Seminars in Nephrology
Volume 24, Issue 4 , Pages 333-344 , July 2004

Role of nitric oxide in diabetic nephropathy

  • Sharma S Prabhakar

      Affiliations

    • Department of Internal Medicine-Nephrology, Texas Tech University Health Sciences Center, Lubbock, TX, USA
    • Corresponding Author InformationAddress reprint requests to: Sharma Prabhakar, MD, Associate Professor of Medicine, Department of Internal Medicine-Nephrology, 3601 4th St, 4C-178, Texas Tech University Health Sciences Center, Lubbock TX 79430 USA

References 

  1. Baylis C, Mitruka B, Deng A. Chronic blockade of nitric oxide synthesis in the rat produces systemic hypertension and glomerular damage. J Clin Invest. 1992;90:278–281
  2. Narita I, Border WA, Ketteler M, et al.  L-arginine may mediate the therapeutic effects of low protein diets. Proc Natl Acad Sci U S A. 1995;9:4552–4556
  3. Wardle EN. How does hyperglycemia predispose to diabetic nephropathy?. QJM. 1997;90:493
  4. Verbeke P, Perichon M, Friguet B, et al.  Inhibition of nitric oxide synthase activity by early and advanced glycation end products in cultured rabbit proximal tubular epithelial cells. Biochim Biophys Acta. 2000;1502:481–494
  5. Du XL, Edelstein D, Dimmeler S, et al.  Hyperglycemia inhibits endothelial nitric oxide synthase activity by posttranslational modification at the Akt site. J Clin Invest. 2001;108:1341–1348
  6. Craven PA, Studer RK, DeRubertis FR. Impaired nitric oxide release by glomeruli from diabetic rats. Metabolism. 1995;44:695–698
  7. Craven PA, Studer RK, DeRubertis FR. Impaired nitric oxide-dependent cyclic guanosine monophosphate generation in glomeruli from diabetic rats. Evidence for protein kinase C-mediated suppression of cholinergic response. J Clin Invest. 1994;93:311–320
  8. Dai FX, Diederich A, Skopec J, et al.  Diabetes-induced endothelial dysfunction in streptozotocin-treated rats (Role of prostaglandin endoperoxides and free radicals). J Am Soc Nephrol. 1993;4:1327–1336
  9. Schnackenberg CG, Wilcox CS. The SOD mimetic tempol restores vasodilation in afferent arterioles of experimental diabetes. Kidney Int. 2001;59:1859–1864
  10. Ohishi K, Carmines PK. Superoxide dismutase restores the influence of nitric oxide on renal arterioles in diabetes mellitus. J Am Soc Nephrol. 1995;5:1559–1566
  11. Trachtman H, Futterweit S, Crimmins DL. High glucose inhibits nitric oxide production in cultured rat mesangial cells. J Am Soc Nephrol. 1997;8:1276–1282
  12. Prabhakar SS. Tetrahydrobiopterin reverses the inhibition of nitric oxide by high glucose in cultured murine mesangial cells. Am J Physiol. 2001;281:F179–F188
  13. Sharma K, Danoff TM, DePiero A, et al.  Enhanced expression of inducible nitric oxide synthase in murine macrophages and glomerular mesangial cells by elevated glucose levels (Possible mediation via protein kinase C). Biochem Biophys Res Commun. 1995;6:80–88
  14. Noh H, Ha H, Yu MR, et al.  High glucose increases inducible NO production in cultured rat mesangial cells. Possible role in fibronectin production. Nephron. 2002;90:78–85
  15. Hink U, Li H, Mollnau H, et al.  Mechanisms underlying endothelial dysfunction in diabetes mellitus. Circ Res. 2001;88:E14–E22
  16. Brodsky SV, Morrishow AM, Dharia N, et al.  Glucose scavenging of nitric oxide. Am J Physiol. 2001;280:F480–F486
