Regulation of endothelial cell tetrahydrobiopterin. Pathophysiological and therapeutic implications

Advances in Pharmacology

Volumn 60, Issue C, 2010, Pages 107-132

  Harrison, David G ^a   Chen, Wei ^a   Dikalov, Sergey ^a   Li, Li ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Atherosclerosis; Diabetes; Hypertension; Nitric oxide; Peroxynitrite; Superoxide

Indexed keywords

DIHYDROFOLATE REDUCTASE; GUANOSINE TRIPHOSPHATE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; REGULATOR PROTEIN; SUPEROXIDE; TETRAHYDROBIOPTERIN; 5,6,7,8-TETRAHYDROBIOPTERIN; BIOPTERIN; DRUG DERIVATIVE;

ATHEROSCLEROSIS; BOOK; DIABETES MELLITUS; DRUG STRUCTURE; ENDOTHELIAL DYSFUNCTION; ENDOTHELIUM CELL; ENZYME ACTIVITY; GENE EXPRESSION; HUMAN; HYPERCHOLESTEROLEMIA; HYPERTENSION; INSULIN RESISTANCE; NONHUMAN; OXIDATION; OXIDATION REDUCTION REACTION; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; ANIMAL; CHEMISTRY; DRUG EFFECT; ENZYMOLOGY; METABOLISM; PATHOLOGY; REVIEW;

ANIMALS; BIOPTERIN; ENDOTHELIAL CELLS; HUMANS;

EID: 78349240645     PISSN: 10543589     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-385061-4.00005-2     Document Type: Chapter

References (87)

