Paradoxes of nitric oxide in the diabetic kidney

American Journal of Physiology - Renal Physiology

Volumn 284, Issue 6 53-6, 2003, Pages

  Komers, Radko ^a,c,d   Anderson, Sharon ^a,b  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b PORTLAND VA MEDICAL CENTER   (United States)

^c INSTITUTE FOR CLINICAL AND EXPERIMENTAL MEDICINE   (Czech Republic)

^d OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Diabetic nephropathy; Endothelial function; Reactive oxygen species; Renal function; Signal transduction

Indexed keywords

GLUCOSE; INSULIN; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; REACTIVE OXYGEN METABOLITE;

CORRELATION ANALYSIS; DIABETES MELLITUS; DIABETIC NEPHROPATHY; DISEASE COURSE; ENDOTHELIUM; ENZYME ACTIVATION; ENZYME ACTIVITY; GLUCOSE BLOOD LEVEL; GLUCOSE METABOLISM; GLYCATION; HEMODYNAMICS; HUMAN; KIDNEY FUNCTION; METABOLIC REGULATION; NONHUMAN; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION;

EID: 0037609623     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00265.2002     Document Type: Review

References (163)

1. Ahn KY, Mohaupt MG, Madsen KM, and Kone BC. In situ hybridization localization of mRNA encoding inducible nitric oxide synthase in rat kidney. Am J Physiol Renal Fluid Electrolyte Physiol 267: F748-F757, 1994.
2. Al-Douahji M, Brugarolas J, Brown PA, Stehman-Breen CO, Alpers CE, and Shankland SJ. The cyclin kinase inhibitor p21WAF1/CIP1 is required for glomerular hypertrophy in experimental diabetic nephropathy. Kidney Int 56: 1691-1699, 1999.
3. Alabadi JA, Miranda FJ, Llorens S, Ruiz de Apodaca RF, Centeno JM, and Alborch E. Diabetes potentiates acetylcholine-induced relaxation in rabbit renal arteries. Eur J Pharmacol 415: 225-232, 2001.
4. Alberola A, Pinilla JM, Quesada T, Romero JC, Salom MG, and Salazar FJ. Role of nitric oxide in mediating renal response to volume expansion. Hypertension 9: 780-784, 1992.
5. Anderson S and Komers R. Pathogenesis of diabetic glomerulopathy: the role of glomerular hemodynamic factors. In: The Kidney and Hypertension in Diabetes Mellitus, edited by Mogensen CE. Boston, MA: Kluwer, 2000, p. 281-294.
6. Arima S, Ito S, Omata K, Takeuchi K, and Abe K. High glucose augments angiotensin II action by inhibiting NO synthesis in in vitro microperfused rabbit afferent arterioles. Kidney Int 48: 683-689, 1995.
7. Bachmann S, Bosse HM, and Mundel P. Topography of nitric oxide synthesis by localizing constitutive NO synthases in mammalian kidney. Am J Physiol Renal Fluid Electrolyte Physiol 268: F885-F898, 1995.
8. Bank N and Aynedjian HS. Role of EDRF (nitric oxide) in diabetic renal hyperfiltration. Kidney Int 43: 1306-1312, 1993.
9. Baylis C and Qiu C. Importance of nitric oxide in the control of renal hemodynamics. Kidney Int 49: 1727-1731, 1996.
10. Beenen OH, Mathy MJ, Pfaffendorf M, and van Zwieten PA. Vascular responsiveness in isolated perfused kidneys of diabetic hypertensive rats. J Hypertens 14: 1125-1130, 1996.
11. Bhardwaj R and Moore PK. Increased vasodilator response to acetylcholine of renal blood vessels from diabetic rats. J Pharm Pharmacol 40: 739-742, 1988.
12. Bosse HM, Bohm R, Resch S, and Bachmann S. Parallel regulation of constitutive NO synthase and renin at JGA of rat kidney under various stimuli. Am J Physiol Renal Fluid Electrolyte Physiol 269: F793-F805, 1995.
13. Brodsky SV, Morrishow AM, Dharia N, Gross SS, and Goligorsky MS. Glucose scavenging of nitric oxide. Am J Physiol Renal Physiol 280: F480-F486, 2001.
14. Bucala R, Tracey KJ, and Cerami A. Advanced glycosylation products quench nitric oxide and mediate defective endothelium-dependent vasodilatation in experimental diabetes. J Clin Invest 87: 432-438, 1991.
15. Carmines PK, Fallet RW, Roscow J, Sasser JM, and Pollock JS. Renal cortical Hsp90 and its impact on NOS activity and afferent arteriolar tone are diminished in diabetes mellitus (Abstract). J Am Soc Nephrol 13: 532A, 2002.
16. Carmines PK, Ohishi K, and Ikenaga H. Functional impairment of renal afferent arteriolar voltage-gated calcium channels in rats with diabetes mellitus. J Clin Invest 98: 2564-2571, 1996.
17. 1 modulates NOS expression and phosphorylation of Akt/PKB in rat myocytes exposed to hypoxia-reoxygenation. Am J Physiol Heart Circ Physiol 281: H1035-H1039, 2001.
