Improvement of endothelial nitric oxide synthase activity retards the progression of diabetic nephropathy in db/db mice

Kidney International

Volumn 82, Issue 11, 2012, Pages 1176-1183

  Cheng, Huifang ^a   Wang, Hanmin ^a   Fan, Xiaofeng ^a   Paueksakon, Paisit ^a   Harris, Raymond C ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

db db mice; diabetic nephropathy; eNOS; glomerular endothelial cells; sepiapterin

Indexed keywords

3 NITROTYROSINE; ARGININE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; GLUCOSE; ISOPROSTANE DERIVATIVE; MONOMER; SEPIAPTERIN; TETRAHYDROBIOPTERIN;

ALBUMINURIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CELL MEMBRANE PERMEABILITY; CONTROLLED STUDY; DIABETIC NEPHROPATHY; DIMERIZATION; ENDOTHELIUM CELL; GLOMERULUS BASEMENT MEMBRANE; GLOMERULUS FILTRATION; KIDNEY HYPERTROPHY; MALE; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION;

EID: 84869220435     PISSN: 00852538     EISSN: 15231755     Source Type: Journal    
DOI: 10.1038/ki.2012.248     Document Type: Article

References (60)

1. Nawroth PP, Isermann B. Mechanisms of diabetic nephropathy-old buddies and newcomers part 1. Exp Clin Endocrinol Diab 2010; 118: 571-576.
2. Patrakka J, Tryggvason K. Molecular make-up of the glomerular filtration barrier. Biochem Biophys Res Commun 2010; 396: 164-169.
3. Stehouwer CD. Endothelial dysfunction in diabetic nephropathy: state of the art and potential significance for non-diabetic renal disease. Nephrol Dial Transplant 2004; 19: 778-781. (Pubitemid 38455645)
4. Hoshiyama M, Li B, Yao J et al. Effect of high glucose on nitric oxide production and endothelial nitric oxide synthase protein expression in human glomerular endothelial cells. Nephron Exp Nephrol 2003; 95: e62-e68.
5. 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. (Pubitemid 24361183)
6. Mohan S, Konopinski R, Yan B et al. High glucose-induced IKK-Hsp-90 interaction contributes to endothelial dysfunction. Am J Physiol Cell Physiol 2009; 296: C182-C192.
7. Janssens S, Flaherty D, Nong Z et al. Human endothelial nitric oxide synthase gene transfer inhibits vascular smooth muscle cell proliferation and neointima formation after balloon injury in rats. Circulation 1998; 97: 1274-1281. (Pubitemid 28169180)
8. Ju H, Zou R, Venema VJ et al. Direct interaction of endothelial nitric-oxide synthase and caveolin-1 inhibits synthase activity. J Biol Chem 1997; 272: 18522-18525. (Pubitemid 27318186)
9. Kashiwagi M, Shinozaki M, Hirakata H et al. Locally activated reninangiotensin system associated with TGF-beta1 as a major factor for renal injury induced by chronic inhibition of nitric oxide synthase in rats. J Am Soc Nephrol 2000; 11: 616-624. (Pubitemid 30171870)
10. 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. (Pubitemid 30620023)
11. 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.
12. Hohenstein B, Hugo CP, Hausknecht B et al. Analysis of NO-synthase expression and clinical risk factors in human diabetic nephropathy. Nephrol Dial Transplant 2008; 23: 1346-1354. (Pubitemid 351767511)
13. Zhao HJ, Wang S, Cheng H et al. Endothelial nitric oxide synthase deficiency produces accelerated nephropathy in diabetic mice. J Am Soc Nephrol 2006; 17: 2664-2669. (Pubitemid 44484656)
14. Komers R, Anderson S. Glomerular endothelial NOS (eNOS) expression in type 2 diabetic patients with nephropathy. Nephrol Dial Transplant 2008; 23: 3037; author reply 3037-3038.
15. Qi Z, Fujita H, Jin J et al. Characterization of susceptibility of inbred mouse strains to diabetic nephropathy. Diabetes 2005; 54: 2628-2637. (Pubitemid 41233584)
16. Gurley SB, Clare SE, Snow KP et al. Impact of genetic background on nephropathy in diabetic mice. Am J Physiol Renal Physiol 2006; 290: F214-F222.
17. Goldberg IJ, Dansky HM. Diabetic vascular disease: an experimental objective. Arterioscler Thromb Vasc Biol 2006; 26: 1693-1701. (Pubitemid 44305321)
18. Bower G, Brown DM, Steffes MW et al. Studies of the glomerular mesangium and the juxtaglomerular apparatus in the genetically diabetic mouse. Lab Invest 1980; 43: 333-341. (Pubitemid 10008959)
