C-peptide corrects endoneurial blood flow but not oxidative stress in type 1 BB/W or rats

American Journal of Physiology - Endocrinology and Metabolism

Volumn 287, Issue 3 50-3, 2004, Pages

  Stevens, Martin J ^a,d   Zhang, Weixian ^b,c   Li, Fei ^a   Sima, Anders A F ^b,c  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c WAYNE STATE UNIVERSITY   (United States)

^d UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

Author keywords

Oxidative stress; Type 1 and type 2 diabetic neuropathy

Indexed keywords

C PEPTIDE; CATALASE; CYCLOOXYGENASE 1; CYCLOOXYGENASE 2; FLURBIPROFEN; GLUCOSE; GLUTATHIONE TRANSFERASE; ISOPHANE INSULIN; MALONALDEHYDE; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE; NITRIC OXIDE SYNTHASE INHIBITOR; PROSTAGLANDIN SYNTHASE; PROSTAGLANDIN SYNTHASE INHIBITOR; SUPEROXIDE DISMUTASE;

ANIMAL MODEL; ARTICLE; BLOOD FLOW; BODY WEIGHT; CONTROLLED STUDY; DIABETIC NEUROPATHY; GLUCOSE BLOOD LEVEL; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; INSULIN DEPENDENT DIABETES MELLITUS; MALE; NERVE CONDUCTION; NERVE FIBER MEMBRANE; NEUROPATHY; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OSMOTIC PUMP; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT;

ANIMALS; BODY WEIGHT; C-PEPTIDE; DIABETIC NEPHROPATHIES; ENZYME INHIBITORS; HEAT; HINDLIMB; HYPERALGESIA; INSULIN; LIPID PEROXIDATION; MALE; MOTOR NEURONS; NERVE TISSUE; NEURAL CONDUCTION; NEURONS, AFFERENT; NG-NITROARGININE METHYL ESTER; OXIDATIVE STRESS; OXIDOREDUCTASES; RATS; RATS, INBRED BB; RATS, ZUCKER; REACTION TIME; REGIONAL BLOOD FLOW;

EID: 4143066829     PISSN: 01931849     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajpendo.00048.2004     Document Type: Article

References (84)

