Ratio of 5,6,7,8-tetrahydrobiopterin to 7,8-dihydrobiopterin in endothelial cells determines glucose-elicited changes in NO vs. superoxide production by eNOS

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 294, Issue 4, 2008, Pages

  Crabtree, Mark J ^a   Smith, Caroline L ^a   Lam, George ^a   Goligorsky, Michael S ^b   Gross, Steven S ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b NEW YORK MEDICAL COLLEGE   (United States)

Author keywords

Diabetes; Endothelial dysfunction; Nitric oxide

Indexed keywords

BIOPTERIN; CALCIUM IONOPHORE; DIHYDROBIOPTERIN; ENDOTHELIAL NITRIC OXIDE SYNTHASE; GLUCOSE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE INHIBITOR; SUPEROXIDE; TETRAHYDROBIOPTERIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; CATALYSIS; CELLULAR DISTRIBUTION; COMPLEX FORMATION; CONTROLLED STUDY; CORRELATION ANALYSIS; DIABETES MELLITUS; ENDOTHELIAL DYSFUNCTION; ENDOTHELIUM CELL; ENZYME ACTIVITY; HYPERGLYCEMIA; IN VIVO STUDY; INFLAMMATION; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OXIDATION; PRIORITY JOURNAL; RAT; ZUCKER DIABETIC FATTY RAT;

ANIMALS; BIOPTERIN; BLOOD GLUCOSE; CELL LINE; DIABETES MELLITUS, TYPE 2; DISEASE MODELS, ANIMAL; ENDOTHELIAL CELLS; ENZYME INHIBITORS; GLUCOSE; GLUTATHIONE; MICE; MITOCHONDRIA; NG-NITROARGININE METHYL ESTER; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; OXIDATION-REDUCTION; PROTEIN BINDING; RATS; RATS, ZUCKER; SUPEROXIDES; TIME FACTORS; TRITIUM;

EID: 41849144894     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00823.2007     Document Type: Article

References (61)