18. Cho H, Mu J, Kim JK, Thorvaldsen JL, Chu Q, Crenshaw EB III, Kaestner KH, Bartolomei MS, Shulman GI, and Birnbaum MJ. Insulin resistance and a diabetes mellitus-like syndrome in mice lacking the protein kinase Akt2 (PKB β). Science 292: 1728-1731, 2001.
19. Choi KC, Kim NH, An MR, Kang DG, Kim SW, and Lee J. Alterations of intrarenal renin-angiotensin and nitric oxide systems in streptozotocin-induced diabetic rats. Kidney Int 52, Suppl 60: S23-S27, 1997.
20. Cosentino F, Hishikawa K, Katusic ZS, and Luscher TF. High glucose increases nitric oxide synthase expression and superoxide anion generation in human aortic endothelial cells. Circulation 96: 25-28, 1997.
21. Craven PA, DeRubertis FR, and Melhem M. Nitric oxide in diabetic nephropathy. Kidney Int 52, Suppl 60: S46-S53, 1997.
22. Craven PA, Studer RK, and DeRubertis FR. Impaired nitric oxide release by glomeruli from diabetic rats. Metabolism 44:695-698, 1995.
23. Craven PA, Studer RK, and DeRubertis FR. Impaired nitric oxide-dependent cyclic guanosine monophosphate generation in glomeruli from diabetic rats. Evidence for protein kinase C-mediated supression of cholinergic response. J Clin Invest 93: 311-320, 1994.
24. Craven PA, Studer RK, Felder J, Phillips S, and DeRubertis FR. Nitric oxide inhibition of transforming growth factor-beta and collagen synthesis in mesangial cells. Diabetes 46: 671-681, 1997.
25. Dai FX, Diederich A, Skopec J, and Diederich D. Diabetes-induced endothelial dysfunction in streptozotocin-treated rats: role of prostaglandin endoperoxides and free radicals. J Am Soc Nephrol 4: 1327-1336, 1993.
26. De Vriese AS, Stoenoiu MS, Elger M, Devuyst O, Vanholder R, Kriz W, and Lameire NH. Diabetes-induced microvascular dysfunction in the hydronephrotic kidney: role of nitric oxide. Kidney Int 60: 202-210, 2001.
27. De Vriese AS, Tilton RG, Elger M, Stephan CC, Kriz W, and Lameire NH. Antibodies against vascular endothelial growth factor improve early renal dysfunction in experimental diabetes. J Am Soc Nephrol 12: 993-1000, 2001.
28. Deng A and Baylis C. Locally produced EDRF controls preglomerular resistance and ultrafiltration coefficient. Am J Physiol Renal Fluid Electrolyte Physiol 264: F212-F215, 1993.
29. Dimmeler S, Fleming I, Fisslthaler B, Hermann C, Busse R, and Zeiher AM. Activation of nitric oxide synthase in endothelial cells by Akt-dependent phosphorylation. Nature 399: 601-605, 1999.
30. Du XL, Edelstein D, Dimmeler S, Ju Q, Sui C, and Brownlee M. Hyperglycemia inhibits endothelial nitric oxide synthase activity by posttranslational modification at the Akt site. J Clin Invest 108: 1341-1348, 2001.
31. Feliers D, Duraisamy S, Faulkner JL, Duch J, Lee AV, Abboud HE, Choudhury GG, and Kasinath BS. Activation of renal signaling pathways in db/db mice with type 2 diabetes. Kidney Int 60: 495-504, 2001.
32. 2+-independent activation of the endothelial nitric oxide synthase in response to tyrosine phosphatase inhibitors and fluid shear stress. Circ Res 82: 686-695, 1998.
33. 2+/calmodulin-dependent endothelial nitric oxide synthase activity. Circ Res 88: E68-E75, 2001.
34. Fulton D, Gratton JP, McCabe TJ, Fontana J, Fujio Y, Walsh K, Franke TF, Papapetropoulos A, and Sessa WC. Regulation of endothelium-derived nitric oxide production by the protein kinase Akt. Nature 399: 597-601, 1999.
35. Garg UC and Hassid A. Inhibition of rat mesangial cell mitogenesis by nitric oxide generating vasodilators. Am J Physiol Renal Fluid Electrolyte Physiol 257: F60-F66, 1989.
36. Gilbert RE and Cooper ME. The tubulointerstitium in progressive diabetic kidney disease: more than an aftermath of glomerular injury? Kidney Int 56: 1627-1637, 1999.
37. Goor Y, Peer G, Iaina A, Blum M, Wollman Y, Chernihovsky T, Silverberg D, and Cabili S. Nitric oxide in ischaemic acute renal failure of streptozotocin diabetic rats. Diabetologia 39: 1036-1040, 1996.
38. Gorin Y, Kim NH, Feliers D, Bhandari B, Choudhury GG, and Abboud HE. Angiotensin II activates Akt/protein kinase B by an arachidonic acid/redox-dependent pathway and independent of phosphoinositide 3-kinase. FASEB J 15: 1909-1920, 2001.