1. Ahlgren SC and Levine JD. Protein kinase C inhibitors decrease hyperalgesia and C-fiber hyperexcitability in the streptozotocin-diabetic rat. J Neurophysiol 72: 684-692, 1994.
2. Aley K and Levine J. Different peripheral mechanisms mediate enhanced nociception in metabolic/toxic and traumatic painful peripheral neuropathies in the rat. Neuroscience 111: 389-397, 2002.
3. Apfel SC. Neurotrophic factors and diabetic peripheral neuropathy. Eur Neurol 41, Suppl 1: 27-34, 1999.
4. Bravenboer B, Kappelle AC, Hamers FP, van Buren T, Erkelens DW, and Gispen WH. Potential use of glutathione for the prevention and treatment of diabetic neuropathy in the streptozotocin-induced diabetic rat. Diabetologia 35: 813-817, 1992.
5. Brownlee M. Biochemistry and molecular cell biology of diabetic complications. Nature 414: 813-820, 2001.
6. Burchiel KJ, Russell LC, Lee RP, and Sima AAF. Spontaneous activity of primary afferent neurons in diabetic BB/Wistar rats. A possible mechanism of chronic diabetic neuropathic pain. Diabetes 34: 1210-1213, 1985.
7. Cameron NE and Cotter MA. Impaired contraction and relaxation in aorta from streptozotocin-diabetic rats: role of polyol pathway. Diabetologia 35: 1011-1019, 1992.
8. Cameron NE and Cotter MA. Effects of chronic treatment with a nitric oxide donor on nerve conduction abnormalities and endoneurial blood flow in streptozotocin diabetic rats. Eur J Clin Invest 25: 19-24, 1995.
9. Cameron NE and Cotter MA. Oxidative stress and abnormal lipid metabolism in diabetic complications. In: Complications in Diabetes, edited by Sima AAF. Amsterdam: Harwood, 1999, p. 97-130.
10. Cameron NE, Cotter MA, Archibald V, Dines KC, and Maxfield EK, Anti-oxidant and pro-oxidant effects on nerve conduction velocity, endoneurial blood flow and oxygen tension in non-diabetic and streptozotocin-diabetic rats. Diabetologia 37: 449-459, 1994.
11. Cameron NE, Cotter MA, Ferguson K, Robertson S, and Radcliffe MA. Effects of chronic alpha-adrenergic receptor blockade on peripheral nerve conduction, hypoxic resistance, polyols, Na(+)-K(+)-ATPase activity, and vascular supply in STZ-D rats. Diabetes 40: 1652-1658, 1991.
12. Cameron NE, Cotter MA, and Hohman TC. Interactions between essential fatty acid, prostenoid, polyol pathway and nitric oxide metabolism in the neurovascular deficit of diabetic rats. Diabetologia 39: 172-182, 1996.
13. Cameron NE, Cotter MA, and Robertson S. Rapid reversal of a motor nerve conduction deficit in streptozotocin-diabetic rats by the angiotensin converting enzyme inhibitor lisinopril. Acta Diabetol 30: 46-48, 1993.
14. Cameron NE, Jack AM, and Cotter MA. Effect of α-lipoic acid on vascular responses and nociception in diabetic rats. Free Radic Biol Med 31: 125-135, 2001.
15. Ceriello A, Mercuri F, Quagliaro L, Assaloni R, Motz E, Tonutti L, and Taboga C. Detection of nitrotyrosine in the diabetic plasma: evidence of oxidative stress. Diabetologia 44: 834-838, 2001.
16. Chen WQ, Jin H, Nguyen M, Carr J, Lee YJ, Hsu CC, Faiman MD, Schloss JV, and Wu JY. Role of taurine in regulation of intracellular calcium level and neuroprotective function in cultured neurons. J Neurosci Res 66: 612-619, 2001.
17. Chen X and Levine JD. Hyper-responsivity in a subset of C-fiber nociceptors in a model of painful diabetic neuropathy in the rat. Neuroscience 102: 185-192, 2001.
18. Cotter MA and Cameron NE. Correction of neurovascular deficits in diabetic rats by beta2-adrenoceptor agonist and alpha1-adrenoceptor antagonist treatment: interactions with the nitric oxide system. Eur J Pharmacol 343: 217-223, 1998.
19. Cotter MA, Cameron NE, Keegan A, and Dines KC. Effects of acetyl- and proprionyl-L-carnitine on peripheral nerve function and vascular supply in experimental diabetes. Metabolism 44: 1209-1214, 1995.
20. Cotter MA, Ekberg K, Wahren J, and Cameron NE. Effects of proinsulin C-peptide in experimental diabetic neuropathy: vascular actions and modulation by nitric oxide synthase inhibition. Diabetes 52: 1812-1817, 2003.
21. Courteix C, Bardin M, Massol J, Fialip J, Lavarenne J, and Eschalier A. Daily insulin treatment relieves long-term hyperalgesia in streptozotocin diabetic rats. Neuroreport 7: 1922-1924, 1996.