1. Alp NJ, Channon KM. Regulation of endothelial nitric oxide synthase by tetrahydrobiopterin in vascular disease. Arterioscler Thromb Vasc Biol 24: 413-420, 2004.
2. Antoniades C, Shirodaria C, Crabtree M, Rinze R, Alp N, Cunnington C, Diesch J, Tousoulis D, Stefanadis C, Leeson P, Ratnatunga C, Pillai R, Channon KM. Altered plasma versus vascular biopterins in human atherosclerosis reveal relationships between endothelial nitric oxide synthase coupling, endothelial function, and inflammation. Circulation 116: 2851-2859, 2007.
3. Bitar MS, Wahid S, Mustafa S, Al-Saleh E, Dhaunsi GS, Al-Mulla F. Nitric oxide dynamics and endothelial dysfunction in type II model of genetic diabetes. Eur J Pharmacol 511: 53-64, 2005.
4. Britten MB, Zeiher AM, Schachinger V. Effects of cardiovascular risk factors on coronary artery remodeling in patients with mild atherosclerosis. Coron Artery Dis 14: 415-422, 2003.
5. Brodsky SV, Gealekman O, Chen J, Zhang F, Togashi N, Crabtree M, Gross SS, Nasjletti A, Goligorsky MS. Prevention and reversal of premature endothelial cell senescence and vasculopathy in obesity-induced diabetes by ebselen. Circ Res 94: 377-384, 2004.
6. Brownlee M. Biochemistry and molecular cell biology of diabetic complications. Nature 414: 813-820, 2001.
7. 4 by gene transfer restores nitric oxide synthase function in hyperglycemic human endothelial cells. Cardiovasc Res 65: 823-831, 2005.
8. Chander PN, Gealekman O, Brodsky SV, Elitok S, Tojo A, Crabtree M, Gross SS, Goligorsky MS. Nephropathy in Zucker diabetic fat rat is associated with oxidative and nitrosative stress: prevention by chronic therapy with a peroxynitrite scavenger ebselen. J Am Soc Nephrol 15: 2391-2403, 2004.
9. d'Uscio LV, Milstien S, Richardson D, Smith L, Katusic ZS. Long-term vitamin C treatment increases vascular tetrahydrobiopterin levels and nitric oxide synthase activity. Circ Res 92: 88-95, 2003.
10. Davis MD, Kaufman S, Milstien S. The auto-oxidation of tetrahydrobiopterin. Eur J Biochem 173: 345-351, 1988.
11. Drexler H, Hornig B. Endothelial dysfunction in human disease. J Mol Cell Cardiol 31: 51-60, 1999.
12. Gori T, Burstein JM, Ahmed S, Miner SE, Al-Hesayen A, Kelly S, Parker JD. Folic acid prevents nitroglycerin-induced nitric oxide synthase dysfunction and nitrate tolerance: a human in vivo study. Circulation 104: 1119-1123, 2001.
13. Griffith OW. Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine. Anal Biochem 106: 207-212, 1980.
14. Gross SS, Jaffe EA, Levi R, Kilbourn RG. Cytokine-activated endothelial cells express an isotype of nitric oxide synthase which is tetrahydrobiopterin-dependent, calmodulin-independent and inhibited by arginine analogs with a rank-order of potency characteristic of activated macrophages. Biochem Biophys Res Commun 178: 823-829, 1991.
15. Heales S, Hyland K. Determination of quinonoid dihydrobiopterin by high-performance liquid chromatography and electrochemical detection. J Chromatogr 494: 77-85, 1989.
16. Heerdt PM, Holmes JW, Cai B, Barbone A, Madigan JD, Reiken S, Lee DL, Oz MC, Marks AR, Burkhoff D. Chronic unloading by left ventricular assist device reverses contractile dysfunction and alters gene expression in end-stage heart failure. Circulation 102: 2713-2719, 2000.
17. Heitzer T, Brockhoff C, Mayer B, Warnholtz A, Mollnau H, Henne S, Meinertz T, Munzel T. Tetrahydrobiopterin improves endothelium-dependent vasodilation in chronic smokers : evidence for a dysfunctional nitric oxide synthase. Circ Res 86: E36-41, 2000.
18. Heitzer T, Schlinzig T, Krohn K, Meinertz T, Munzel T. Endothelial dysfunction, oxidative stress, and risk of cardiovascular events in patients with coronary artery disease. Circulation 104: 2673-2678, 2001.
19. Higashi Y, Sasaki S, Nakagawa K, Fukuda Y, Matsuura H, Oshima T, Chayama K. Tetrahydrobiopterin enhances forearm vascular response to acetylcholine in both normotensive and hypertensive individuals. Am J Hypertens 15: 326-332, 2002.
20. Higman DJ, Strachan AM, Buttery L, Hicks RC, Springall DR, Greenhalgh RM, Powell JT. Smoking impairs the activity of endothelial nitric oxide synthase in saphenous vein. Arterioscler Thromb Vasc Biol 16: 546-552, 1996.