  17. Trachtman H, Koss I, Bogart M, et al.  High glucose enhances growth factor-stimulated nitric oxide production by cultured rat mesangial cells. Res Commun Mol Pathol Pharmocol. 1998;100:213–225
  18. Trachtman H, Futterweit S, Franki N, et al.  Effect of vascular endothelial growth factor on nitric oxide production by cultured rat mesangial cells. Biochem Biophys Res Commun. 1998;245:443–446
  19. Kasai N, Sugimoto K, Horiba N, et al.  Effect of D’glucose on nitric oxide release from glomerular endothelial cells. Diabetes Metab Rev. 2001;17:217–222
  20. Amore A, Cirina P, Mitola S, et al.  Nonenzymatically glycated albumin (Amadori adducts) enhances nitric oxide synthase activity and gene expression in endothelial cells. Kidney Int. 1997;51:27–35
  21. Sugimoto H, Shikata K, Matsuda M, et al.  Increased expression of endothelial cell nitric oxide synthase (ecNOS) in afferent and glomerular endothelial cells is involved in glomerular hyperfiltration of diabetic nephropathy. Diabetologia. 1998;41:1426–1434
  22. Wautier JL, Guillausseau PJ. Advanced glycation end products, their receptors and diabetic angiopathy. Diabetes Metab. 2001;27:535–542
  23. Rojas A, Romay S, Gonzales D, et al.  Regulation of eNOS expression by albumin derived advanced glycation end-products. Circ Res. 2000;86:E50–E54
  24. Goligorsky MS, Chen J, Brodsky S, et al.  Workshop: Endothelial cell dysfunction leading to diabetic nephropathy: Focus on nitric oxide. Hypertension. 2001;37:744–748
  25. Chakravarthy U, Hayes RG, Stitt AW, et al.  Constitutive NOS expression in retinalvascular endothelial cells is suppressed by high glucose and advanced glycation end-products. Diabetes. 1998;47:945–952
  26. Bucala R, Tracey KJ, Cerami A. Advanced glycosylation products quench nitric oxide and mediate defective endothelium-dependent vasodilatation in experimental diabetes. J Clin Invest. 1991;87:432–438
  27. Hogan M, Cerami A, Bucala R. Advanced glycosylation end products block the antiproliferative effect of nitric oxide. Role in the vascular and renal complications of diabetes mellitus. J Clin Invest. 1992;90:1110–1115
  28. Scivittaro V, Ganz MB, Weiss MF. AGEs induce oxidative stress and activate protein kinase C-beta(II) in neonatal mesangial cells. Am J Physiol. 2000;278:F676–F683
  29. Choi KC, Kim NH, An MR, et al.  Alterations of intrarenal renin-angiotensin and nitric oxide systems in streptozotocin-induced diabetic rats. Kidney Int. 1997;52(suppl 60):S23–S27
  30. De Vriese AS, Stoenoiu MS, Elger M, et al.  Diabetes-induced microvascular dysfunction in the hydronephrotic kidney (Role of nitric oxide). Kidney Int. 2001;60:202–210
  31. Veelken R, Hilgers KF, Hartner A, et al.  Nitric oxide synthase isoforms and glomerular hyperfiltration in early diabetic nephropathy. J Am Soc Nephrol. 2000;11:71–79
  32. Ishii N, Patel KP, Lane PH, et al.  Nitric oxide synthesis and oxidative stress in the renal cortex of rats with diabetes mellitus. J Am Soc Nephrol. 2001;12:1630–1639
  33. Omer S, Shan J, Varma DR, et al.  Augmentation of diabetes-associated renal hyperfiltration and nitric oxide production by pregnancy in rats. J Endocrinol. 1999;161:15–23
  34. Keynan S, Hirshberg B, Levin-Iaina N, et al.  Renal nitric oxide production during the early phase of experimental diabetes mellitus. Kidney Int. 2000;58:740–747
