Na+/H+exchanger 1 inhibition reverses manifestation of peripheral diabetic neuropathy in type 1 diabetic rats

American Journal of Physiology - Endocrinology and Metabolism

Volumn 305, Issue 3, 2013, Pages

  Lupachyk, Sergey ^a   Watcho, Pierre ^a   Shevalye, Hanna ^a   Vareniuk, Igor ^a   Obrosov, Alexander ^a   Obrosova, Irina G ^a   Yorek, Mark A ^b  

^a PENNINGTON BIOMEDICAL RESEARCH CENTER   (United States)

^b UNIVERSITY OF IOWA   (United States)

Author keywords

Advanced glycation end product; Diabetic peripheral neuropathy; Endoneurial blood flow; Na+ H+ exchanger; Nerve conduction velocity; Vascular reactivity

Indexed keywords

ADVANCED GLYCATION END PRODUCT; CARIPORIDE; SODIUM PROTON EXCHANGE PROTEIN;

ALLODYNIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTERIOLE; ARTICLE; BLOOD FLOW; BLOOD VESSEL REACTIVITY; CELL DENSITY; CONTROLLED STUDY; DIABETES MELLITUS; DIABETIC NEUROPATHY; HYPOALGESIA; INSULIN DEPENDENT DIABETES MELLITUS; MALE; NERVE FIBER; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT; SCIATIC NERVE; SENSORY NERVE CONDUCTION; STREPTOZOCIN DIABETES; WESTERN BLOTTING;

ADVANCED GLYCATION END PRODUCT; DIABETIC PERIPHERAL NEUROPATHY; ENDONEURIAL BLOOD FLOW; NA+/H+ EXCHANGER-; NERVE CONDUCTION VELOCITY; VASCULAR REACTIVITY;

ALDEHYDES; ANIMALS; ARTERIOLES; BEHAVIOR, ANIMAL; BLOOD GLUCOSE; BLOTTING, WESTERN; BODY WEIGHT; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 1; DIABETIC NEUROPATHIES; GLYCOSYLATION END PRODUCTS, ADVANCED; GUANIDINES; MALE; NERVE FIBERS; NITRATES; PAIN MEASUREMENT; PYRUVALDEHYDE; RATS; RATS, WISTAR; REDUCED FOLATE CARRIER PROTEIN; SCIATIC NERVE; SKIN; SULFONES; SUPEROXIDES; TYROSINE;

EID: 84881004137     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00186.2013     Document Type: Article

References (65)