1. Alp N.J., McAteer M.A., Khoo J., Choudhury R.P., Channon K.M. Increased endothelial tetrahydrobiopterin synthesis by targeted transgenic GTP-cyclohydrolase I overexpression reduces endothelial dysfunction and atherosclerosis in ApoE-knockout mice. Arteriosclerosis, Thrombosis, and Vascular Biology 2004, 24(3):445-450.
2. Alp N.J., Mussa S., Khoo J., Cai S., Guzik T., Jefferson A., et al. Tetrahydrobiopterin-dependent preservation of nitric oxide-mediated endothelial function in diabetes by targeted transgenic GTP-cyclohydrolase I overexpression. Journal of Clinical Investigation 2003, 112(5):725-735.
3. Beckman J.S., Koppenol W.H. Nitric oxide, superoxide, and peroxynitrite: The good, the bad, and ugly. The American Journal of Physiology 1996, 271(5 Pt 1):C1424-C1437.
4. Berka V., Wu G., Yeh H.C., Palmer G., Tsai A.L. Three different oxygen-induced radical species in endothelial nitric-oxide synthase oxygenase domain under regulation by l-arginine and tetrahydrobiopterin. The Journal of Biological Chemistry 2004, 279(31):32243-32251.
5. Bigham E.C., Smith G.K., Reinhard J.F., Mallory W.R., Nichol C.A., Morrison R.W. Synthetic analogues of tetrahydrobiopterin with cofactor activity for aromatic amino acid hydroxylases. Journal of Medicinal Chemistry 1987, 30(1):40-45.
6. Boger R.H., Bode-Boger S.M., Szuba A., Tsao P.S., Chan J.R., Tangphao O., et al. Asymmetric dimethylarginine (ADMA): A novel risk factor for endothelial dysfunction: Its role in hypercholesterolemia. Circulation 1998, 98(18):1842-1847.
7. Bossaller C., Habib G.B., Yamamoto H., Williams C., Wells S., Henry P.D. Impaired muscarinic endothelium-dependent relaxation and cyclic guanosine 5'-monophosphate formation in atherosclerotic human coronary artery and rabbit aorta. Journal of Clinical Investigation 1987, 79(1):170-174.
8. Burney S., Caulfield J.L., Niles J.C., Wishnok J.S., Tannenbaum S.R. The chemistry of DNA damage from nitric oxide and peroxynitrite. Mutation Research 1999, 424(1-2):37-49.
9. Chalupsky K., Cai H. Endothelial dihydrofolate reductase: Critical for nitric oxide bioavailability and role in angiotensin II uncoupling of endothelial nitric oxide synthase. Proceedings of the National Academy of Sciences of the United States of America 2005, 102(25):9056-9061.
10. Chiu J.J., Usami S., Chien S. Vascular endothelial responses to altered shear stress: Pathologic implications for atherosclerosis. Annali Medici 2009, 41(1):19-28.
11. Cosentino F., Patton S., d'Uscio L.V., Werner E.R., Werner-Felmayer G., Moreau P., et al. Tetrahydrobiopterin alters superoxide and nitric oxide release in prehypertensive rats. Journal of Clinical Investigation 1998, 101(7):1530-1537.
12. Crabtree M.J., Tatham A.L., Hale A.B., Alp N.J., Channon K.M. Critical role for tetrahydrobiopterin recycling by dihydrofolate reductase in regulation of endothelial nitric-oxide synthase coupling: Relative importance of the de novo biopterin synthesis versus salvage pathways. The Journal of Biological Chemistry 2009, 284(41):28128-28136.
13. Creager M.A., Gallagher S.J., Girerd X.J., Coleman S.M., Dzau V.J., Cooke J.P. l-arginine improves endothelium-dependent vasodilation in hypercholesterolemic humans. Journal of Clinical Investigation 1992, 90(4):1248-1253.
14. Dominguez-Rodriguez A., Abreu-Gonzalez P., Kaski J.C. Inflammatory systemic biomarkers in setting acute coronary syndromes-effects of the diurnal variation. Current Drug Targets 2009, 10(10):1001-1008.
15. Fortin C.F., McDonald P.P., Fulop T., Lesur O. Sepsis, leukocytes, and nitric oxide (NO): An intricate affair. Shock 2010, 33(4):344-352.
16. Freiman P.C., Mitchell G.G., Heistad D.D., Armstrong M.L., Harrison D.G. Atherosclerosis impairs endothelium-dependent vascular relaxation to acetylcholine and thrombin in primates. Circulation Research 1986, 58(6):783-789.
17. Gangula P.R., Mukhopadhyay S., Ravella K., Cai S., Channon K.M., Garfield R.E., et al. Tetrahydrobiopterin (BH4), a cofactor for nNOS, restores gastric emptying and nNOS expression in female diabetic rats. American Journal of Physiology. Gastrointestinal and Liver Physiology 2010, 298(5):G692-G699.
