The two faces of endothelial nitric oxide synthase in the pathophysiology of atherosclerosis

Endothelium: Journal of Endothelial Cell Research

Volumn 11, Issue 2, 2004, Pages 99-107

  Kawashima, Seinosuke ^a  

^a KOBE UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Atherosclerosis; BH4; Endothelial nitric oxide synthase; Nitric oxide; Superoxide

Indexed keywords

ARGININE; ASCORBIC ACID; BIOPTERIN; CITRULLINE; DIHYDROBIOPTERIN; ENDOTHELIAL NITRIC OXIDE SYNTHASE; ENDOTHELIUM DERIVED RELAXING FACTOR; HYDRALAZINE; MESSENGER RNA; N(G) NITROARGININE METHYL ESTER; N(G),N(G) DIMETHYLARGININE; NITRIC OXIDE; OXIDIZED LOW DENSITY LIPOPROTEIN; PTERIDINE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SEPIAPTERIN; SEX HORMONE; SUPEROXIDE; SUPEROXIDE DISMUTASE; TETRAHYDROBIOPTERIN;

ANTIOXIDANT ACTIVITY; ATHEROGENESIS; ATHEROSCLEROSIS; DIABETES MELLITUS; ENDOTHELIUM LESION; ENZYME ACTIVITY; ENZYME METABOLISM; HUMAN; HYPERTENSION; NONHUMAN; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PRIORITY JOURNAL; REVIEW; VASCULAR DISEASE; VASCULAR ENDOTHELIUM;

ANIMALS; ARTERIOSCLEROSIS; BIOPTERIN; HUMANS; NITRIC OXIDE SYNTHASE; SUPEROXIDES;

EID: 4444376995     PISSN: 10623329     EISSN: None     Source Type: Journal    
DOI: 10.1080/10623320490482637     Document Type: Review

References (87)