22. Cowell RM and Russell JW. Nitrosative injury and antioxidant therapy in the management of diabetic neuropathy. J Investig Med 52: 33-44, 2004.
23. Cryer B and Feldman M. Cyclooxygenase-1 and cyclooxygenase-2 selectivity of widely used nonsteroidal anti-inflammatory drugs. Am J Med 104:413-421, 1998.
24. El-Remessy AB, Abou-Mohamed G, Caldwell RW, and Caldwell RB. High glucose-induced tyrosine nitration in endothelial cells: role of eNOS uncoupling and aldose reductase activation. Invest Ophthalmol Vis Sci 44: 3135-3143, 2003.
25. Forst T, Kunt T, Pohlmann T, Goitom K, Engelbach M, Beyer J, and Pfützner A. Biological activity of C-peptide on the skin microcirculation in patients with insulin-dependent diabetes mellitus. J Clin Invest 101: 2036-2041, 1998.
26. Greene DA, Lattimer SA, and Sima AAF. Are disturbances of sorbitol, phosphoinositide, and Na+-K+-ATPase regulation involved in pathogenesis of diabetic neuropathy? Diabetes 37: 688-693, 1988.
27. Greene DA, Sima AAF, Stevens MJ, Feldman EL, Killen PD, Henry DN, Thomas T, Dananberg J, and Lattimer SA. Aldose reductase inhibitors: an approach to the treatment of diabetic nerve damage. Diabetes Metab Rev 9: 189-217, 1993.
28. Grunberger G, Qiang X, Li Z, Mathews ST, Sbrissa D, Shisheva A, and Sima AAF. Molecular basis for the insulinomimetic effects of C-peptide. Diabetologia 44: 1247-1257, 2001.
29. Hall K, Liu J, Sima AAF, and Wiley J. Impaired inhibitory G-protein function contributes to increased calcium currents in rats with diabetic neuropathy. J Neurophysiol 86: 760-770, 2001.
30. Hargreaves K, Dubner R, Brown F, Flores C, and Joris J. A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain 32: 77-88, 1988.
31. Hattori Y, Kawasaki H, Abe K, and Kanno M. Superoxide dismutase recovers altered endothelium-dependent relaxation in diabetic rat aorta. Am J Physiol Heart Circ Physiol 261: H1086-H1094, 1991.
32. Ischiropoulos H. Biological tyrosine nitration: a pathophysiological function of nitric oxide and reactive oxygen species. Arch Biochem Biophys 356: 1-11, 1998.
33. Jensen ME and Messina EJ. C-peptide induces a concentration-dependent dilatation of skeletal muscle arterioles only in the presence of insulin. Am J Physiol Heart Circ Physiol 276: H1223-H1228, 1999.
34. Khan GM, Chen SR, and Pan HL. Role of primary afferent nerves in allodynia caused by diabetic neuropathy in rats. Neuroscience 114: 291-299, 2002.
35. Kunt T, Forst T, Class E, Pfützner A, Beyer J, and Wahren J. Activation of endothelial nitric oxide synthase (eNOS) by C-peptide (Abstract). Diabetologia 41A: 176, 1998.
36. Li ZG, Zhang W, and Sima AAF. C-peptide prevents hippocampal apoptosis in type 1 diabetes. Int J Exp Diabetes Res 3: 241-245, 2002.
37. Li ZG, Zhang W, and Sima AAF. C-peptide enhances insulin-mediated cell growth and protection against high glucose-induced apoptosis in SH-SY5Y cells. Diabetes Metab Res Rev 19: 375-385, 2003.
38. Low PA and Nickander KK. Oxygen free radical effects in sciatic nerve in experimental diabetes. Diabetes 40: 873-877, 1991.
39. Low PA, Nickander KK, and Tritschler HJ. The roles of oxidative stress and antioxidant treatment in experimental diabetic neuropathy. Diabetes 46, Suppl 2: 38S-42S, 1997.
40. Maejima K, Nakano S, Himeno M, Tsuda S, Makiishi H, Ito T, Nakagawa A, Kigoshi T, Ishibashi T, Nishio M, and Uchida K. Increased basal levels of plasma nitric oxide in Type 2 diabetic subjects. Relationship to microvascular complications. J Diabetes Complications 15: 135-143, 2001.
41. Meade EA, Smith WL, and DeWitt DL. Differential inhibition of prostaglandin endoperoxide synthase (cyclooxygenase) isozymes by aspirin and other non-steroidal anti-inflammatory drugs. J Biol Chem 268: 6610-6614, 1993.
42. Meiler S, Pechman P, Gebhart G, and Maves T. Nitric oxide mediates thermal behavioral responses of rats to intradermal infection of capsaicin. Neuroscience 50: 7-10, 1997.
43. Moncada S, Palmer RM, and Higgs EA. Biosynthesis of nitric oxide from L-arginine. A pathway for the regulation of cell function and communication. Biochem Pharmacol 38: 1709-1715, 1989.
