Pathophysiology of neuropathic pain. In: Veves A, Malik RA, editors. Diabetic neuropathy. Clinical management. Totowa: Humana Press; 2007. p. 339–50.

    Google Scholar 

  103. Kamiya H, Zhang W, Sima AAF. C-peptide prevents nociceptive sensory neuropathy in type 1 diabetes. Ann Neurol. 2004;56:827–35.

    Article  PubMed  CAS  Google Scholar 

  104. Kamiya H, Zhang W, Ekberg K, Wahren J, Sima AAF. C-peptide reverses nociceptive neuropathy in type 1 diabetic BB/Wor-rat. Diabetes. 2006;55:3581–7.

    Article  PubMed  CAS  Google Scholar 

  105. Kamiya H, Zhang W, Sima AAF. Degeneration of Golgi and neuronal loss in DRG’s in diabetic BB/Wor-rats. Diabetologia. 2006;49:2763–74.

    Article  PubMed  CAS  Google Scholar 

  106. Kapur D. Neuropathic pain and diabetes. Diabetes Metab Res Rev. 2003;19:S9–15.

    Article  PubMed  CAS  Google Scholar 

  107. Kamijo M, Merry AC, Akdas G, Cherian PV, Sima AAF. Nerve fiber regeneration following axotomy in the diabetic BB/W-rat. The effect of ARI-treatment. J Diabetes Complications. 1996;10:183–91.

    Article  PubMed  CAS  Google Scholar 

  108. Sima AAF, Levitan I, Ristic H, Kamijo M. Nerve fiber regeneration in the spontaneously diabetic BB/W-rat. In: Hotta N, Greene DA, Ward JD, Sima AAF, Boulton AJM, editors. Diabetic neuropathy: new concepts and insights. Amsterdam: Elsevier; 1995. p. 27–36.

    Google Scholar 

  109. Ide C. Peripheral nerve regeneration. Neurosci Res. 1996;25:101–21.

    PubMed  CAS  Google Scholar 

  110. Ishii DN, Glazner GW, Pu S. Role of insulin-like growth factor in peripheral nerve regeneration. Mol Neurobiol. 1997;14:67–116.

    Article  Google Scholar 

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Authors and Affiliations

  1. Department of Pathology, Wayne State University and Detroit Medical Center, 540 E. Canfield Avenue, Detroit, MI, 48201, USA

    Hideki Kamiya, Wei-Xian Zhang & Anders A. F. Sima

  2. Department of Endocrinology and Diabetes, Graduate School of Medicine, University of Nagoya, Nagoya, 466-8550, Japan

    Hideki Kamiya

  3. Department of Neurology, Wayne State University and Detroit Medical Center, Detroit, MI, 48201, USA

    Anders A. F. Sima

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  1. Hideki Kamiya
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    Anders A.F. Sima

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Kamiya, H., Zhang, WX., Sima, A.A.F. (2012). The Mechanisms Underlying the Effects of C-Peptide on Type 1 Diabetic Neuropathy. In: Sima, A. (eds) Diabetes & C-Peptide. Contemporary Diabetes. Humana Press. https://doi.org/10.1007/978-1-61779-391-2_8

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