  35. Wilcox CS, Welch WJ, Murad F, et al.  Nitric oxide synthase in macula densa regulates glomerular capillary pressure. Proc Natl Acad Sci U S A. 1992;89:11993–11997
  36. Sugimoto H, Shikata K, Wada J, et al.  Advanced glycation end products-cytokine-nitric oxide sequence pathway in the development of 1diabetic nephropathy (Aminoguanidine ameliorates the overexpression of tumour necrosis factor-alpha and inducible nitric oxide synthase in diabetic rat glomeruli). Diabetologia. 1999;42:878–886
  37. Schwartz D, Schwartz IF, Blantz RC. An analysis of renal nitric oxide contribution to hyperfiltration in diabetic rats. J Lab Clin Med. 2001;137:107–114
  38. Komers R, Oyama TT, Chapman JG, et al.  Effects of systemic inhibition of neuronal nitric oxide synthase in diabetic rats. Hypertension. 2000;34:655–661
  39. Komers R, Lindsley JN, Oyama TT, et al.  Role of neuronal nitric oxide synthase (NOS1) in the pathogenesis of renal hemodynamic changes in diabetes. Am J Physiol. 2000;279:F573–F583
  40. Ito A, Uriu K, Inada Y, et al.  Inhibition of neuronal nitric oxide synthase ameliorates renal hyperfiltration in streptozotocin-induced diabetic rat. J Lab Clin Med. 2001;138:177–185
  41. Komers R, Anderson S. Paradoxes of nitric oxide in the diabetic kidney. Am J Physiol. 2003;284:F1121–F1137
  42. Cosenzi A, Bernobich E, Bonavita M, et al.  Role of nitric oxide in the early renal changes induced by high fructose diet in rats. Kidney Blood Press Res. 2002;25:363–369
  43. Soulis T, Cooper ME, Sastra S, et al.  Relative contributions of advanced glycation and nitric oxide synthase inhibition to aminoguanidine-mediated renoprotection in diabetic rats. Diabetologia. 1997;40:1141–1151
  44. Nishio E, Watanabe Y. Glucose-induced down-regulation of NO production and inducible NOS expression in cultured rat aortic vascular smooth muscle cells (Role of protein kinase C). Biochem Biophys Res Commun. 1996;24:857–863
  45. Guo X, Chen LW, Liu WL, et al.  High glucose inhibits expression of inducible and constitutive nitric oxide synthase in bovine aortic endothelial cells. Acta Pharmacol Sin. 2000;21:325–328
  46. Begum N, Ragolia L. High glucose and insulin inhibit VSMC MKP-1 expression by blocking iNOS via p38 MAPK inactivation. Am J Physiol. 2000;278:C81–C91
  47. Trachtman H, Futterweit S, Pine E, et al.  Chronic diabetic nephropathy (Role of inducible nitric oxide synthase). Pediatric Nephrol. 2002;17:20–29
  48. King AJ, Troy JL, Anderson S, et al.  Nitric oxide (A potential mediator of amino acid-induced renal hyperemia and hyperfiltration). J Am Soc Nephrol. 1991;1:1271–1277
  49. Tolins JP, Shultz PJ, Raij L, et al.  Abnormal renal hemodynamic response to reduced renal perfusion pressure in diabetic rats (Role of NO). Am J Physiol. 1993;265:F886–F895
  50. Komers R, Allen TJ, Cooper ME. Role of endothelium-derived nitric oxide in the pathogenesis of the renal hemodynamic changes of experimental diabetes. Diabetes. 1994;43:1190–1197
  51. Bank N, Aynedjian HS. Role of EDRF (nitric oxide) in diabetic renal hyperfiltration. Kidney Int. 1993;43:1306–1312
  52. Mattar AL, Fujihara CK, Ribeiro MO, et al.  Renal effects of acute and chronic nitric oxide inhibition in experimental diabetes. Nephron. 1996;74:136–143
  53. Goor Y, Peer G, Iaina A, et al.  Nitric oxide in ischaemic acute renal failure of streptozotocin diabetic rats. Diabetologia. 1996;39:1036–1040