1. Al-Nimer MS, Al-Ani FS, Ali FS. Role of nitrosative and oxidative stress in neuropathy in patients with type 2 diabetes mellitus. J Neurosci Rural Pract 3: 41-44, 2012.
2. Anzawa R, Seki S, Nagoshi T, Taniguchi I, Feuvray D, Yoshimura M. The role of Na+/H+ exchanger in Ca2+ overload and ischemic myocardial damage in hearts from type 2 diabetic db/db mice. Cardiovasc Diabetol 10.1186/1475-2840-11-33, 2012.
3. Askarova S, Yang X, Sheng W, Sun GY, Lee JC. Role of Ap-receptor for advanced glycation endproducts interaction in oxidative stress and cytosolic phospholipase A2 activation in astrocytes and cerebral endothelial cells. Neuroscience 199: 375-385, 2011.
4. Beckman JS. Oxidative damage and tyrosine nitration from peroxynitrite. Chem Res Toxicol 9: 836-844, 1996.
5. Beisswenger PJ, Drummond KS, Nelson RG, Howell SK, Szwergold BS, Mauer M. Susceptibility to diabetic nephropathy is related to dicarbonyl and oxidative stress. Diabetes 54: 3274-3281, 2005.
6. Beisswenger PJ, Howell SK, Nelson RG, Mauer M, Szwergold BS. Alpha-oxoaldehyde metabolism and diabetic complications. Biochem Soc Trans 31: 1358-1363, 2003.
7. Beisswenger PJ, Howell SK, Smith K, Szwergold BS. Glyceraldehyde- 3-phosphate dehydrogenase activity as an independent modifier of meth- ylglyoxal levels in diabetes. Biochim Biophys Acta 1637: 98-106, 2003.
8. Bkaily G, Nader M, Avedanian L, Jacques D, Perrault C, Abdel- Samad D, D'Orleans-Juste P, Gobeil F, Hazzouri KM. Immunofluorescence revealed the presence of NHE-1 in the nuclear membranes of rat cardiomyocytes and isolated nuclei of human, rabbit, and rat aortic and liver tissues. Can J Physiol Pharmacol 82: 805-811, 2004.
9. Boulton AJ, Vinik AI, Arezzo JC, Bril V, Feldman EL, Freeman R, Malik RA, Maser RE, Sosenko JM, Ziegler D; American Diabetes Association. Diabetic neuropathies: a statement by the American Diabetes Association. Diabetes Care 28: 956-962, 2005.
10. Chen S, Khan ZA, Karmazyn M, Chakrabarti S. Role of endothelin-1, sodium exchanger-1 and mitogen activated protein kinase (MAPK) activation in glucose-induced cardiomyocte hypertrophy. Diabetes Metab Res Rev 23: 356-367, 2007.
11. Cheng C, Zochodne DW. Sensory neurons with activated caspase-3 survive long-term experimental diabetes. Diabetes 52: 2363-2371, 2003.
12. Coppey LJ, Davidson EP, Dunlap JA, Lund DD, Yorek MA. Slowing of motor nerve conduction velocity in streptozotocin-induced diabetic rats is preceded by impaired vasodilation in arterioles that overlie the sciatic nerve. Int J Exp Diabetes Res 1: 131-143, 2000.
13. Coppey LJ, Davidson EP, Rinehart TW, Gellett JS, Oltman CL, Lund DD, Yorek MA. ACE inhibition or angiotensin II receptor antagonist attenuates diabetic neuropathy in streptozotocin-induced diabetic rats. Diabetes 55: 341-348, 2006.
14. Coppey LJ, Gellett JS, Davidson EP, Dunlap JA, Lund DD, Salvemini D, Yorek MA. Effect of M40403 treatment of diabetic rats on endoneurial blood flow, motor nerve conduction velocity and vascular function of epineurial arterioles of the sciatic nerve. Br J Pharmacol 134: 21-29, 2001.
15. Coppey LJ, Gellett JS, Davidson EP, Dunlap JA, Lund DD, Yorek MA. Effect of antioxidant treatment of streptozotocin-induced diabetic rats on endoneurial blood flow, motor nerve conduction velocity, and vascular reactivity of epineurial arterioles of the sciatic nerve. Diabetes 50: 1927-1937, 2001.
16. Cowell RM, Russell JW. Nitrosative injury and antioxidant therapy in the management of diabetic neuropathy. J Investig Med 52: 33-44, 2004.
17. Cukiernik M, Hileeto D, Downey D, Evans T, Khan ZA, Karmazyn M, Chakrabarti S. The role of the sodium hydrogen exchanger-1 in mediating diabetes-induced changes in the retina. Diabetes Metab Res Rev 20: 61-71, 2004.
18. Darmellah A, Baetz D, Prunier F, Tamareille S, Rucker-Martin C, Feuvray D. Enhanced activity of the myocardial Na+/H+ exchanger contributes to left ventricular hypertrophy in the Goto-Kakizaki rat model of type 2 diabetes: critical role of Akt. Diabetologia 50: 1335-1344, 2007.
19. Davidson EP, Kleinschmidt TL, Oltman CL, Lund DD, Yorek MA. Treatment of streptozotocin-induced diabetic rats with AVE7688, a vaso- peptidase inhibitor: effect on vascular and neural disease. Diabetes 56: 355-362, 2007.
20. DeFronzo RA. Pharmacologic therapy for type 2 diabetes mellitus. Ann Intern Med 133: 73-74, 2000.