39. Govers R and Rabelink TJ. Cellular regulation of endothelial nitric oxide synthase. Am J Physiol Renal Physiol 280: F193-F206, 2001.
40. Griendling KK and Ushio-Fukai M. Reactive oxygen species as mediators of angiotensin II signaling. Regul Pept 91: 21-27, 2000.
41. Guo K, Andres V, and Walsh K. Nitric oxide-induced down-regulation of Cdk2 activity and cyclin A gene transcription in vascular smooth muscle cells. Circulation 97: 2066-2072, 1998.
42. Harris MB, Ju H, Venema VJ, Liang H, Zou R, Michell BJ, Chen ZP, Kemp BE, and Venema RC. Reciprocal phosphorylation and regulation of endothelial nitric-oxide synthase in response to bradykinin stimulation. J Biol Chem 276: 16587-16591, 2001.
43. Hayashi K, Loutzenhiser R, Epstein M, Suzuki H, and Saruta T. Multiple factors contribute to acetylcholine-induced renal afferent arteriolar vasodilation during myogenic and norepinephrine- and KCl-induced vasoconstriction. Studies in the isolated perfused hydronephrotic kidney. Circ Res 75: 821-828, 1994.
44. He H, Venema VJ, Gu X, Venema RC, Marrero MB, and Caldwell RB. Vascular endothelial growth factor signals endothelial cell production of nitric oxide and prostacyclin through flk-1/KDR activation of c-Src. J Biol Chem 274: 25130-25135, 1999.
45. Hellermann GR and Solomonson LP. Calmodulin promotes dimerization of the oxygenase domain of human endothelial nitric-oxide synthase. J Biol Chem 272: 12030-12034, 1997.
46. Hink U, Li H, Mollnau H, Oelze M, Matheis E, Hartmann M, Skatchkov M, Thaiss F, Stahl RA, Warnholtz A, Meinertz T, Griendling K, Harrison DG, Forstermann U, and Munzel T. Mechanisms underlying endothelial dysfunction in diabetes mellitus. Circ Res 88: E14-E22, 2001.
47. Hirata K, Kuroda R, Sakoda T, Katayama M, Inoue N, Suematsu M, Kawashima S, and Yokoyama M. Inhibition of endothelial nitric oxide synthase activity by protein kinase C. Hypertension 25: 180-185, 1995.
48. Horowitz JR, Rivard A, van der Zee R, Hariawala M, Sheriff DD, Esakof DD, Chaudhry GM, Symes JF, and Isner JM. Vascular endothelial growth factor/vascular permeability factor produces nitric oxide-dependent hypotension. Evidence for a maintenance role in quiescent adult endothelium. Arterioscler Thromb Vasc Biol 17: 2793-2800, 1997.
49. Hostetter TH, Rennke HG, and Brenner BM. The case for intrarenal hypertension in the initiation and progression of diabetic and other glomerulopathies. Am J Med 80: 443-453, 1982.
50. Hostetter TH, Troy JL, and Brenner BM. Glomerular hemodynamics in experimental diabetes mellitus. Kidney Int 19: 410-415, 1981.
51. Ichihara A, Inscho EW, Imig JD, and Navar LG. Neuronal nitric oxide synthase modulates rat renal microvacular function. Am J Physiol Renal Physiol 274: F516-F524, 1998.
52. Inoue N, Venema RC, Sayegh HS, Ohara Y, Murphy TJ, and Harrison DG. Molecular regulation of the bovine endothelial cell nitric oxide synthase by transforming growth factor-beta 1. Arterioscler Thromb Vasc Biol 15: 1255-1261, 1995.
53. Ishida A, Sasaguri T, Kosaka C, Nojima H, and Ogata J. Induction of the cyclin-dependent kinase inhibitor p21(Sdi1/Cip1/Waf1) by nitric oxide-generating vasodilator in vascular smooth muscle cells. J Biol Chem 272: 10050-10057, 1997.
54. Ishii N, Patel KP, Lane PH, Taylor T, Bian K, Murad F, Pollock JS, and Carmines PK. Nitric oxide synthesis and oxidative stress in the renal cortex of rats with diabetes mellitus. J Am Soc Nephrol 12: 1630-1639, 2001.
55. Ito A, Uriu K, Inada Y, Qie YL, Takagi I, Ikeda M, Hashimoto O, Suzuka K, Eto S, Tanaka Y, and Kaizu K. Inhibition of neuronal nitric oxide synthase ameliorates renal hyperfiltration in streptozotocin-induced diabetic rat. J Lab Clin Med 138: 177-185, 2001.
56. Jaimes EA, Sweeney C, and Raij L. Effects of the reactive oxygen species hydrogen peroxide and hypochlorite on endothelial nitric oxide production. Hypertension 38: 877-883, 2001.
57. Janssens S, Flaherty D, Nong Z, Varenne O, van Pelt N, Haustermans C, Zoldhelyi P, Gerard R, and Collen D. Human endothelial nitric oxide synthase gene transfer inhibits vascular smooth muscle cell proliferation and neointima formation after balloon injury in rats. Circulation 97: 1274-1281, 1998.