19. Thum T, Fraccarollo D, Schultheiss M et al. Endothelial nitric oxide synthase uncoupling impairs endothelial progenitor cell mobilization and function in diabetes. Diabetes 2007; 56: 666-674. (Pubitemid 46348461)
20. Wu G, Meininger CJ. Nitric oxide and vascular insulin resistance. Biofactors 2009; 35: 21-27.
21. Jin RC, Loscalzo J. Vascular nitric oxide: formation and function. J Blood Med 2010; 2010: 147-162.
22. Baylis C. Nitric oxide deficiency in chronic kidney disease. Am J Physiol Renal Physiol 2008; 294: F1-F9.
23. 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. (Pubitemid 30020428)
24. Mohan S, Reddick RL, Musi N et al. Diabetic eNOS knockout mice develop distinct macro-and microvascular complications. Lab Invest 2008; 88: 515-528. (Pubitemid 351581457)
25. Kanetsuna Y, Takahashi K, Nagata M et al. Deficiency of endothelial nitric-oxide synthase confers susceptibility to diabetic nephropathy in nephropathy-resistant inbred mice. Am J Pathol 2007; 170: 1473-1484. (Pubitemid 47339294)
26. Komers R, Anderson S. Paradoxes of nitric oxide in the diabetic kidney. Am J Physiol Renal Physiol 2003; 284: F1121-F1137. (Pubitemid 36578439)
27. Guzik TJ, Mussa S, Gastaldi D et al. Mechanisms of increased vascular superoxide production in human diabetes mellitus: role of NAD(P)H oxidase and endothelial nitric oxide synthase. Circulation 2002; 105: 1656-1662. (Pubitemid 34298608)
28. Kobayashi T, Taguchi K, Nemoto S et al. Activation of the PDK-1/Akt/eNOS pathway involved in aortic endothelial function differs between hyperinsulinemic and insulin-deficient diabetic rats. Am J Physiol Heart Circ Physiol 2009; 297: H1767-H1775.
29. Liu J, Wei S, Tian L et al. Effects of endomorphins on human umbilical vein endothelial cells under high glucose. Peptides 2011; 32: 86-92.
30. Kim HW, Lim JH, Kim MY et al. Long-term blockade of vascular endothelial growth factor receptor-2 aggravates the diabetic renal dysfunction associated with inactivation of the Akt/eNOS-NO axis. Nephrol Dial Transplant 2011; 26: 1173-1188.
31. Ballermann BJ. Glomerular endothelial cell differentiation. Kidney Int 2005; 67: 1668-1671. (Pubitemid 40577697)
32. Satchell SC, Braet F. Glomerular endothelial cell fenestrations: an integral component of the glomerular filtration barrier. Am J Physiol Renal Physiol 2009; 296: F947-F956.
33. Thomas SR, Witting PK, Drummond GR. Redox control of endothelial function and dysfunction: molecular mechanisms and therapeutic opportunities. Antioxid Redox Signal 2008; 10: 1713-1765.
34. Li H, Wallerath T, Munzel T et al. Regulation of endothelial-type NO synthase expression in pathophysiology and in response to drugs. Nitric Oxide 2002; 7: 149-164. (Pubitemid 35346221)
35. Searles CD. Transcriptional and posttranscriptional regulation of endothelial nitric oxide synthase expression. Am J Physiol Cell Physiol 2006; 291: C803-C816. (Pubitemid 44771801)
36. Luo Z, Fujio Y, Kureishi Y et al. Acute modulation of endothelial Akt/PKB activity alters nitric oxide-dependent vasomotor activity in vivo. J Clin Invest 2000; 106: 493-499. (Pubitemid 30666382)
37. Mount PF, Kemp BE, Power DA. Regulation of endothelial and myocardial NO synthesis by multi-site eNOS phosphorylation. J Mol Cell Cardiol 2007; 42: 271-279. (Pubitemid 46135596)
38. Komers R, Schutzer WE, Reed JF et al. Altered endothelial nitric oxide synthase targeting and conformation and caveolin-1 expression in the diabetic kidney. Diabetes 2006; 55: 1651-1659. (Pubitemid 44324117)
39. Xu J, Xie Z, Reece R et al. Uncoupling of endothelial nitric oxidase synthase by hypochlorous acid: role of NAD(P)H oxidase-derived superoxide and peroxynitrite. Arterioscler Thromb Vasc Biol 2006; 26: 2688-2695.
40. Alp NJ, Channon KM. Regulation of endothelial nitric oxide synthase by tetrahydrobiopterin in vascular disease. Arterioscler Thromb Vasc Biol 2004; 24: 413-420. (Pubitemid 38326132)
41. Munzel T, Daiber A, Ullrich V et al. Vascular consequences of endothelial nitric oxide synthase uncoupling for the activity and expression of the soluble guanylyl cyclase and the cGMP-dependent protein kinase. Arterioscler Thromb Vasc Biol 2005; 25: 1551-1557. (Pubitemid 41098921)