1. Aji W., Ravalli S., Szabolcs M., Jiang X.C., Sciacca R.R., Michler R.E., and Cannon P.J. (1997) L-Arginine prevents xanthoma development and inhibits atherosclerosis in LDL receptor knockout mice. Circulation, 95, 430-437.
2. Alp N.J., and Channon K.M. (2003) Nitric oxide bioactivity in apo E-/- mice is manitained by increased tetrahydrobiopterin synthesis via targeted GTP cyclohydlase-1 over expression. Circulation, 108, IV-39 (suppl).
3. Alp N.J., and Channon K.M. (2004) Regulation of endothelial nitric oxide synthase by tetrahydrobiopterin in vascular disease. Arteriosclerosis, Thrombosis, and Vascular Biology, 24, 1-9.
4. Alp N.J., Mussa S., Khoo J., Cai S., Guzik T., Jefferson A., Goh N., Rockett K.A., and Channon K.M. (2003) Tetrahydrobiopterin-dependent preservation of nitric oxide-mediated endothelial function in diabetes by targeted transgenic GTP-cyclohydrolase I overexpression. Journal of Clinical Investigation, 112, 725-735.
5. Amano K., Matsubara H., Iba O., Okigaki M., Fujiyama S., Imada T., Kojima H., Nozawa Y., Kawashima S., Yokoyama M., and Iwasaka T. (2003) Enhancement of ischemia-induced angiogenesis by eNOS overexpression. Hypertension, 41, 156-162.
6. Avogaro A., Piarulli F., Valerio A., Miola M., Calveri M., Pavan P., Vicini P., Cobelli C., Tiengo A., Calo L., and Del Prato S. (1997) Forearm nitric oxide balance, vascular relaxation, and glucose metabolism in NIDDM patients. Diabetes, 46, 1040-1046.
7. Azumi H., Inoue N., Ohashi Y., Terashima M., Mori T., Fujita H., Awano K., Kobayashi K., Maeda K., Hata K., Shinke T., Kobayashi S., Hirata K., Kawashima S., Itabe H., Hayashi Y., Imajoh-Ohmi S., Itoh H., and Yokoyama M. (2002) Superoxide generation in directional coronary atherectomy specimens of patients with angina pectoris: Important role of NAD(P)H oxidase. Arteriosclerosis, Thrombosis, and Vascular Biology, 22, 1838-1844.
8. Azumi H., Inoue N., Takeshita S., Rikitake Y., Kawashima S., Hayashi Y., Itoh H., and Yokoyama M. (1999) Expression of NADH/NADPH oxidase p22phox in human coronary arteries. Circulation, 100, 1494-1498.
9. Beckman J.A., Goldfine A.B., Gordon M.B., and Creager M.A. (2001) Ascorbate restores endothelium-dependent vasodilation impaired by acute hyperglycemia in humans. Circulation, 103, 1618-1623.
10. Cai H., and Harrison D.G. (2000) Endothelial dysfunction in cardiovascular diseases: The role of oxidant stress. Circulation Research, 87, 840-844.
11. Chan S.Y., Mancini G.B., Kuramoto L., Schulzer M., Frohlich J., and Ignaszewski A. (2003) The prognostic importance of endothelial dysfunction and carotid atheroma burden in patients with coronary artery disease. Journal of American College of Cardiology, 42, 1037-1043.
12. Chen J., Kuhlencordt P.J., Astern J., Gyurko R., and Huang P.L. (2001) Hypertension does not account for the accelerated atherosclerosis and development of aneurysms in male apolipoprotein e/endothelial nitric oxide synthase double knockout mice. Circulation, 104, 2391-2394.
13. Cooke J.P. (2000) Does ADMA cause endothelial dysfunction? Arteriosclerosis, Thrombosis, and Vascular Biology, 20, 2032-2037.
14. Cooke J.P., Singer A.H., Tsao P., Zera P., Rowan R.A., and Billingham M.E. (1992) Antiatherogenic effects of L-arginine in the hypercholesterolemic rabbit. Journal of Clinical Investigation, 90, 1168-1172.
15. Cosentino F., and Luscher T.F. (1999) Tetrahydrobiopterin and endothelial nitric oxide synthase activity. Cardiovascular Research, 43, 274-278.
16. Creager M.A., Cooke J.P., Mendelsohn M.E., Gallagher S.J., Coleman S.M., Loscalzo J., and Dzau V.J. (1990) Impaired vasodilation of forearm resistance vessels in hypercholesterolemic humans. Journal of Clinical Investigation, 86, 228-234.
17. De Caterina R., Libby P., Peng H.B., Thannickal V.J., Rajavashisth T.B., Gimbrone M.A. Jr., Shin W.S., and Liao J.K. (1995) Nitric oxide decreases cytokine-induced endothelial activation. Nitric oxide selectively reduces endothelial expression of adhesion molecules and proinflammatory cytokines. Journal of Clinical Investigation, 96, 60-68.