  54. Kiff RJ, Gardiner SM, Compton AM, et al.  The effects of endothelin-1 and NG-nitro-L-arginine methyl ester on regional haemodynamics in conscious rats with streptozotocin-induced diabetes mellitus. Br J Pharmacol. 1991;103:1321–1326
  55. Pflueger AC, Larson TS, Hagl S, et al.  Role of nitric oxide in intrarenal hemodynamics in experimental diabetes mellitus in rats. Am J Physiol. 1999;277:R725–R733
  56. Pflueger AC, Larson TS, Hagl S, et al.  Role of nitric oxide in intrarenal hemodynamics in experimental diabetes mellitus in rats. Am J Physiol. 1999;277:R725–R733
  57. Wang YX, Brooks DP, Edwards RM. Attenuated glomerular cGMP production and renal vasodilation in streptozotocin-induced diabetic rats. Am J Physiol. 1993;264:R952–R956
  58. Craven PA, DeRubertis FR, Melhem M. Nitric oxide in diabetic nephropathy. Kidney Int. 1997;52(suppl 60):S46–S53
  59. Wessels J, Peake P, Pussell BA, et al.  Nitric oxide synthase inhibition in a spontaneously hypertensive rat model of diabetic nephropathy. Clin Exp Pharmacol Physiol. 1997;24:451–453
  60. Reyes AA, Karl IE, Kissane J, et al.  L-arginine administration prevents glomerular hyperfiltration and decreases proteinuria in diabetic rats. J Am Soc Nephrol. 1993;4:1039–1045
  61. Lubec B, Aufricht C, Amann G, et al.  Arginine reduces kidney collagen accumulation, cross-linking, lipid peroxidation, glycoxidation, kidney weight and albuminuria in the diabetic kk mouse. Nephron. 1997;75:213–218
  62. Fujihara CK, De-Nucci G, Zatz R. Chronic nitric oxide synthase inhibition aggravates glomerular injury in rats with subtotal nephrectomy. J Am Soc Nephrol. 1995;5:1498–1507
  63. Klahr S. Can L-arginine manipulation reduce renal disease?. Semin Nephrol. 1999;19:304–309
  64. Hiragushi K, Sugimoto H, Shikata K, et al.  Nitric oxide system is involved in glomerular hyperfiltration in Japanese normo- and micro-albuminuric patients with type 2 diabetes. Diabetes Res Clin Pract. 2001;53:149–159
  65. Dalla Vestra M, Sacerdoti D, Bombonato G, et al.  Nitric oxide modulation of renal and cardiac hemodynamics in type 2 diabetes. Eur J Endocrinol. 2002;146:687–694
  66. Earle KA, Mehrotra S, Dalton RN, et al.  Defective nitric oxide production and functional renal reserve in patients with type 2 diabetes who have microalbuminuria of African and Asian compared with white origin. J Am Soc Nephrol. 2001;12:2125–2130
  67. Maejima K, Nakano S, Himeno M, et al.  Increased basal levels of plasma nitric oxide in type 2 diabetic subjects. Relationship to microvascular complications. J Diabetes Complications. 2001;15:135–143
  68. Yamada K, Nakano H, Nakayama M, et al.  Endothelium-dependent relaxation in peripheral vasculature and kidney of non-insulin-dependent diabetes mellitus. J Diabetes Complications. 1995;9:203–207
  69. Frauchiger B, Nussbaumer P, Hugentobler M, et al.  Duplex sonographic registration of age and diabetes-related loss of renal vasodilatory response to nitroglycerine. Nephrol Dial Transplant. 2000;15:827–832
  70. Thuraisingham RC, Nott CA, Dodd SM, et al.  Increased nitrotyrosine staining in kidneys from patients with diabetic nephropathy. Kidney Int. 2000;57:1968–1972
  71. Asakimori Y, Yorioka N, Yamamoto I, et al.  Endothelial nitric oxide synthase intron 4 polymorphism influences the progression of renal disease. Nephron. 2001;89:219–223