18. Gates M. The chemistry of the pteridines. Chemical Reviews 1947, 41(1):63-95.
19. Hamon C.G., Cutler P., Blair J.A. Tetrahydrobiopterin metabolism in the streptozotocin induced diabetic state in rats. Clinica Chimica Acta 1989, 181(3):249-253.
20. Harrison D.G., Cai H. Endothelial control of vasomotion and nitric oxide production. Cardiology Clinics 2003, 21(3):289-302.
21. Hattori Y., Hattori S., Wang X., Satoh H., Nakanishi N., Kasai K. Oral administration of tetrahydrobiopterin slows the progression of atherosclerosis in apolipoprotein E-knockout mice. Arteriosclerosis, Thrombosis, and Vascular Biology 2007, 27(4):865-870.
22. Hattori Y., Nakanishi N., Akimoto K., Yoshida M., Kasai K. HMG-CoA reductase inhibitor increases GTP cyclohydrolase I mRNA and tetrahydrobiopterin in vascular endothelial cells. Arteriosclerosis, Thrombosis, and Vascular Biology 2003, 23(2):176-182.
23. Heitzer T., Brockhoff C., Mayer B., Warnholtz A., Mollnau H., Henne S., et al. Tetrahydrobiopterin improves endothelium-dependent vasodilation in chronic smokers: Evidence for a dysfunctional nitric oxide synthase. Circulation Research 2000, 86(2):E36-E41.
24. Heitzer T., Krohn K., Albers S., Meinertz T. Tetrahydrobiopterin improves endothelium-dependent vasodilation by increasing nitric oxide activity in patients with Type II diabetes mellitus. Diabetologia 2000, 43(11):1435-1438.
25. Heller R., Unbehaun A., Schellenberg B., Mayer B., Werner-Felmayer G., Werner E.R. l-ascorbic acid potentiates endothelial nitric oxide synthesis via a chemical stabilization of tetrahydrobiopterin. The Journal of Biological Chemistry 2001, 276(1):40-47.
26. Higashi Y., Sasaki S., Nakagawa K., Fukuda Y., Matsuura H., Oshima T., et al. Tetrahydrobiopterin enhances forearm vascular response to acetylcholine in both normotensive and hypertensive individuals. American Journal of Hypertension 2002, 15(4 Pt 1):326-332.
27. Higman D.J., Strachan A.M., Buttery L., Hicks R.C., Springall D.R., Greenhalgh R.M., et al. Smoking impairs the activity of endothelial nitric oxide synthase in saphenous vein. Arteriosclerosis, Thrombosis, and Vascular Biology 1996, 16(4):546-552.
28. Hink U., Li H., Mollnau H., Oelze M., Matheis E., Hartmann M., et al. Mechanisms underlying endothelial dysfunction in diabetes mellitus. Circulation Research 2001, 88(2):E14-E22.
29. Hong H.J., Hsiao G., Cheng T.H., Yen M.H. Supplemention with tetrahydrobiopterin suppresses the development of hypertension in spontaneously hypertensive rats. Hypertension 2001, 38(5):1044-1048.
30. Huang A., Vita J.A., Venema R.C., Keaney J.F. Ascorbic acid enhances endothelial nitric-oxide synthase activity by increasing intracellular tetrahydrobiopterin. The Journal of Biological Chemistry 2000, 275(23):17399-17406.
31. Huraux C., Makita T., Kurz S., Yamaguchi K., Szlam F., Tarpey M.M., et al. Superoxide production, risk factors, and endothelium-dependent relaxations in human internal mammary arteries. Circulation 1999, 99(1):53-59.
32. Ishii M., Shimizu S., Nagai T., Shiota K., Kiuchi Y., Yamamoto T. Stimulation of tetrahydrobiopterin synthesis induced by insulin: Possible involvement of phosphatidylinositol 3-kinase. The International Journal of Biochemistry & Cell Biology 2001, 33(1):65-73.
33. Jiang J., Valen G., Tokuno S., Thoren P., Pernow J. Endothelial dysfunction in atherosclerotic mice: Improved relaxation by combined supplementation with l-arginine-tetrahydrobiopterin and enhanced vasoconstriction by endothelin. British Journal of Pharmacology 2000, 131(7):1255-1261.
34. Kase H., Hashikabe Y., Uchida K., Nakanishi N., Hattori Y. Supplementation with tetrahydrobiopterin prevents the cardiovascular effects of angiotensin II-induced oxidative and nitrosative stress. Journal of Hypertension 2005, 23(7):1375-1382.
35. Katusic Z.S., Stelter A., Milstien S. Cytokines stimulate GTP cyclohydrolase I gene expression in cultured human umbilical vein endothelial cells. Arteriosclerosis, Thrombosis, and Vascular Biology 1998, 18(1):27-32.
36. Kerr S., Brosnan M.J., McIntyre M., Reid J.L., Dominiczak A.F., Hamilton C.A. Superoxide anion production is increased in a model of genetic hypertension: Role of the endothelium. Hypertension 1999, 33(6):1353-1358.