58. Ju H, Zou R, Venema VJ, and Venema RC. Direct interaction of endothelial nitric-oxide synthase and caveolin-1 inhibits synthase activity. J Biol Chem 272: 18522-18525, 1997.
59. 1 as a major factor for renal injury induced by chronic inhibition of nitric oxide synthase in rats. J Am Soc Nephrol 11: 616-624, 2000.
60. Keynan S, Hirshberg B, Levin-Iaina N, Wexler ID, Dahan R, Reinhartz E, Ovadia H, Wollman Y, Chernihovskey T, Iaina A, and Raz I. Renal nitric oxide production during the early phase of experimental diabetes mellitus. Kidney Int 58: 740-747, 2000.
61. G-nitro-L-arginine methyl ester on regional haemodynamics in conscious rats with streptozotocin-induced diabetes mellitus. Br J Pharmacol 103: 1321-1326, 1991.
62. ω-monomethyl-L-arginine (L-NMMA) (Abstract). J Am Soc Nephrol 1: 666, 1990.
63. Komers R, Allen TJ, and Cooper ME. Role of endotheliumderived nitric oxide in the pathogenesis of the renal hemodynamic changes of experimental diabetes. Diabetes 43: 1190-1197, 1994.
64. Komers R, Lindsley JN, Oyama TT, Allison KM, and Anderson S. Role of neuronal NOS (NOS1) in the pathogenesis of renal hemodynamic changes in diabetes. Am J Physiol Renal Physiol 279: F573-F583, 2000.
65. Komers R, Lindsley JN, Oyama TT, and Anderson S. Functional expression of endothelial nitric oxide synthase and caveolin-1 in diabetic kidney cortex (Abstract). J Am Soc Nephrol 13: 532A, 2002.
66. Komers R, Oyama TT, Chapman JG, Allison KM, and Anderson S. Effects of systemic inhibition of neuronal nitric oxide synthase in diabetic rats. Hypertension 34: 655-661, 2000.
67. Komers R, Oyama TT, Lindsley JN, and Anderson S. Long-term inhibition of neuronal nitric oxide (NO) synthase (NOS1) postpones development of proteinuria in uninephrectomized diabetic rats (Abstract). J Am Soc Nephrol 12: A4391, 2001.
68. Kone BC and Baylis C. Biosynthesis and homeostatic roles of nitric oxide in the normal kidney. Am J Physiol Renal Physiol 272: F561-F578, 1997.
69. Koya D, Jirousek MR, Lin YW, Ishii H, Kuboki K, and King GL. Characterization of protein kinase C-β isoform activation on the gene expression of transforming factor-β, extracellular matrix components, and prostanoids in the glomeruli of diabetic rats. J Clin Invest 100: 115-126, 1997.
70. Koya D and King GL. Protein kinase C activation and the development of diabetic complications. Diabetes 47: 859-866, 1998.
71. Koya D, Lee IK, Ishii H, Kanoh H, and King GL. Prevention of glomerular dysfunction in diabetic rats by treatment with D-α-tocopherol. J Am Soc Nephrol 8: 426-435, 1997.
72. Krishna MC, Samuni A, Taira J, Goldstein S, Mitchell JB, and Russo A. Stimulation by nitroxides of catalase-like activity of hemeproteins. Kinetics and mechanism. J Biol Chem 271: 26018-26025, 1996.
73. Krook A, Roth RA, Jiang XJ, Zierath JR, and Wallberg-Henriksson H. Insulin-stimulated Akt kinase activity is reduced in skeletal muscle from NIDDM subjects. Diabetes 47: 1281-1286, 1998.
74. Kuan CJ, al-Douahji M, and Shankland SJ. The cyclin kinase inhibitor p21WAF1, CIP1 is increased in experimental diabetic nephropathy: potential role in glomerular hypertrophy. J Am Soc Nephrol 9: 986-993, 1998.
75. Kuboki K, Jiang ZY, Takahara N, Ha SW, Igarashi M, Yamauchi T, Feener EP, Herbert TP, Rhodes CJ, and King GL. Regulation of endothelial constitutive nitric oxide synthase gene expression in endothelial cells and in vivo: a specific vascular action of insulin. Circulation 101: 676-681, 2000.
76. Malinski T, Taha Z, Grunfeld S, Patton S, Kapturczak M, and Tomboulian P. Diffusion of nitric oxide in the aorta wall monitored in situ by porphyrinic microsensors. Biochem Biophys Res Commun 193: 1076-1082, 1993.
77. Marletta MA. Nitric oxide: biosynthesis and biological significance. Trends Pharmacol Sci 158: 348-352, 1989.
78. Mattar AL, Fujihara CK, Ribeiro MO, de Nucci G, and Zatz R. Renal effects of acute and chronic nitric oxide inhibition in experimental diabetes. Nephron 74: 136-143, 1996.
79. Mattson DL, Roman RJ, and Cowley AW. Role of nitric oxide in renal papillary blood flow and sodium excretion. Hypertension 19: 766-769, 1992.