42. Schmidt TS, Alp NJ. Mechanisms for the role of tetrahydrobiopterin in endothelial function and vascular disease. Clin Sci (Lond) 2007; 113: 47-63. (Pubitemid 47066025)
43. Meininger CJ, Marinos RS, Hatakeyama K et al. Impaired nitric oxide production in coronary endothelial cells of the spontaneously diabetic BB rat is due to tetrahydrobiopterin deficiency. Biochem J 2000; 349: 353-356. (Pubitemid 30440201)
44. Kohli R, Meininger CJ, Haynes TE et al. Dietary L-arginine supplementation enhances endothelial nitric oxide synthesis in streptozotocin-induced diabetic rats. J Nutr 2004; 134: 600-608. (Pubitemid 38298503)
45. Pannirselvam M, Simon V, Verma S et al. Chronic oral supplementation with sepiapterin prevents endothelial dysfunction and oxidative stress in small mesenteric arteries from diabetic (db/db) mice. Br J Pharmacol 2003; 140: 701-706. (Pubitemid 37386434)
46. Heitzer T, Krohn K, Albers S et al. Tetrahydrobiopterin improves endothelium-dependent vasodilation by increasing nitric oxide activity in patients with Type II diabetes mellitus. Diabetologia 2000; 43: 1435-1438.
47. Ferre J, Naylor EW. Sepiapterin reductase in human amniotic and skin fibroblasts, chorionic villi, and various blood fractions. Clin Chim Acta 1988; 174: 271-282.
48. Coronel I, Arellano-Mendoza MG, del Valle-Mondragon L et al. L-arginine and antioxidant diet supplementation partially restores nitric oxide-dependent regulation of phenylephrine renal vasoconstriction in diabetics rats. J Ren Nutr 2010; 20: 158-168.
49. Bello E, Caramelo C, Martell N et al. Impairment of renal vasodilation with l-arginine is related to more severe disease in untreated hypertensive patients. Hypertension 2001; 38: 907-912. (Pubitemid 34258691)
50. Burton BK, Nowacka M, Hennermann JB et al. Safety of extended treatment with sapropterin dihydrochloride in patients with phenylketonuria: results of a phase 3b study. Mol Genet Metab 2011; 103: 315-322.
51. Puff R, Dames P, Weise M et al. Reduced proliferation and a high apoptotic frequency of pancreatic beta cells contribute to genetically- determined diabetes susceptibility of db/db BKS mice. Horm Metab Res 2011; 43: 306-311.
52. Leiter EH, Le PH, Coleman DL. Susceptibility to db gene and streptozotocin-induced diabetes in C57BL mice: control by genderassociated, MHC-unlinked traits. Immunogenetics 1987; 26: 6-13. (Pubitemid 17096981)
53. Morrow JD, Roberts 2nd LJ. Mass spectrometric quantification of F2-isoprostanes in biological fluids and tissues as measure of oxidant stress. Methods Enzymol 1999; 300: 3-12. (Pubitemid 28500576)
54. Morrow JD, Zackert WE, Yang JP et al. Quantification of the major urinary metabolite of 15-F2t-isoprostane (8-iso-PGF2alpha) by a stable isotope dilution mass spectrometric assay. Anal Biochem 1999; 269: 326-331. (Pubitemid 29201031)
55. Takemoto M, Asker N, Gerhardt H et al. A new method for large scale isolation of kidney glomeruli from mice. Am J Pathol 2002; 161: 799-805. (Pubitemid 34988366)
56. Akis N, Madaio MP. Isolation, culture, and characterization of endothelial cells from mouse glomeruli. Kidney Int 2004; 65: 2223-2227. (Pubitemid 38670008)
57. Korda M, Kubant R, Patton S et al. Leptin-induced endothelial dysfunction in obesity. Am J Physiol Heart Circ Physiol 2008; 295: H1514-H1521.
58. Cheng HF, Harris RC. Cyclooxygenase-2 expression in cultured cortical thick ascending limb of henle increases in response to decreased extracellular ionic content by both transcriptional and post-transcriptional mechanisms. Role of p38-mediated pathways. J Biol Chem 2002; 277: 45638-45643. (Pubitemid 36159175)
59. Chen S, Apostolova MD, Cherian MG et al. Interaction of endothelin-1 with vasoactive factors in mediating glucose-induced increased permeability in endothelial cells. Lab Invest 2000; 80: 1311-1321. (Pubitemid 30637071)
60. Bonner SM, O'Sullivan MA. Endothelial cell monolayers as a model system to investigate dengue shock syndrome. J Virol Methods 1998; 71: 159-167. (Pubitemid 28196170)