21. Huang A, Vita JA, Venema RC, Keaney JF Jr. Ascorbic acid enhances endothelial nitric-oxide synthase activity by increasing intracellular tetrahydrobiopterin. J Biol Chem 275: 17399-17406, 2000.
22. Huie RE, Padmaja S. The reaction of NO with superoxide. Free Radic Res Commun 18: 195-199, 1993.
23. Hurshman AR, Krebs C, Edmondson DE, Huynh BH, Marletta MA. Formation of a pterin radical in the reaction of the heme domain of inducible nitric oxide synthase with oxygen. Biochemistry 38: 15689-15696, 1999.
24. Ishii K, Sheng H, Warner TD, Forstermann U, Murad F. A simple and sensitive bioassay method for detection of EDRF with RFL-6 rat lung fibroblasts. Am J Physiol Heart Circ Physiol 261: H598-H603, 1991.
25. Kirsch M, Korth HG, Stenert V, Sustmann R, de Groot H. The autoxidation of tetrahydrobiopterin revisited. Proof of superoxide formation from reaction of tetrahydrobiopterin with molecular oxygen. J Biol Chem 278: 24481-24490, 2003.
26. Kuzkaya N, Weissmann N, Harrison DG, Dikalov S. Interactions of peroxynitrite, tetrahydrobiopterin, ascorbic acid, and thiols: implications for uncoupling endothelial nitric-oxide synthase. J Biol Chem 278: 22546-22554, 2003.
27. Kwon NS, Nathan CF, Stuehr DJ. Reduced biopterin as a cofactor in the generation of nitrogen oxides by murine macrophages. J Biol Chem 264: 20496-20501, 1989.
28. Landmesser U, Dikalov S, Price SR, McCann L, Fukai T, Holland SM, Mitch WE, Harrison DG. Oxidation of tetrahydrobiopterin leads to uncoupling of endothelial cell nitric oxide synthase in hypertension. J Clin Invest 111: 1201-1209, 2003.
29. Laursen JB, Somers M, Kurz S, McCann L, Warnholtz A, Freeman BA, Tarpey M, Fukai T, Harrison DG. Endothelial regulation of vasomotion in apoE-deficient mice: implications for interactions between peroxynitrite and tetrahydrobiopterin. Circulation 103: 1282-1288, 2001.
30. Li H, Brodsky S, Kumari S, Valiunas V, Brink P, Kaide J, Nasjletti A, Goligorsky MS. Paradoxical overexpression and translocation of connexin43 in homocysteine-treated endothelial cells. Am J Physiol Heart Circ Physiol 282: H2124-H2133, 2002.
31. Martasek P, Liu Q, Liu J, Roman LJ, Gross SS, Sessa WC, Masters BS. Characterization of bovine endothelial nitric oxide synthase expressed in E. coli. Biochem Biophys Res Commun 219: 359-365, 1996.
32. McMillan K, Bredt DS, Hirsch DJ, Snyder SH, Clark JE, Masters BS. Cloned, expressed rat cerebellar nitric oxide synthase contains stoichiometric amounts of heme, which binds carbon monoxide. Proc Natl Acad Sci USA 89: 11141-11145, 1992.
33. Meininger CJ, Marinos RS, Hatakeyama K, Martinez-Zaguilan R, Rojas JD, Kelly KA, Wu G. Impaired nitric oxide production in coronary endothelial cells of the spontaneously diabetic BB rat is due to tetrahydrobiopterin deficiency. Biochem J 349: 353-356, 2000.
34. Milstien S, Katusic Z. Oxidation of tetrahydrobiopterin by peroxynitrite: implications for vascular endothelial function. Biochem Biophys Res Commun 263: 681-684, 1999.
35. Nishikawa T, Edelstein D, Du XL, Yamagishi S, Matsumura T, Kaneda Y, Yorek MA, Beebe D, Oates PJ, Hammes HP, Giardino I, Brownlee M. Normalizing mitochondrial superoxide production blocks three pathways of hyperglycaemic damage. Nature 404: 787-790, 2000.
36. Ono S, Ichikura T, Mochizuki H. [The pathogenesis of the systemic inflammatory response syndrome and compensatory antiinflammatory response syndrome following surgical stress]. Nippon Geka Gakkai Zasshi 104: 499-505, 2003.
37. Pieper GM, Siebeneich W, Moore-Hilton G, Roza AM. Reversal by L-arginine of a dysfunctional arginine/nitric oxide pathway in the endothelium of the genetic diabetic BB rat. Diabetologia 40: 910-915, 1997.
38. 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.
39. Sawabe K, Wakasugi KO, Hasegawa H. Tetrahydrobiopterin uptake in supplemental administration: elevation of tissue tetrahydrobiopterin in mice following uptake of the exogenously oxidized product 7,8-dihydrobiopterin and subsequent reduction by an anti-folate-sensitive process. J Pharmacol Sci 96: 124-133, 2004.
40. Schachinger V, Britten MB, Zeiher AM. Prognostic impact of coronary vasodilator dysfunction on adverse long-term outcome of coronary heart disease. Circulation 101: 1899-1906, 2000.