  72. Negebauer S, Baba T, Watanabe T. Association of the nitric oxide synthase gene polymorphism with an increased risk for progression to diabetic nephropathy in type 2 diabetes. Diabetes. 2000;49:500–503
  73. Wang Y, Kikuchi S, Suzuki H, et al.  Endothelial nitric oxide synthase gene polymorphism in intron 4 affects the progression of renal failure in non-diabetic renal diseases. Nephrol Dial Transplant. 1999;14:2898–2902
  74. Zhang C, Mayeux P. Angiotensin II signaling activities the NO-cGMP pathway in rat proximal tubules. Life Sci. 1998;63:75–80
  75. Moreno C, Lopez A, Llinas MT, et al.  Changes in NOS activity and protein expression during acute and prolonged ANG II administration. Am J Physiol. 2002;282:R31–R37
  76. Hennington B, Zhang H, Miller M, et al.  Angiotensin II stimulates synthesis of endothelial nitric oxide synthase. Hypertension. 1998;31:283–288
  77. Zou A, Wu F, Cowley A. Protective effect of angiotensin II induced increase in nitric oxide in renal medullary circulation. Hypertension. 1998;31:271–276
  78. Thorup C, Kornfeld M, Winaver J, et al.  Angiotensin II stimulates nitric oxide release in isolated perfused renal arteries. Pflugers Arch. 1998;435:432–434
  79. Kihara M, Yabana M, Toya Y, et al.  Angiotensin II inhibits interleukin-1β induced nitric oxide production in cultured rat mesangial cells. Kidney Int. 1999;55:1277–1283
  80. Wolf G, Ziyadeh F, Schroeder R, et al.  Angiotensin II inhibits inducible nitric oxide synthase in tubular MCT cells by a posttranscriptional mechanism. J Am Soc Nephrol. 1997;8:551–557
  81. Nakayama I, Kawahara Y, Okuda M, et al.  Angiotensin II type 1 receptor-mediated inhibition of cytokine-stimulated inducible nitric oxide synthase expression in vascular smooth muscle cells. Blood Press. 1994;5(Suppl):32–37
  82. Onozato ML, Tojo A, Fujita T, et al.  Oxidative stress and nitric oxide synthase in rat diabetic nephropathy (Effects of ACEI and ARB). Kidney Int. 2002;61:186–194
  83. Forbes JM, Cooper ME, Thallas V, et al.  Reduction of the accumulation of advanced glycation end products by ACE inhibition in experimental diabetic nephropathy. Diabetes. 2002;51:3274–3282
  84. Schmetterer L, Muller M, Fasching P, et al.  Renal and ocular hemodynamic effects of insulin. Diabetes. 1997;46:1868–1874
  85. Komers R, Pelikanova T, Kazdova L. Effect of hyperinsulinemia on renal function and nitrate/nitrite excretion in healthy subjects. Clin Exp Pharmacol Physiol. 1999;26:336–341
  86. Prabhakar SS. Insulin stimulates inducible nitric oxide synthesis in normal human mesangial cells by augmenting cellular uptake of L-arginine. Nephrol Dial Transplant. 2003;18:49
  87. Smukler SR, Tang L, Wheeler MB, et al.  Exogenous nitric oxide and endogenous glucose-stimulated beta-cell nitric oxide augment insulin release. Diabetes. 2002;51:3450–3460
  88. Prabhakar SS. Role of nitric oxide in the regulation of insulin secretion by pancreatic islet cells. J Am Soc Nephrol. 2003;14:323A
  89. Derubertis FR, Craven PA. Activation of protein kinase C in glomerular cells in diabetes. Mechanisms and potential links to the pathogenesis of diabetic glomerulopathy. Diabetes. 1994;43:1–8
  90. McCarty MF. A central role for protein kinase C overactivity in diabetic glomerulosclerosis (Implications for prevention with antioxidants, fish oil, and ACE inhibitors). Med Hypotheses. 1998;50:155–165