37. Khan B.V., Harrison D.G., Olbrych M.T., Alexander R.W., Medford R.M. Nitric oxide regulates vascular cell adhesion molecule 1 gene expression and redox-sensitive transcriptional events in human vascular endothelial cells. Proceedings of the National Academy of Sciences of the United States of America 1996, 93(17):9114-9119.
38. Kosmicki M.A. Long-term use of short- and long-acting nitrates in stable angina pectoris. Current Clinical Pharmacology 2009, 4(2):132-141.
39. Kubes P., Suzuki M., Granger D.N. Nitric oxide: An endogenous modulator of leukocyte adhesion. Proceedings of the National Academy of Sciences of the United States of America 1991, 88(11):4651-4655.
40. Kuzkaya N., Weissmann N., Harrison D.G., Dikalov S. Interactions of peroxynitrite, tetrahydrobiopterin, ascorbic acid, and thiols: Implications for uncoupling endothelial nitric-oxide synthase. The Journal of Biological Chemistry 2003, 278(25):22546-22554.
41. Landmesser U., Dikalov S., Price S.R., McCann L., Fukai T., Holland S.M., et al. Oxidation of tetrahydrobiopterin leads to uncoupling of endothelial cell nitric oxide synthase in hypertension. Journal of Clinical Investigation 2003, 111(8):1201-1209.
42. Laursen J.B., Somers M., Kurz S., McCann L., Warnholtz A., Freeman B.A., et al. Endothelial regulation of vasomotion in apoE-deficient mice: Implications for interactions between peroxynitrite and tetrahydrobiopterin. Circulation 2001, 103(9):1282-1288.
43. Li L., Rezvan A., Salerno J.C., Husain A., Kwon K., Jo H., et al. GTP cyclohydrolase I phosphorylation and interaction with GTP cyclohydrolase feedback regulatory protein provide novel regulation of endothelial tetrahydrobiopterin and nitric oxide. Circulation Research 2010, 106(2):328-336.
44. Ludmer P.L., Selwyn A.P., Shook T.L., Wayne R.R., Mudge G.H., Alexander R.W., et al. Paradoxical vasoconstriction induced by acetylcholine in atherosclerotic coronary arteries. The New England Journal of Medicine 1986, 315(17):1046-1051.
45. Meininger C.J., Marinos R.S., Hatakeyama K., Martinez-Zaguilan R., Rojas J.D., Kelly K.A., et al. Impaired nitric oxide production in coronary endothelial cells of the spontaneously diabetic bib rat is due to tetrahydrobiopterin deficiency. The Biochemical Journal 2000, 349(Pt 1):353-356.
46. Miller M.R., Megson I.L. Recent developments in nitric oxide donor drugs. British Journal of Pharmacology 2007, 151(3):305-321.
47. Moens A.L., Takimoto E., Tocchetti C.G., Chakir K., Bedja D., Cormaci G., et al. Reversal of cardiac hypertrophy and fibrosis from pressure overload by tetrahydrobiopterin: Efficacy of recoupling nitric oxide synthase as a therapeutic strategy. Circulation 2008, 117(20):2626-2636.
48. Moncada S., Palmer R.M., Higgs E.A. The discovery of nitric oxide as the endogenous nitrovasodilator. Hypertension 1988, 12(4):365-372.
49. Moncada S., Palmer R.M., Higgs E.A. Nitric oxide: Physiology, pathophysiology, and pharmacology. Pharmacological Reviews 1991, 43(2):109-142.
50. Mugge A., Elwell J.H., Peterson T.E., Hofmeyer T.G., Heistad D.D., Harrison D.G. Chronic treatment with polyethylene-glycolated superoxide dismutase partially restores endothelium-dependent vascular relaxations in cholesterol-fed rabbits. Circulation Research 1991, 69(5):1293-1300.
51. Nakai K., Urushihara M., Kubota Y., Kosaka H. Ascorbate enhances iNOS activity by increasing tetrahydrobiopterin in RAW 264.7 cells. Free Radical Biology & Medicine 2003, 35(8):929-937.
52. Nandi M., Miller A., Stidwill R., Jacques T.S., Lam A.A., Haworth S., et al. Pulmonary hypertension in a GTP-cyclohydrolase 1-deficient mouse. Circulation 2005, 111(16):2086-2090.
53. Noris M., Morigi M., Donadelli R., Aiello S., Foppolo M., Todeschini M., et al. Nitric oxide synthesis by cultured endothelial cells is modulated by flow conditions. Circulation Research 1995, 76(4):536-543.
54. Oak J.H., Cai H. Attenuation of angiotensin II signaling recouples eNOS and inhibits nonendothelial NOX activity in diabetic mice. Diabetes 2007, 56(1):118-126.
55. Ohara Y., Peterson T.E., Harrison D.G. Hypercholesterolemia increases endothelial superoxide anion production. Journal of Clinical Investigation 1993, 91(6):2546-2551.