80. Melhem MF, Craven PA, and Derubertis FR. Effects of dietary supplementation of α-lipoic acid on early glomerular injury in diabetes mellitus. J Am Soc Nephrol 12: 124-133, 2001.
81. Michel T and Feron O. Nitric oxide synthases: which, where, how, and why? J Clin Invest 100: 2146-2152, 1997.
82. Michell BJ, Chen Z, Tiganis T, Stapleton D, Katsis F, Power DA, Sim AT, and Kemp BE. Coordinated control of endothelial nitric-oxide synthase phosphorylation by protein kinase C and the cAMP-dependent protein kinase. J Biol Chem 276: 17625-17628, 2001.
83. Mogensen CE. Early glomerular hyperfiltration in insulin-dependent diabetics and late nephropathy. Scand J Clin Invest 1986: 201-206, 1986.
84. Mohaupt MG, Elzie JL, Ahn KY, Clapp WL, Wilcox CS, and Kone BC. Differential expression and induction of mRNAs encoding two inducible nitric oxide synthases in rat kidney. Kidney Int 46: 653-665, 1994.
85. Moncada S and Higgs EA. The L-arginine-nitric oxide pathway. N Engl J Med 329: 2002-2012, 1993.
86. Moore LC, Thorup C, Ellinger A, Paccione J, Casellas D, and Kaskel FJ. Advanced glycosylation end-products and NO-dependent vasodilation in renal afferent arterioles from diabetic rats. Acta Physiol Scand 168: 101-106, 2000.
87. Morbidelli L, Chang CH, Douglas JG, Granger HJ, Ledda F, and Ziche M. Nitric oxide mediates mitogenic effect of VEGF on coronary venular endothelium. Am J Physiol Heart Circ Physiol 270: H411-H415, 1996.
88. Morrisey JJ, McCracken R, Kaneto H, Vehaskari M, Montani D, and Klahr S. Location of an inducible nitric oxide synthase mRNA in the normal kidney. Kidney Int 45: 998-1005, 1994.
89. Narayanan K, Spack L, McMillan K, Kilbourn RG, Hayward MA, Masters BSS, and Griffith OW. Salkyl-L-thiocitrullines. J Biol Chem 270: 11103-11110, 1995.
90. Ohishi K and Carmines PK. Superoxide dismutase restores the influence of nitric oxide on renal arterioles in diabetes mellitus. J Am Soc Nephrol 5: 1559-1566, 1995.
91. Omer S, Shan J, Varma DR, and Mulay S. Augmentation of diabetes-associated renal hyperfiltration and nitric oxide production by pregnancy in rats. J Endocrinol 161: 15-23, 1999.
92. Onozato ML, Tojo A, Goto A, Fujita T, and Wilcox CS. Oxidative stress and nitric oxide synthase in rat diabetic nephropathy: effects of ACEI and ARB. Kidney Int 61: 186-194, 2002.
93. Osterby R. Glomerular structural changes in type 1 (insulin-dependent) diabetes mellitus: causes, consequences, and prevention. Diabetologia 35: 803-812, 1992.
94. Oyadomari S, Gotoh T, Aoyagi K, Araki E, Shichiri M, and Mori M. Coinduction of endothelial nitric oxide synthase and arginine recycling enzymes in aorta of diabetic rats. Nitric Oxide 5: 252-260, 2001.
95. Peterson TE, Poppa V, Ueba H, Wu A, Yan C, and Berk BC. Opposing effects of reactive oxygen species and cholesterol on endothelial nitric oxide synthase and endothelial cell caveolae. Circ Res 85: 29-37, 1999.
96. Pflueger AC, Larson TS, Hagl S, and Knox F. Role of nitric oxide in intrarenal hemodynamics in experimental diabetes mellitus in rats. Am J Physiol Regul Integr Comp Physiol 277: R725-R733, 1999.
97. Pflueger AC, Osswald H, and Knox F. Adenosine-induced renal vasoconstriction in diabetes mellitus. Am J Physiol Renal Physiol 276: F340-F346, 1999.
98. Pieper GM. Enhanced, unaltered and impaired nitric oxidemediated endothelium-dependent relaxation in experimental diabetes mellitus: importance of disease duration. Diabetologia 42: 204-213, 1999.
99. Pieper GM. Review of alterations in endothelial nitric oxide production in diabetes. Protective role of arginine on endothelial dysfunction. Hypertension 31: 1047-1060, 1998.
100. Pieper GM, Jordan M, Adams MB, and Roza AM. Syngeneic pancreatic islet transplantation reverses endothelial dysfunction in experimental diabetes. Diabetes 33: 1106-1113, 1995.
101. Poppa V, Miyashiro JK, Corson MA, and Berk BC. Endothelial NO synthase is increased in regenerating endothelium after denuding injury of the rat aorta. Arterioscler Thromb Vasc Biol 18: 1312-1321, 1998.
102. Pou S, Pou WS, Bredt DS, Snyder SH, and Rosen GM. Generation of superoxide by purified brain nitric oxide synthase. J Biol Chem 267: 24173-24176, 1992.