  91. Michell BJ, Chen ZP, Tiganis T, et al.  Coordinated control of endothelial nitric-oxide synthase phosphorylation by protein kinase C and the cAMP-dependent protein kinase. J Biol Chem. 2001;25:17625–17628
  92. Sharma K, Ziayadh FN, Alzahabi B, et al.  Increased renal production of TGF-beta 1 in patients with type II diabetes mellitus. Diabetes. 1997;46:854–859
  93. Chen S, Jim B, Ziyadeh FN. Diabetic nephropathy and transforming growth factor-beta (Transforming our view of glomerulosclerosis and fibrosis build-up). Semin Nephrol. 2003;23:532–543
  94. Kagami S, Border WA, Miller DE, et al.  Angiotensin II stimulates extracellular matrix protein synthesis through induction of TGF-beta expression in rat glomerular mesangial cells. J Clin Invest. 1994;93:2431–2437
  95. Wang S, Shiva S, Poczatek MH, et al.  Nitric oxide and cGMP-dependent protein kinase regulation of glucose-mediated thrombospondin 1-dependent transforming growth factor-beta activation in mesangial cells. J Biol Chem. 2002;277:9880–9888
  96. Agarwal R, Siva S, Dunn SR, et al.  Add-on angiotensin II receptor blockade lowers urinary transforming growth factor-beta levels. Am J Kidney Dis. 2002;39:486–492
  97. Asakimori Y, Yorioka N, Taniguchi Y, et al.  T)-786)->C polymorphism of the endothelial nitric oxide synthase gene influences the progression of renal disease. Nephron. 2002;91:747–751
  98. Suzuki H, Nagase S, Kikuchi S, et al.  Association of a missense Glu298Asp mutation of the endothelial nitric oxide synthase gene with end stage renal disease. Clin Chem. 2000;46:1858–1860
  99. Cai H, Wang X, Colagiuri S, et al.  A common Glu298->Asp (894G->T) mutation at exon 7 of the endothelial nitric oxide synthase gene and vascular complications in type 2 diabetes. Diabetes Care. 1998;21:2195–2196
  100. Noiri E, Satoh H, Taguchi J, et al.  Association of eNOS Glu298Asp polymorphism with end stage renal disease. Hypertension. 2002;40:535–540
  101. Li C, Dong Y, Lu W. The association between polymorphism of endothelial nitric oxide synthase gene and diabetic nephropathy. Zhonghua Nei Ke Za Zhi. 2001;40:729–732
  102. Freedman BI, Yu H, Anderson PJ, et al.  Genetic analysis of nitric oxide and endothelin in end-stage renal disease. Nephrol Dial Transplant. 2000;15:1794–1800
  103. Fujita H, Narita T, Meguro H, et al.  Lack of association between an ecNOS gene polymorphism and diabetic nephropathy in type 2 diabetic patients with proliferative diabetic retinopathy. Horm Metab Res. 2000;32:80–83
  104. Shimizu T, Onuma T, Kawamori R, et al.  Endothelial nitric oxide synthase gene and the development of diabetic nephropathy. Diabetes Res Clin Pract. 2002;58:179–185
  105. Rippin JD, Patel A, Belyaev ND, et al.  Nitric oxide synthase gene polymorphisms and diabetic nephropathy. Diabetologia. 2003;46:426–428
  106. Zanchi A, Moczulski DK, Hanna LS, et al.  Risk of advanced diabetic nephropathy in type 1 diabetes is associated with endothelial nitric oxide synthase gene polymorphism. Kidney Int. 2000;57:405–413
  107. Johannesen J, Tarnow L, Parving HH, et al.  CCTTT-repeat polymorphism in the human NOS2- promoter confers low risk of diabetic nephropathy in type 1 diabetic patients. Diabetes Care. 2000;23:560–562

PII: S0270-9295(04)00053-1

doi: 10.1016/j.semnephrol.2004.04.005

Seminars in Nephrology
Volume 24, Issue 4 , Pages 333-344 , July 2004