18. Drexler H. (1997) Endothelial dysfunction: Clinical implications. Progress in Cardiovascular Diseases, 39, 287-324.
19. d'Uscio L.V., Milstien S., Richardson D., Smith L., and Katusic Z.S. (2003) Long-term vitamin C treatment increases vascular tetrahydrobiopterin levels and nitric oxide synthase activity. Circulation Research, 92, 88-95.
20. d'Uscio L.V., Smith L.A., and Katusic Z.S. (2001) Hypercholesterolemia impairs endotheliumdependent relaxations in common carotid arteries of apolipoprotein E-deficient mice. Stroke, 32, 2658-2664.
21. Felmayer-Werner G., Werner E.R., Fuchs D., Hausen A., Reibnegger G., Schmidt K., Weiss G., and Wachter H. (1993) Pteridine biosynthesis in human endothelial cells. Journal of Biological Chemistry, 268, 1842-1846.
22. Feron O., Dessy C., Moniotte S., Desager J.P., and Balligand J.L. (1999) Hypercholesterolemia decreases nitric oxide production by promoting the interaction of caveolin and endothelial nitric oxide synthase. Journal of Clinical Investigation, 103, 897-905.
23. Griendling K.K., Sorescu D., and Ushio-Fukai M. (2000) NAD(P)H oxidase: role in cardiovascular biology and disease. Circulation Research, 86, 494-501.
24. Halcox J.P., Schenke W.H., Zalos G., Mincemoyer R., Prasad A., Waclawiw M.A., Nour K.R., and Quyyumi A.A. (2002) Prognostic value of coronary vascular endothelial dysfunction. Circulation, 106, 653-658.
25. Harrison D.G. (1997) Cellular and molecular mechanisms of endothelial cell dysfunction. Journal of Clinical Investigation, 100, 2153-2157.
26. Harrison D., Griendling K.K., Landmesser U., Hornig B., and Drexler H. (2003) Role of oxidative stress in atherosclerosis. American Journal of Cardiology, 91(3A), 7A-11A.
27. Hathaway C.A., Heistad D.D., Piegors D.J., and Miller F.J. Jr. (2002) Regression of atherosclerosis in monkeys reduces vascular superoxide levels. Circulation Research, 90, 277-283.
28. Hattori Y., Nakanishi N., Akimoto K., Yoshida M., and Kasai K. (2003) HMG-CoA reductase inhibitor increases GTP cyclohydrolase 1 mRNA and tetrahydrobippterin in vascular endothelial cells. Arteriosclerosis, Thrombosis, and Vascular Biology, 23, 176-182.
29. Heitzer T., Brockhoff C., Mayer B., Warnholtz A., Mollnau H., Henne S., Meinertz T., and Munzel T. (2000) Tetrahydrobiopterin improves endothelium-dependent vasodilation in chronic smokers: Evidence for a dysfunctional nitric oxide synthase. Circulation Research, 86, E36-E41.
30. Hirata K., Akita H., and Yokoyama M. (1991) Oxidized low density lipoprotein inhibits bradykinin-induced phosphoinositide hydrolysis in cultured bovine aortic endothelial cells. FEBS Letters, 287, 181-184.
31. Hodgin J.B., Knowles J.W., Kim H.S., Smithies O., and Maeda N. (2002) Interactions between endothelial nitric oxide synthase and sex hormones in vascular protection in mice. Journal of Clinical Investigation, 109, 541-548.
32. Inoue N., Kawashima S., Kanazawa K., Yamada S., Akita H., and Yokoyama M. (1998) Polymorphism of the NADH/NADPH oxidase p22 phox gene in patients with coronary artery disease. Circulation, 97, 135-137.
33. Kanazawa K., Kawashima S., Mikami S., Miwa Y., Hirata K., Suematsu M., Hayashi Y., Itoh H., and Yokoyama M. (1996) Endothelial constitutive nitric oxide synthase protein and mRNA increased in rabbit atherosclerotic aorta despite impaired endothelium-dependent vascular relaxation. American Journal of Pathology, 148, 1949-1956.
34. Katusic Z.S. (2001) Vascular endothelial dysfunction: Does tetrahydrobiopterin play a role? American Journal of Physiology Heart and Circulatory Physiology, 281, H981-H986.
35. Kauser K., da Cunha V., Fitch R., Mallari C., and Rubanyi G.M. (2000) Role of endogenous nitric oxide in progression of atherosclerosis in apolipoprotein E-deficient mice. American Journal of Physiology Heart and Circulatory Physiology, 278, H1679-H1685.