103. Reyes AA, Karl IE, Kissane J, and Klahr S. L-arginine administration prevents glomerular hyperfiltration and decreases proteinuria in diabetic rats. J Am Soc Nephrol 4: 1039-1045, 1993.
104. Roczniak A, Zimpelmann J, and Burns KD. Effect of dietary salt on neuronal nitric oxide synthase in inner medullary collecting duct. Am J Physiol Renal Physiol 275: F46-F54, 1998.
105. Rudberg S, Persson B, and Dahlquist G. Increased glomerular filtration rate as a predictor of diabetic nephropathy-an 8-year prospective study. Kidney Int 41: 822-828, 1992.
106. Santizo RA, Koenig HM, and Pelligrino DA. β-Adrenoceptor and nNOS-derived NO interactions modulate hypoglycemic pial arteriolar dilation in rats. Am J Physiol Heart Circ Physiol 280: H562-H568, 2001.
107. Schini-Kerth VB and Vanhoutte PM. Nitric oxide synthases in vascular cells. Exp Physiol 80: 885-905, 1995.
108. Schnackenberg CG. Physiological and pathophysiological roles of oxygen radicals in the renal microvasculature. Am J Physiol Regul Integr Comp Physiol 282: R335-R342, 2002.
109. Schnackenberg CG and Wilcox CS. The SOD mimetic tempol restores vasodilation in afferent arterioles of experimental diabetes. Kidney Int 59: 1859-1864, 2001.
110. Scholey JW and Meyer TW. Control of glomerular hypertension by insulin administration in diabetic rats. J Clin Invest 83: 1384-1389, 1989.
111. Schoonmaker GC, Fallet RW, and Carmines PK. Superoxide anion curbs nitric oxide modulation of afferent arteriolar ANG II responsiveness in diabetes mellitus. Am J Physiol Renal Physiol 278: F302-F309, 2000.
112. Schwartz D, Schwartz IF, and Blantz RC. An analysis of renal nitric oxide contribution to hyperfiltration in diabetic rats. J Lab Clin Med 137: 107-114, 2001.
113. Sharma K, Danoff TM, DePiero A, and Ziyadeh FN. 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 207: 80-88, 1995.
114. Sharma RV, Tan E, Fang S, Gurjar MV, and Bhalla RC. NOS gene transfer inhibits expression of cell cycle regulatory molecules in vascular smooth muscle cells. Am J Physiol Heart Circ Physiol 276: H1450-H1459, 1999.
115. Shin SJ, Lai FJ, Wen JD, Hsiao PJ, Hsieh MC, Tzeng TF, Chen HC, Guh JY, and Tsai JH. Neuronal and endothelial nitric oxide synthase expression in outer medulla of streptozotocin-induced diabetic rat kidney. Diabetologia 43: 649-659, 2000.
116. Soulis T, Cooper ME, Sastra S, Thallas V, Panagiotopoulos S, Bjerrum OJ, and Jerums G. Relative contributions of advanced glycation and nitric oxide synthase inhibition to aminoguanidine-mediated renoprotection in diabetic rats. Diabetologia 40: 1141-1151, 1997.
117. Studer RK, DeRubertis FR, and Craven PA. Nitric oxide suppresses increases in mesangial cell protein kinase C, transforming growth factor beta, and fibronectin synthesis induced by thromboxane. J Am Soc Nephrol 7: 999-1005, 1996.
118. Sugimoto H, Shikata K, Matsuda M, Kushiro M, Hayashi Y, Hiragushi K, Wada J, and Makino H. Increased expression of endothelial cell nitric oxide synthase (ecNOS) in afferent and glomerular endothelial cells is involved in glomerular hyperfiltration of diabetic nephropathy. Diabetologia 41: 1426-1434, 1998.
119. Sugimoto H, Shikata K, Wada J, Horiuchi S, and Makino H. Advanced glycation end products-cytokine-nitric oxide sequence pathway in the development of diabetic nephropathy: aminoguanidine ameliorates the overexpression of tumour necrosis factor-alpha and inducible nitric oxide synthase in diabetic rat glomeruli. Diabetologia 42: 878-886, 1999.
120. Suto T, Losonczy G, Qiu C, Hill C, Samsell L, Ruby J, Charon N, Venuto R, and Baylis C. Acute changes in urinary excretion of nitrite + nitrate do not necessarily predict renal vascular NO production. Kidney Int 48: 1272-1277, 1995.
121. Takahashi T, Taniguchi T, Konishi H, Kikkawa U, Ishikawa Y, and Yokoyama M. Activation of Akt/protein kinase B after stimulation with angiotensin II in vascular smooth muscle cells. Am J Physiol Heart Circ Physiol 276: H1927-H1934, 1999.
122. Tanner FC, Meier P, Greutert H, Champion C, Nabel EG, and Luscher TF. Nitric oxide modulates expression of cell cycle regulatory proteins: a cytostatic strategy for inhibition of human vascular smooth muscle cell proliferation. Circulation 101: 1982-1989, 2000.