44. Nagamatsu M, Nickander KK, Schmelzer JD, Ray A, Wittrock DA, Tritschler H, and Low PA. Lipoic acid improves nerve blood flow, reduces oxidative stress, and improves distal nerve conduction in experimental diabetic neuropathy. Diabetes Care 18: 1160-1167, 1995.
45. Nickander KK, Schmelzer JD, Rohwer DA, and Low PA. Effect of alpha-tocopherol deficiency on indices of oxidative stress in normal and diabetic peripheral nerve. J Neurol Sci 126: 6-14, 1994.
46. Obrosova IG, Fathallah L, and Stevens MJ. Taurine counteracts oxidative stress and nerve growth factor deficit in early experimental diabetic neuropathy. Exp Neural 172: 211-219, 2001.
47. Obrosova IG and Stevens MJ. Effect of dietary taurine supplementation on GSH and NAD(P)-redox status, lipid peroxidation, and energy metabolism in diabetic precataractous lens. Invest Ophthalmol Vis Sci 40: 680-688, 1999.
48. Obrosova IG, Van Huysen C, Fathallah L, Cao X, Stevens MJ, and Greene DA. Evaluation of alpha(1)-adrenoceptor antagonist on diabetes-induced changes in peripheral nerve function, metabolism, and antioxidative defense. FASEB J 14: 1548-1558, 2000.
49. Obrosova IG, Van Huysen C, Fathallah L, Cao XC, Greene DA, and Stevens MJ. An aldose reductase inhibitor reverses early diabetes-induced changes in peripheral nerve function, metabolism, and antioxidative defense. FASEB J 16: 123-125, 2002.
50. Pierson CR, Zhang W, Murakawa Y, Sima AAF. Tubulin and neurofilament expression and axonal growth differ in type 1 and type 2 diabetic polyneuropathy. J Neuropath Exp Neural 62: 260-271, 2003.
51. Pierson CR, Zhang W, and Sima AAF. Proinsulin C-peptide replacement in type 1 diabetic BB/Wor-rats prevents deficits in nerve fiber regeneration. J Neuropathol Exp Neural 62: 765-779, 2003.
52. Pop-Busui R, Marinescu V, Van Huysen C, Li F, Sullivan K, Greene DA, Larkin D, and Stevens MJ. Dissection of metabolic, vascular, and nerve conduction interrelationships in experimental diabetic neuropathy by cyclooxygenase inhibition and acetyl-L-carnitine administration. Diabetes 51: 2619-2628, 2002.
53. Pop-Busui R, Sullivan KA, Van Huysen C, Bayer L, Cao X, Towns R, and Stevens MJ. Depletion of taurine in experimental diabetic neuropathy: implications for nerve metabolic, vascular, and functional deficits. Exp Neural 168: 259-272, 2001.
54. Rees DD, Palmer RM, Hodson HF, and Moncada S. A specific inhibitor of nitric oxide formation from L-arginine attenuates endothelium-dependent relaxation. Br J Pharmacol 96: 418-424, 1989.
55. Requena JR and Baynes JW. Studies in animal models on the role of glycation and advanced glycation end-products (AGE's) in the pathogenesis of diabetic complications: pitfalls and limitations. In: Chronic Complications in Diabetes, edited by Sima AAF. Amsterdam: Harwood, 1999, p. 43-70.
56. Rigler R, Pramanik A, Jonasson P, Kratz G, Jansson OT, Nygren P, Stahl S, Ekberg K, Johansson B, Uhlen S, Uhlen M, Jornvall H, and Wahren J. Specific binding of proinsulin C-peptide to human cell membranes. Proc Natl Acad Sci USA 96: 13318-13323, 1999.
57. Ru-Rong J and Woolf CJ. Neuronal plasticity and signal transduction in nociceptive neurons: implications for the initiation and maintenance of pathological pain. Neurobiol Dis: 1-10, 2001.
58. Schmeichel AM, Schmelzer JD, and Low PA. Oxidative injury and apoptosis of dorsal root ganglion neurons in chronic experimental diabetic neuropathy. Diabetes 52: 165-171, 2003.
59. Schmidt RE, Dorsey DA, Beaudet LN, and Peterson RG. Analysis of the Zucker diabetic fatty (ZDF) type 2 diabetic rat model suggests a neurotrophic role for insulin/IGF-I in diabetic autonomie neuropathy. Am J Pathol 163: 21-28, 2003.
60. Schmidt RE, Dorsey DA, McDaniel ML, and Corbett JA. Characterization of NADPH diaphorase activity in rat sympathetic autonomic ganglia-effect of diabetes and aging. Brain Res 617: 343-348, 1993.
61. Shindo H, Thomas TP, Larkin DD, Karihaloo AK, Inada H, Onaya T, Stevens MJ, and Greene DA. Modulation of basal nitric oxide-dependent cyclic-GMP production by ambient glucose, myo-inositol, and protein kinase C in SH-SY5Y human neuroblastoma cells. J Clin Invest 97: 736-745, 1996.
62. Shindo T, Kurihara H, Maemura K, Kurihara Y, Ueda O, Suzuki H, Kuwaki T, Ju KH, Wang Y, Ebihara A, Nishimatsu H, Moriyama N, Fukuda M, Akimoto Y, Hirano H, Morita H, Kumada M, Yazaki Y, Nagai R, and Kimura K. Renal damage and salt-dependent hypertension in aged transgenic mice overexpressing endothelin-1. J Mol Med 80: 105-116, 2002.