41. Schmidt TS, Alp NJ. Mechanisms for the role of tetrahydrobiopterin in endothelial function and vascular disease. Clin Sci (Lond) 113: 47-63, 2007.
42. Schock BC, Van der Vliet A, Corbacho AM, Leonard SW, Finkelstein E, Valacchi G, Obermueller-Jevic U, Cross CE, Traber MG. Enhanced inflammatory responses in alpha-tocopherol transfer protein null mice. Arch Biochem Biophys 423: 162-169, 2004.
43. Setoguchi S, Hirooka Y, Eshima K, Shimokawa H, Takeshita A. Tetrahydrobiopterin improves impaired endothelium-dependent forearm vasodilation in patients with heart failure. J Cardiovasc Pharmacol 39: 363-368, 2002.
44. Shinozaki K, Nishio Y, Okamura T, Yoshida Y, Maegawa H, Kojima H, Masada M, Toda N, Kikkawa R, Kashiwagi A. Oral administration of tetrahydrobiopterin prevents endothelial dysfunction and vascular oxidative stress in the aortas of insulin-resistant rats. Circ Res 87: 566-573, 2000.
45. Srinivasan S, Hatley ME, Bolick DT, Palmer LA, Edelstein D, Brownlee M, Hedrick CC. Hyperglycaemia-induced superoxide production decreases eNOS expression via AP-1 activation in aortic endothelial cells. Diabetologia 47: 1727-1734, 2004.
46. Stroes E, Kastelein J, Cosentino F, Erkelens W, Wever R, Koomans H, Luscher T, Rabelink T. Tetrahydrobiopterin restores endothelial function in hypercholesterolemia. J Clin Invest 99: 41-46, 1997.
47. Tayeh MA, Marletta MA. Macrophage oxidation of L-arginine to nitric oxide, nitrite, and nitrate. Tetrahydrobiopterin is required as a cofactor. J Biol Chem 264: 19654-19658, 1989.
48. Tiefenbacher CP, Chilian WM, Mitchell M, DeFily DV. Restoration of endothelium-dependent vasodilation after reperfusion injury by tetrahydrobiopterin. Circulation 94: 1423-1429, 1996.
49. Tsutsui M, Milstien S, Katusic ZS. Effect of tetrahydrobiopterin on endothelial function in canine middle cerebral arteries. Circ Res 79: 336-342, 1996.
50. Vasquez-Vivar J, Duquaine D, Whitsett J, Kalyanaraman B, Rajagopalan S. Altered tetrahydrobiopterin metabolism in atherosclerosis: implications for use of oxidized tetrahydrobiopterin analogues and thiol antioxidants. Arterioscler Thromb Vasc Biol 22: 1655-1661, 2002.
51. Vasquez-Vivar J, Kalyanaraman B, Martasek P, Hogg N, Masters BS, Karoui H, Tordo P, Pritchard KA Jr. Superoxide generation by endothelial nitric oxide synthase: the influence of cofactors. Proc Natl Acad Sci USA 95: 9220-9225, 1998.
52. Vasquez-Vivar J, Martasek P, Whitsett J, Joseph J, Kalyanaraman B. The ratio between tetrahydrobiopterin and oxidized tetrahydrobiopterin analogues controls superoxide release from endothelial nitric oxide synthase: an EPR spin trapping study. Biochem J 362: 733-739, 2002.
53. Vasquez-Vivar J, Whitsett J, Martasek P, Hogg N, Kalyanaraman B. Reaction of tetrahydrobiopterin with superoxide: EPR-kinetic analysis and characterization of the pteridine radical. Free Radic Biol Med 31: 975-985, 2001.
54. Warnholtz A, Wendt M, August M, Munzel T. Clinical aspects of reactive oxygen and nitrogen species. Biochem Soc Symp: 121-133, 2004.
55. Weissman BA, Gross SS. Measurement of NO and NO Synthase. New York: Wiley, 1998.
56. Williams RL, Courtneidge SA, Wagner EF. Embryonic lethalities and endothelial tumors in chimeric mice expressing polyoma virus middle T oncogene. Cell 52: 121-131, 1988.
57. Wolff DJ, Datto GA, Samatovicz RA. The dual mode of inhibition of calmodulin-dependent nitric-oxide synthase by antifungal imidazole agents. J Biol Chem 268: 9430-9436, 1993.
58. Yetik-Anacak G, Catravas JD. Nitric oxide and the endothelium: history and impact on cardiovascular disease. Vascul Pharmacol 45: 268-276, 2006.
59. Yoshida A, Pozdnyakov N, Dang L, Orselli SM, Reddy VN, Sitaramayya A. Nitric oxide synthesis in retinal photoreceptor cells. Vis Neurosci 12: 493-500, 1995.
60. Zanetti M, Sato J, Katusic ZS, O'Brien T. Gene transfer of endothelial nitric oxide synthase alters endothelium-dependent relaxations in aortas from diabetic rabbits. Diabetologia 43: 340-347, 2000.
61. Zou MH, Shi C, Cohen RA. Oxidation of the zinc-thiolate complex and uncoupling of endothelial nitric oxide synthase by peroxynitrite. J Clin Invest 109: 817-826, 2002.