36. Kawashima S., Yamashita T., Ozaki M., Ohashi Y., Azumi H., Inoue N., Hirata K., Hayashi Y., Itoh H., and Yokoyama M. (2001) Endothelial NO synthase overexpression inhibits lesion formation in mouse model of vascular remodeling. Arteriosclerosis, Thrombosis, and Vascular Biology, 21, 201-207.
37. Knowles J.W., Reddick R.L., Jennette J.C., Shesely E.G., Smithies O., and Maeda N. (2000) Enhanced atherosclerosis and kidney dysfunction in eNOS(-/-)Apoe(-/-) mice are ameliorated by enalapril treatment. Journal of Clinical Investigation, 105, 451-458.
38. Kuhlencordt P.J., Gyurko R., Han F., Scherrer-Crosbie M., Aretz T.H., Hajjar R., Picard M.H., and Huang P.L. (2001) Accelerated atherosclerosis, aortic aneurysm formation, and ischemic heart disease in apolipoprotein E/endothelial nitric oxide synthase doubleknockout mice. Circulation, 104, 448-454.
39. Kuzkaya N., Weissmann N., Harrison D.G., and Dikalov S. (2003) Interactions of peroxynitrite, tetrahydrobiopterin, ascorbic acid, and thiols: Implications for uncoupling endothelial nitric-oxide synthase. Journal of Biological Chemistry, 278, 22546-22554.
40. Lam K.K., Ho S.T., and Yen M.H. (2002) Tetrahydrobiopterin improves vascular endothelial function in ovariectomized rats. Journal Biomedical Science, 9, 119-125.
41. Landmesser U., Dikalov S., Price S.R., McCann L., Fukai T., Holland S.M., Mitch W.E., and Harrison D.G. (2003) Oxidation of tetrahydrobiopterin leads to uncoupling of endothelial cell nitric oxide synthase in hypertension. Journal of Clinical Investigation, 111, 1201-1209.
42. Laursen J.B., Somers M., Kurz S., McCann L., Warnholtz A., Freeman B.A., Tarpey M., Fukai T., and Harrison D.G. (2001) Endothelial regulation of vasomotion in apoE-deficient mice: Implications for interactions between peroxynitrite and tetrahydrobiopterin. Circulation, 103, 1282-1288.
43. Lloyd-Jones D.M., and Bloch K.D. (1996) The vascular biology of nitric oxide and its role in atherogenesis. Annual Reviews in Medicine, 47, 365-375.
44. Mayer B., and Werner E.R. (1995) In search of a function for tetrahydrobiopterin in the biosynthesis of nitric oxide. Naunyn-Schmiedebergs Archives of Pharmacology, 351, 453-463.
45. Meininger C.J., Marinos R.S., Hatakeyama K., Martinez-Zaguilan R., Rojas J.D., Kelly K.A., and Wu G. (2000) Impaired nitric oxide production in coronary endothelial cells of the spontaneously diabetic BB rat is due to tetrahydrobiopterin deficiency. Biochemical Journal, 349, 353-356.
46. 2+ mobilization in intact endothelial cells of rabbit aorta. Arteriosclerosis, Thrombosis, and Vascular Biology, 17, 1561-1567.
47. Moncada S., and Higgs A. (1993) The L-arginine-nitric oxide pathway. New England Journal of Medicine, 329, 2002-2012.
48. Moncada S., Palmer R.M., and Higgs E.A. (1991) Nitric oxide: Physiology, pathophysiology, and pharmacology. Pharmacological Reviews, 43, 109-142.
49. Mugge A., Elwell J.H., Peterson T.E., Hofmeyer T.G., Heistad D.D., and Harrison D.G. (1991) Chronic treatment with polyethylene-glycolated superoxide dismutase partially restores endothelium-dependent vascular relaxations in cholesterol-fed rabbits. Circulation Research, 69, 1293-1300.
50. Nathan C., and Xie Q.-W. (1994) Regulation of biosynthesis of nitric oxide. Journal of Biological Chemistry, 269, 13725-13728.
51. Oemar B.S., Tschudi M.R., Godoy N., Brovkovich V., Malinski T., and Luscher T.F. (1998) Reduced endothelial nitric oxide synthase expression and production in human atherosclerosis. Circulation, 97, 2494-2498.
52. Ohara Y., Peterson T.E., and Harrison D.G. (1993) Hypercholesterolemia increases endothelial superoxide anion production. Journal of Clinical Investigation, 91, 2546-2551.
53. Ohara Y., Peterson T.E., Sayegh H.S., Subramanian R.R., Wilcox J.N., and Harrison D.G. (1995) Dietary correction of hypercholesterolemia in the rabbit normalizes endothelial superoxide anion production. Circulation, 92, 898-903.