63. Sima AAF. C-peptide and diabetic neuropathy. Expert Opinion Invest Drugs 12: 1471-1488, 2003.
64. Sima AAF. New insights into the metabolic and molecular basis for diabetic neuropathy. Cell Mol Life Sci 60: 1-20, 2003.
65. Sima AAF, Bril V, and Greene DA. Pathogenetic heterogeneity in human diabetic neuropathy. Pediatr Adolesc Endocrinol 18: 56-62, 1989.
66. Sima AAF, Nathaniel V, Bril V, McEwen TAJ, and Greene DA. Histopathological heterogeneity of neuropathy in insulin-dependent and non-insulin-dependent diabetes, and demonstrations of axo-glial disjunction in human diabetic neuropathy. J Clin Invest 81: 349-364, 1988.
67. Sima AAF, Zhang W, Sugimoto K, Henry D, Li Z, Wahren J, and Grunberger G. C-peptide prevents and improves chronic Type I diabetic polyneuropathy in the BB/Wor rat. Diabetologia 44: 889-897, 2001.
68. Sima AAF, Zhang W, Xu G, Sugimoto K, Guberski D, and Yorek MA. A comparison of diabetic polyneuropathy in type II diabetic BBZDR/Wor rats and in type I diabetic BB/Wor rats. Diabetologia 43: 786-793, 2000.
69. Sluka K and Willis W. The effects of G-protein kinase inhibitors on the behavioral responses of rats to intradermal injection of capsaicin. Pain 71: 165-178, 1997.
70. Srinivasan S, Stevens M, and Wiley JW. Diabetic peripheral neuropathy: evidence for apoptosis and associated mitochondrial dysfunction. Diabetes 49: 1932-1938, 2000.
71. Stevens EJ, Lockett MJ, Carrington AL, and Tomlinson DR. Essential fatty acid treatment prevents nerve ischemia and associated conduction anomalies in rats with experimental diabetes mellitus. Diabetologia 36: 397-401, 1993.
72. +)-ATPase in the slowing of nerve conduction in the streptozotocin diabetic rat. J Clin Invest 94: 853-859, 1994.
73. Stevens MJ, Lattimer SA, Feldman EL, Helton ED, Millington DS, Sima AAF, and Greene DA. 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 45: 865-872, 1996.
74. Stevens MJ, Obrosova I, Cao X, Van Huysen C, and Greene DA. Effects of DL-α-lipoic acid on peripheral nerve conduction, blood flow, energy metabolism, and oxidative stress in experimental diabetic neuropathy. Diabetes 49: 1006-1015, 2000.
75. Stevens MJ, Obrosova I, Pop-Busui R, Greene DA, and Feldman EL. Pathogenesis of diabetic neuropathy. In: Ellenberg and Rifkin's Diabetes Mellitus, edited by Porte D Jr., Sherwin RS, and Baron A. New York: McGraw-Hill, 2002, p. 747-770.
76. Sugimoto K, Murakawa Y, and Sima AAF. Diabetic neuropathy - a continuing enigma. Diabetes Metab Res Rev 16: 408-433, 2000.
77. Tomlinson DR and Fernyhough P. Neurotrophism in various animal models. In: Chronic Complications in Diabetes, edited by Sima AAF. Amsterdam: Harwood, 1999, p. 167-182.
78. Vincent AM, Brownlee M, and Russell JW. Oxidative stress and programmed cell death in diabetic neuropathy. Ann NY Acad Sci 959: 368-383, 2002.
79. Voitenko N, Kostyuk E, Kruglikov I, and Kostyuk P. Changes in calcium signaling in dorsal horn neurons in rats with streptozotocin-induced diabetes. Neuroscience 94: 887-890, 1999.
80. Wahren J, Ekberg K, Johansson J, Henriksson M, Pramanik A, Johansson BL, Rigler R, and Jornvall H. Role of C-peptide in human physiology. Am J Physiol Endocrinol Metab 278: E759-E768, 2000.
81. Windebank AJ and Feldman EL. Diabetes and the nervous system. In: Neurology and General Medicine (3rd ed.), edited by Aminoff MJ. New York: Churchill Livingstone, 2001, p. 341-364.
82. Yasuda H, Sonobe M, Yamashita M, Terada M, Hatanaka I, Huitian Z, and Shigeta Y. Effect of prostaglandin E1 analogue TFC 612 on diabetic neuropathy in streptozotocin-induced diabetic rats. Comparison with aldose reductase inhibitor ONO 2235. Diabetes 38: 832-838, 1989.
83. Zhang W, Slusher B, Murakawa Y, Wozniak KM, Tsukamoto T, Jackson PF, and Sima AAF. GCPII (NAALADase) inhibition prevents long-term diabetic neuropathy in type 1 diabetic BB/Wor rats. J Neurol Sci 194: 21-28, 2002.
84. Zhang W, Yorek M, Pierson CR, Murakawa Y, Breidenbach A, and Sima AAF. Human C-peptide dose dependently prevents early neuropathy in the BB/Wor-rat. In: J Exp Diabetes Res 2: 187-193, 2001.