21. Dilley RJ, Farrelly CA, Allen TJ, Jandeleit-Dahm K, Cooper ME, Morahan G, Little PJ. Diabetes induces Na/H exchange activity and hypertrophy of rat mesenteric but not basilar arteries. Diabetes Res Clin Pract 70: 201-208, 2005.
22. Ding Y, Kantarci A, Hasturk H, Trackman PC, Malabanan A, Van Dyke TF. Activation of RAGE induces elevated O2-generation by mononuclear phagocytes in diabetes. J Leukoc Biol 81: 520-527, 2007.
23. Drel VR, Pacher P, Vareniuk I, Pavlov I, Ilnytska O, Valeriy V, Lyzogubov VV, Tibrewala J, Groves JT, Obrosova IG. A peroxynitrite decomposition catalyst counteracts sensory neuropathy in streptozotocin- diabetic mice. Eur J Pharmacol 569: 48-58, 2007.
24. Dyck JR, Lopaschuk GD. Glucose metabolism, H+ production and Na+/H+-exchanger mRNA levels in ischemic hearts from diabetic rats. Mol Cell Biochem 180: 85-93, 1998.
25. Erecinska M, Thoresen M, Silver IA. Effects of hypothermia on energy metabolism in Mammalian central nervous system. J Cereb Blood Flow Metab 23: 513-530, 2003.
26. Farmer KL, Li C, Dobrowsky RT. Diabetic peripheral neuropathy: should a chaperone accompany our therapeutic approach? Pharmacol Rev 64: 880-900, 2012.
27. Fern R, Ransom BR. Ischemic injury of optic nerve axons: the nuts and bolts. Clin Neurosci 4: 246-250, 1997.
28. Fleming T, Cuny J, Nawroth G, Djuric Z, Humpert PM, Zeier M, Bierhaus A, Nawroth PP. Is diabetes an acquired disorder of reactive glucose metabolites and their intermediates? Diabetologia 55: 1151-1155, 2012.
29. Forbes JM, Cooper ME. Mechanisms of diabetic complications. Physiol Rev 93: 137-188, 2013.
30. Ford P, Rivarola V, Kierbel A, Chara O, Blot-Chabaud M, Farman N, Parisi M, Capurro C. Differential role of Na+/H+ exchange isoforms NHE-1 and NHE-2 in a rat cortical collecting duct cell line. J Membr Biol 190: 117-125, 2002.
31. Hannan KM, Little PJ. Mechanisms regulating the vascular smooth muscle Na/H exchanger (NHE-1) in diabetes. Biochem Cell Biol 76: 751-759, 1998.
32. Karmazyn M, Sawyer M, Fliegel L. The Na(+)/H(+) exchanger: a target for cardiac therapeutic intervention. Curr Drug Targets Cardiovasc Haematol Disord 5: 323-335, 2005.
33. Khan I, Thomas N, Haridas S. Expression and sub cellular localization of the sodium hydrogen exchanger isoform-1 in rat tissues: a possible functional relevance. Mol Cell Biochem 219: 153-161, 2001.
34. Lang KS, Mueller MM, Tanneur V, Wallisch S, Fedorenko O, Pal- mada M, Lang F, Broer S, Heilig CW, Schleicher E, Weigert C. Regulation of cytosolic pH and lactic acid release in mesangial cells overexpressing GLUT1. Kidney Int 64: 1338-1347, 2003.
35. Lewis EJ, Hunsicker LG, Bain RP, Rohde RD. The effect of angioten- sin-converting-enzyme inhibition on diabetic nephropathy. The Collaborative Study Group. N Engl J Med 329: 1456-1462, 1993.
36. Lewis EJ, Hunsicker LG, Clarke WR, Berl T, Pohl MA, Lewis JB, Ritz E, Atkins RC, Rohde R, Raz I. Renoprotective effect of the angiotensin-receptor antagonist irbesartan in patients with nephropathy due to type 2 diabetes. N Engl J Med 345: 851-860, 2001.
37. Lupachyk S, Stavniichuk R, Komissarenko JI, Drel VR, Obrosov AA, El-Remessy AB, Pacher P, Obrosova IG. Na+/H+-exchanger-1 inhibition counteracts diabetic cataract formation and retinal oxidative-nitra- tive stress and apoptosis. Int J Mol Med 29: 989-998, 2012.
38. Obrosova IG. Update on the pathogenesis of diabetic neuropathy. Curr Diab Rep 3: 439-445, 2003.
39. Obrosova IG. Diabetic painful and insensate neuropathy: pathogenesis and potential treatments. Neurotherapeutics 6: 638-647, 2009.
40. Obrosova IG, Drel VR, Pacher P, Ilnytska O, Wang ZQ, Stevens MJ, Yorek MA. Oxidative-nitrosative stress and poly(ADp-ribose) polymerase (PARP) activation in experimental diabetic neuropathy: the relation is revisited. Diabetes 54: 3435-3441, 2005.
41. Obrosova IG, Fathallah L, Stevens MJ. Taurine counteracts oxidative stress and nerve growth factor deficit in early experimental diabetic neuropathy. Exp Neurol 172: 211-219, 2001.
42. Obrosova IG, Pacher P, Szabo C, Zsengeller Z, Hirooka H, Stevens MJ, Yorek MA. Aldose reductase inhibition counteracts oxidative-nitro- sative stress and poly(ADP-Ribose) polymerase activation in tissue sites for diabetes complications. Diabetes 54: 234-242, 2005.
43. Obrosova IG, Van Huysen C, Fathallah L, Cao X, Stevens MJ, Greene DA. Evaluation of a1-adrenoceptor antagonist on nerve function, metabolism and antioxidative defense. FASEB J 14: 1548-1558, 2000.