54. Ohashi Y., Kawashima S., Hirata K., Yamashita T., Ishida T., Inoue N., Sakoda T., Kurihara H., Yazaki Y., and Yokoyama M. (1998) Hypotension and reduced nitric oxide-elicited vasorelaxation in transgenic mice overexpressing endothelial nitric oxide synthase. Journal of Clinical Investigation, 102, 2061-2071.
55. Ozaki M., Kawashima S., Yamashita T., Hirase T., Namiki M., Inoue N., Hirata K., Yasui H., Sakurai H., Yoshida Y., Masada M., and Yokoyama M. (2002) Overexpression of endothelial nitric oxide synthase accelerates atherosclerotic lesion formation in apoE-deficient mice. Journal of Clinical Investigation, 110, 331-340.
56. Palmer R.M., Ferrige A.G., and Moncada S. (1987) Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor. Nature, 327, 524-526.
57. Pou S., Pou W.S., Predt D.S., Snyder S.H., and Rosen G.M. (1992) Generation of superoxide by purified brain nitric oxide synthase. Journal of Biological Chemistry, 267, 24173-24176.
58. Quyyumi A.A. (2003) Prognostic value of endothelial function. American Journal of Cardiology, 91, 19H-24H.
59. Rikitake Y., Kawashima S., Takeshita S., Yamashita T., Azumi H., Yasuhara M., Nishi H., Inoue N., and Yokoyama M. (2001) Anti-oxidative properties of fluvastatin, an HMG-CoA reductase inhibitor, contribute to prevention of atherosclerosis in cholesterol-fed rabbits. Atherosclerosis, 154, 87-96.
60. Sarkar R., Meinberg E.G., Stanley J.C., Gordon D., and Webb R.C. (1996) Nitric oxide reversibly inhibits the migration of cultured vascular smooth muscle cells. Circulation Research, 78, 225-230.
61. Schmidt K., Werner E.R., Mayer B., Wachter H., and Kukovetz W.R. (1992) Tetrahydrobiopterin-dependent formation of endothelium-derived relaxing factor (nitric oxide) in aortic endothelial cells. Biochemical Journal, 281, 297-300.
62. Setoguchi S., Mohri M., Shimokawa H., and Takeshita A. (2001) Tetrahydrobiopterin improves endothelial dysfunction in coronary micro circulation, in patients without epicardial coronary artery disease. Journal of the American College of Cardiology, 38, 493-498.
63. Shi W., Wang X., Shih D.M., Laubach V.E., Navab M., and Lusis A.J. (2002) Paradoxical reduction of fatty streak formation in mice lacking endothelial nitric oxide synthase. Circulation, 105, 2078-2082.
64. Shinohara M., Kawashima S., Takaya T., Yamashita M., Inove N., Hirata K., and Yokoyama M. (2004) Over expression of endothelial nitric oxide synthase accelerates vascular remodeling in apo E-deficient mice. Circulation Journal, 68(S1), 373.
65. - imbalance in insulin-resistant rat aorta. Diabetes, 48, 2437-2445.
66. Shinozaki K., Nishio Y., Okamura T., Yoshida Y., Maegawa H., Kojima H., Masada M., Toda N., Kikkawa R., and Kashiwagi A. (2000) Oral administration of tetrahydrobiopterin prevents endothelial dysfunction and vascular oxidative stress in the aortas of insulin-resistant rats. Circulation Research, 87, 566-573.
67. Sorescu D., Weiss D., Lassegue B., Clempus R.E., Szocs K., Sorescu G.P., Valppu L., Quinn M.T., Lambeth J.D., Vega J.D., Taylor W.R., and Griendling K.K. (2002) Superoxide production and expression of nox family proteins in human atherosclerosis. Circulation, 105, 1429-1435.
68. Stroes E., Hijmering M., van Zandvoort M., Wever R., Rabelink T.J., and van Faassen E.E. (1998) Origin of superoxide production by endothelial nitric oxide synthase. FEBS Letters, 438, 161-164.
69. Stroes E., Kastelein J., Cosentino F., Erkelens W., Wever R., Koomans H., Luscher T., and Rabelink T. (1997) Tetrahydrobiopterin restores endothelial function in hypercholesterolemia. Journal of Clinical Investigation, 99, 41-46.
70. Stuehr D.J. (1999) Mammalian nitric oxide synthases. Biochimica Biophysica Acta, 1411, 217-230.