123. Terada Y, Tomita K, Nonoguchi H, and Marumo F. Polymerase chain reaction localization of constitutive nitric oxide synthase and soluble guanylate cyclase messenger RNAs in microdissected rat nephron segments. J Clin Invest 90: 659-665, 1992.
124. Thorup C, Erik A, and Persson G. Macula densa derived nitric oxide in regulation of glomerular capillary pressure. Kidney Int 49: 430-436, 1996.
125. Thuraisingham RC, Nott CA, Dodd SM, and Yaqoob MM. Increased nitrotyrosine staining in kidneys from patients with diabetic nephropathy. Kidney Int 57: 1968-1972, 2000.
126. Tilton RG, Kawamura T, Chang KC, Ido Y, Bjercke RJ, Stephan CC, Brock TA, and Williamson JR. Vascular dysfunction induced by elevated glucose levels in rats is mediated by vascular endothelial growth factor. J Clin Invest 99: 2192-2202, 1997.
127. Tojo A, Gross SS, Zhang L, Tisher CC, Schmidt HHHW, Wilcox CS, and Madsen KM. Immunohistochemical localization of distinct isoforms of nitric oxide synthase in the juxtaglomerular apparatus of normal rat kidney. J Am Soc Nephrol 4:1438-1447, 1994.
128. Tolins JP, Shultz PJ, Raij L, Brown DM, and Mauer SM. Abnormal renal hemodynamic response to reduced renal perfusion pressure in diabetic rats: role of NO. Am J Physiol Renal Fluid Electrolyte Physiol 265: F886-F895, 1993.
129. Tomita H, Egashira K, Ohara Y, Takemoto M, Koyanagi M, Katoh M, Yamamoto H, Tamaki K, Shimokawa H, and Takeshita A. Early induction of transforming growth factorbeta via angiotensin II type 1 receptors contributes to cardiac fibrosis induced by long-term blockade of nitric oxide synthesis in rats. Hypertension 32: 273-279, 1998.
130. Torffvit O and Edvinsson L. Blockade of nitric oxide decreases the renal vasodilatory effect of neuropeptide Y in the insulin-treated diabetic rat. Pflügers Arch 434: 445-450, 1997.
131. Torffvit O and Edvinsson L. Relaxing effect of insulin in renal arteries from diabetic rats. Regul Pept 79: 147-152, 1999.
132. Trachtman H, Futterweit S, and Crimmins DL. High glucose inhibits nitric oxide production in cultured rat mesangial cells. J Am Soc Nephrol: 1276-1282, 1997.
133. Uematsu M, Ohara Y, Navas JP, Nishida K, Murphy TJ, Alexander RW, Nerem RM, and Harrison DG. Regulation of endothelial cell nitric oxide synthase mRNA expression by shear stress. Am J Physiol Cell Physiol 269: C1371-C1378, 1995.
134. Ushio-Fukai M, Alexander RW, Akers M, Yin Q, Fujio Y, Walsh K, and Griendling KK. Reactive oxygen species mediate the activation of Akt/protein kinase B by angiotensin II in vascular smooth muscle cells. J Biol Chem 274: 22699-22704, 1999.
135. Vallon V, Blantz RC, and Thomson S. Homeostatic efficiency of tubuloglomerular feedback is reduced in established diabetes mellitus in rats. Am J Physiol Renal Fluid Electrolyte Physiol 269: F876-F883, 1995.
136. Van der Zee R, Murohara T, Luo Z, Zollmann F, Passeri J, Lekutat C, and Isner JM. Vascular endothelial growth factor/vascular permeability factor augments nitric oxide release from quiescent rabbit and human vascular endothelium. Circulation 95: 1030-1037, 1997.
137. Vanhoutte PM. Endothelium-derived free radicals: for worse and for better. J Clin Invest 107: 23-25, 2001.
138. Vasquez-Vivar J, Hogg N, Martasek P, Karoui H, Pritchard KA Jr, and Kalyanaraman B. Tetrahydrobiopterin-dependent inhibition of superoxide generation from neuronal nitric oxide synthase. J Biol Chem 274: 26736-26742, 1999.
139. Vasquez-Vivar J, Kalyanaraman B, Martasek P, Hogg N, Masters BS, Karoui H, Tordo P, and Pritchard KA Jr. Superoxide generation by endothelial nitric oxide synthase: the influence of cofactors. Proc Natl Acad Sci USA 95: 9220-9225, 1998.
140. Vecchione C, Maffei A, Colella S, Aretini A, Poulet R, Frati G, Gentile MT, Fratta L, Trimarco V, Trimarco B, and Lembo G. Leptin effect on endothelial nitric oxide is mediated through Akt-endothelial nitric oxide synthase phosphorylation pathway. Diabetes 51: 168-173, 2002.
141. Veelken R, Hilgers KF, Hartner A, Haas A, Bohmer K, and Sterzel RB. Nitric oxide synthase isoforms and glomerular hyperfiltration in early diabetic nephropathy. J Am Soc Nephrol 11: 71-79, 2000.