44. Oltman CL, Coppey LJ, Gellett JS, Davidson EP, Lund DD, Yorek MA. Progression of vascular and neural dysfunction in sciatic nerves of Zucker diabetic fatty and Zucker rats. Am J Physiol Endocrinol Metab 289: E113-E122, 2005.
45. Oltman CL, Davidson EP, Coppey LJ, Kleinschmidt TL, Lund DD, Yorek MA. Attenuation of vascular/neural dysfunction in Zucker rats treated with enalapril or rosuvastatin. Obesity (Silver Spring) 16: 82-89, 2008.
46. Peak M, al-Habori M, Agius L. Regulation of glycogen synthesis and glycolysis by insulin, pH and cell volume. Interactions between swelling and alkalinization in mediating the effects of insulin. Biochem J 282: 797-805, 1992.
47. Pryor WA, Squadrito GL. The chemistry of peroxynitrite: a product from the reaction of nitric oxide with superoxide. Am J Physiol Lung Cell Mol Physiol 268: L699-L722, 1995.
48. Putney LK, Denker SP, Barber DL. The changing face of the Na+/H+ exchager, NHE1: structure, regulation, and cellular actions. Annu Rev Pharmacol Toxicol 42: 527-552, 2002.
49. Reshkin SJ, Bellizzi A, Caldeira S, Albarani V, Malanchi I, Poignee M, Alunni-Fabbroni M, Casavola V, Tommasino M. Na+/H+ exchanger-dependent intracellular alkalinization is an early event in malignant transformation and plays an essential role in the development of subsequent transformation-associated phenotypes. FASEB J 14: 2185-2197, 2000.
50. Rieder CV, Fliegel L. Transcriptional regulation of Na+/H+ exchanger expression in the intact mouse. Mol Cell Biochem 243: 87-95, 2005.
51. Stavniichuk R, Drel VR, Shevalye H, Maksimchyk Y, Kuchmerovska TM, Nadler JL, Obrosova IG. Baicalein alleviates diabetic peripheral neuropathy through inhibition of oxidative-nitrosative stress and p38 MAPK activation. Exp Neurol 230: 106-113, 2011.
52. Stevens MJ, Zhang W, Li F, Sima AA. C-peptide corrects endoneurial blood flow but not oxidative stress in type 1 BB/Wor rats. Am J Physiol Endocrinol Metab 287: E497-E505, 2004.
53. Sun YM, Su Y, Li J, Tian Y, Wang LF. Role of the Na(+)/H(+) exchanger on the development of diabetes mellitus and its chronic complications. Biochem Biophys Res Commun 427: 229-231, 2012.
54. Tahrani AA, Askwith T, Stevens MJ. Emerging drugs for diabetic neuropathy. Expert Opin Emerg Drugs 15: 661-683, 2010.
55. Terata K, Coppey LJ, Davidson EP, Dunlap JA, Gutterman DD, Yorek MA. Acetylcholine-induced arteriolar dilation is reduced in strep- tozotocin-induced diabetic rats with motor nerve dysfunction. Br J Pharmacol 128: 837-843, 1999.
56. No authors listed. The effect of intensive diabetes therapy on the development and progression of neuropathy. The Diabetes Control and Complications Trial Research Group. Ann Int Med 122: 561-568, 1995.
57. Vial G, Dubouchaud H, Couturier K, Lanson M, Leverve X, Demai- son L. Na+/H+ exchange inhibition with cariporide prevents alterations of coronary endothelial function in streptozotocin-induced diabetes. Mol Cell Biochem 310: 93-102, 2008.
58. Wang S, Peng Q, Zhang J, Liu L. Na+/H+ exchanger is required for hyperglycaemia-induced endothelial dysfunction via calcium-dependent calpain. Cariovasc Res 80: 255-262, 2008.
59. Wang SX, Xiong XM, Song T, Liu LY. Protective effects of cariporide on endothelial dysfunction induced by high glucose. Acta Pharmacol Sin 26: 329-333, 2005.
60. Wattanapitayakul SK, Weinstein DM, Holycross BJ, Bauer JA. Endothelial dysfunction and peroxynitrite formation are early events in angiotensin-induced cardiovascular disorders. FASEB J 14: 271-278, 2000.
61. Xiong Y, Rabchevsky AG, Hall ED. Role of peroxynitrite in secondary oxidative damage after spinal cord injury. J Neurochem 100: 639-649, 2007.
62. Yin QQ, Dong CF, Dong SQ, Dong XL, Hong Y, Hou XY, Luo DZ, Pei JJ, Liu XP. AGEs induce cell death via oxidative and endoplasmic reticulum stresses in both human SH-SY5Y neuroblastoma cells and rat cortical neurons. Cell Mol Neurobiol 32: 1299-1309, 2012.
63. Yorek MA. The potential role of angiotensin converting enzyme and vasopeptidase inhibitors in the treatment of diabetic neuropathy. Curr Drug Targets 9: 77-84, 2008.
64. Young W. H2 clearance measurement of blood flow: a review of technique and polarographic principles. Stroke 11: 552-564, 1980.
65. Zhao P, Ma MC, Qian H, Xia Y. Down-regulation of delta-opioid receptors in Na+/H+ exchanger 1 null mutant mouse brain with epilepsy. Neurosci Res 53: 442-446, 2005.