71. Taddei S., Virdis A., Ghiadoni L., Magagna A., and Salvetti A. (1998) Vitamin C improves endothelium-dependent vasodilation by restoring nitric oxide activity in essential hypertension. Circulation, 97, 2222-2229.
72. Tiefenbacher C.P. (2001) Tetreahydrobiopterin: A critical factor for eNOS and a strategy in the treatment of endothelial function? American Journal of Physiology Heart and Circulatory Physiology, 280, H2484-H2488.
73. Tiefenbacher C.P., Bleeke T., Vahl C., Amann K., Vogt A., and Kubler W. (2000) Endothelial dysfunction of coronary resistance arteries is improved by tetrahydrobiopterin in atherosclerosis. Circulation, 102, 2172-2179.
74. Tsutsui M., Milstien S., and Katusic Z.S. (1996) Effect of tetrahydrobiopterin on endothelial function in canine middle cerebral arteries. Circulation Research, 79, 336-342.
75. van Haperen R., de Waard M., van Deel E., Mees B., Kutryk M., van Aken T., Hamming J., Grosveld F., Duncker D.J., and de Crom R. (2002) Reduction of blood pressure, plasma cholesterol, and atherosclerosis by elevated endothelial nitric oxide. Journal of Biological Chemistry, 277, 48803-48807.
76. Vanhoutte P.M., and Boulanger C.M. (1995) Endothelium-dependent responses in hypertension. Hypertension Research, 18, 87-98.
77. Vasquez-Vivar J., Duquaine D., Whitsett J., Kalyanaraman B., and Rajagopalan S. (2002a) Altered tetrahydrobiopterin metabolism in atherosclerosis: Implications for use of oxidized tetrahydrobiopterin analogues and thiol antioxidants. Arteriosclerosis, Thrombosis, and Vascular Biology, 22, 1655-1661.
78. Vasquez-Vivar J., Kalyanaraman B., and Martasek P. (2003) The role of tetrahydrobiopterin in superoxide generation from eNOS: Enzymology and physiological implications. Free Radical Research, 37, 121-127.
79. Vasquez-Vivar J., Kalyanaraman B., Martasek P., Hogg N., Masters B.S., Karoui H., Tordo P., and Pritchard K.A. Jr. (1998) Superoxide generation by endothelial nitric oxide synthase: The influence of cofactors. Proceedings of the National Academy of Sciences of the United States of America, 95, 9220-9225.
80. Vasquez-Vivar J., Martasek P., Whitsett J., Joseph J., and Kalyanaraman B. (2002b) The ratio between tetrahydrobiopterin and oxidized tetrahydrobiopterin analogues controls superoxide release from endothelial nitric oxide synthase: An EPR spin trapping study. Biochemical Journal, 362(Pt 3): 733-739.
81. Warnholtz A., Nickenig G., Schulz E., Macharzina R., Brasen J.H., Skatchkov M., Heitzer T., Stasch J.P., Griendling K.K., Harrison D.G., Bohm M., Meinertz T., and Munzel T. (1999) Increased NADH-oxidase-mediated superoxide production in the early stages of atherosclerosis: Evidence for involvement of the renin-angiotensin system. Circulation, 99, 2027-2033.
82. Werner-Felmayer G., Golderer G., and Werner E.R. (2002) Tetrahydrobiopterin biosynthesis, utilization and pharmacological effects. Current Drug Metabolism, 3, 159-173.
83. Wever R.M.F., Luscher T.F., Cosentino F., and Rabelink T.J. (1998) Atherosclerosis and the two faces of endothelial nitric oxide synthase. Circulation, 97, 108-112.
84. Wever R.M., van Dam T., van Rijn H.J., de Groot F., and Rabelink T.J. (1997) Tetrahydrobiopterin regulates superoxide and nitric oxide generation by recombinant endothelial nitric oxide synthase. Biochemical Biophysical Research Communications, 237, 340-344.
85. 2+/calmodulin-dependent and tetrahydrobiopterin regulatory process. Journal of Biological Chemistry, 273, 25804-25808.
86. Zheng J.S., Yang X.Q., Lookingland K.J., Fink G.D., Hesslinger C., Kapatos G., Kovesdi I., and Chen A.F. (2003) Gene transfer of human guanosine 5′-triphosphate cyclohydrolase I restores vascular tetrahydrobiopterin level and endothelial function in low renin hypertension. Circulation, 108, 1238-1245.
87. Zou M.H., Shi C., and Cohen R.A. (2002) Oxidation of the zinc-thiolate complex and uncoupling of endothelial nitric oxide synthase by peroxynitrite. Journal of Clinical Investigation, 109, 817-826.