142. Venema RC, Sayegh HS, Kent JD, and Harrison DG. Identification, characterization, and comparison of calmodulin binding domains of the endothelial and inducible nitric oxide synthases. J Biol Chem 271: 6435-6440, 1996.
143. Verbeke P, Perichon M, Friguet B, and Bakala H. Inhibition of nitric oxide synthase activity by early and advanced glycation end products in cultured rabbit proximal tubular epithelial cells. Biochim Biophys Acta 1502: 481-494, 2000.
144. Von der Leyen HE, Gibbons GH, Morishita R, Lewis NP, Zhang L, Nakajima M, Kaneda Y, Cooke JP, and Dzau VJ. Gene therapy inhibiting neointimal vascular lesion: in vivo transfer of endothelial cell nitric oxide synthase gene. Proc Natl Acad Sci USA 92: 1137-1141, 1995.
145. Wang S, Shiva S, Poczatek MH, Darley-Usmar V, and Murphy-Ullrich JE. Nitric oxide and cGMP-dependent protein kinase regulation of glucose-mediated thrombospondinldependent TGF-β activation in mesangial cells. J Biol Chem 277: 9880-9888, 2002.
146. Wang YX, Brooks DP, and Edwards RM. Attenuated glomerular cGMP production and renal vasodilation in streptozotocin-induced diabetic rats. Am J Physiol Regul Integr Comp Physiol 264: R952-R956, 1993.
147. Welch WJ and Wilcox CS. Macula densa arginine delivery and uptake in the rat regulates glomerular capillary pressure. J Clin Invest 100: 2235-2242, 1997.
148. Wever RM, van Dam T, van Rijn HJ, de Groot F, and Rabelink TJ. Tetrahydrobiopterin regulates superoxide and nitric oxide generation by recombinant endothelial nitric oxide synthase. Biochem Biophys Res Commun 237: 340-344, 1997.
149. Wilcox CS and Welch WJ. Macula densa nitric oxide synthase: expression, regulation, and function. Kidney Int 54: S53-S57, 1998.
150. Wilcox CS, Welch WJ, Murad F, Gross SS, Taylor G, Levi R, and Schmidt HH. Nitric oxide synthase in macula densa regulates glomerular capillary pressure. Proc Natl Acad Sci USA 89: 11993-11997, 1992.
151. Wolf G. Cell cycle regulation in diabetic nephropathy. Kidney Int 58, Suppl 77: S-59-S-66, 2000.
152. Wolf G, Hamann A, Han DC, Helmchen U, Thaiss F, Ziyadeh FN, and Stahl RA. Leptin stimulates proliferation and TGF-β expression in renal glomerular endothelial cells: potential role in glomerulosclerosis. Kidney Int 56: 860-872, 1999.
153. Wolf G, Schroeder R, Thaiss F, Ziyadeh FN, Helmchen U, and Stahl RA. Glomerular expression of p27Kip1 in diabetic db/db mouse: role of hyperglycemia. Kidney Int 53: 869-879, 1998.
154. Wu F, Park F, Cowley AW, and Mattson DL. Quantification of nitric oxide synthase activity in microdissected segments of the rat kidney. Am J Physiol Renal Physiol 276: F874-F881, 1999.
155. 2+/calmodulin-dependent and tetrahydrobiopterin regulatory process. J Biol Chem 273: 25804-25808, 1998.
156. Xia Y and Zweier JL. Superoxide and peroxynitrite generation from inducible nitric oxide synthase in macrophages. Proc Natl Acad Sci USA 94: 6954-6958, 1997.
157. Yagihashi N, Nishida N, Seo HG, Taniguchi N, and Yagihashi S. Expression of nitric oxide synthase in macula densa in streptozotocin diabetic rats. Diabetologia 39: 793-799, 1996.
158. 1. Am J Physiol Renal Physiol 275: F18-F24, 1998.
159. Zatz R and de Nucci G. Effects of acute nitric oxide inhibition on rat glomerular microcirculation. Am J Physiol Renal Fluid Electrolyte Physiol 261: F360-F363, 1991.
160. Zatz R, Dunn BR, Meyer TW, Anderson S, Rennke HG, and Brenner BM. Prevention of diabetic glomerulopathy by pharmacological amelioration of glomerular capillary hypertension. J Clin Invest 77: 1925-1930, 1986.
161. Zatz R, Meyer TW, Rennke HG, and Brenner BM. Predominance of hemodynamic rather than metabolic factors in the pathogenesis of diabetic nephropathy. Proc Natl Acad Sci USA 82:5963-5967, 1985.
162. Zeng G, Nystrom FH, Ravichandran LV, Cong LN, Kirby M, Mostowski H, and Quon MJ. Roles for insulin receptor, PI3-kinase, and Akt in insulin-signaling pathways related to production of nitric oxide in human vascular endothelial cells. Circulation 101: 1539-1545, 2000.
163. Zeng G and Quon MJ. Insulin-stimulated production of nitric oxide is inhibited by wortmannin. Direct measurement in vascular endothelial cells. J Clin Invest 98: 894-898, 1996.