56. Okumura M., Masada M., Yoshida Y., Shintaku H., Hosoi M., Okada N., et al. Decrease in tetrahydrobiopterin as a possible cause of nephropathy in type II diabetic rats. Kidney International 2006, 70(3):471-476.
57. Patel K.B., Stratford M.R., Wardman P., Everett S.A. Oxidation of tetrahydrobiopterin by biological radicals and scavenging of the trihydrobiopterin radical by ascorbate. Free Radical Biology & Medicine 2002, 32(3):203-211.
58. Pieper G.M. Acute amelioration of diabetic endothelial dysfunction with a derivative of the nitric oxide synthase cofactor, tetrahydrobiopterin. Journal of Cardiovascular Pharmacology 1997, 29(1):8-15.
59. Porkert M., Sher S., Reddy U., Cheema F., Niessner C., Kolm P., et al. Tetrahydrobiopterin: A novel antihypertensive therapy. Journal of Human Hypertension 2008, 22(6):401-407.
60. Ren J., Kotaka M., Lockyer M., Lamb H.K., Hawkins A.R., Stammers D.K. GTP cyclohydrolase II structure and mechanism. The Journal of Biological Chemistry 2005, 280(44):36912-36919.
61. Schmidt T.S., McNeill E., Douglas G., Crabtree M.J., Hale A.B., Khoo J., et al. Tetrahydrobiopterin supplementation reduces atherosclerosis and vascular inflammation in apolipoprotein E-knockout mice. Clinical Science (London) 2010, 19(3):131-142.
62. Shinozaki K., Kashiwagi A., Nishio Y., Okamura T., Yoshida Y., Masada M., et al. Abnormal biopterin metabolism is a major cause of impaired endothelium-dependent relaxation through nitric oxide/O2-imbalance in insulin-resistant rat aorta. Diabetes 1999, 48(12):2437-2445.
63. Silberman G.A., Fan T.H., Liu H., Jiao Z., Xiao H.D., Lovelock J.D., et al. Uncoupled cardiac nitric oxide synthase mediates diastolic dysfunction. Circulation 2010, 121(4):519-528.
64. Stroes E., Kastelein J., Cosentino F., Erkelens W., Wever R., Koomans H., et al. Tetrahydrobiopterin restores endothelial function in hypercholesterolemia. Journal of Clinical Investigation 1997, 99(1):41-46.
65. Stuehr D.J. Structure-function aspects in the nitric oxide synthases. Annual Review of Pharmacology and Toxicology 1997, 37:339-359.
66. Sugiyama T., Levy B.D., Michel T. Tetrahydrobiopterin recycling, a key determinant of endothelial nitric-oxide synthase-dependent signaling pathways in cultured vascular endothelial cells. The Journal of Biological Chemistry 2009, 284(19):12691-12700.
67. Sun X., Kumar S., Tian J., Black S.M. Estradiol increases guanosine 5'-triphosphate cyclohydrolase expression via the nitric oxide-mediated activation of cyclic adenosine 5'-monophosphate response element binding protein. Endocrinology 2009, 150(8):3742-3752.
68. Tada K., Yoshida T., Mochizuki K., Konno T., Nakagawa H. Two siblings of hyperphenylalaninemia: Suggestion to a genetic variant of phenylketonuria. The Tohoku Journal of Experimental Medicine 1970, 100(3):249-253.
69. Taylor N.E., Maier K.G., Roman R.J., Cowley A.W. NO synthase uncoupling in the kidney of Dahl S rats: Role of dihydrobiopterin. Hypertension 2006, 48(6):1066-1071.
70. Taylor A.L., Ziesche S., Yancy C., Carson P., D'Agostino R., Ferdinand K., et al. Combination of isosorbide dinitrate and hydralazine in blacks with heart failure. The New England Journal of Medicine 2004, 351(20):2049-2057.
71. Thomas G.D., Sander M., Lau K.S., Huang P.L., Stull J.T., Victor R.G. Impaired metabolic modulation of alpha-adrenergic vasoconstriction in dystrophin-deficient skeletal muscle. Proceedings of the National Academy of Sciences of the United States of America 1998, 95(25):15090-15095.
72. Thony B., Auerbach G., Blau N. Tetrahydrobiopterin biosynthesis, regeneration and functions. The Biochemical Journal 2000, 347(Pt 1):1-16.
73. Tie L., Li X.J., Wang X., Channon K.M., Chen A.F. Endothelium-specific GTP cyclohydrolase I overexpression accelerates refractory wound healing by suppressing oxidative stress in diabetes. American Journal of Physiology. Endocrinology and Metabolism 2009, 296(6):E1423-E1429.
74. Tiefenbacher C.P., Bleeke T., Vahl C., Amann K., Vogt A., Kubler W. Endothelial dysfunction of coronary resistance arteries is improved by tetrahydrobiopterin in atherosclerosis. Circulation 2000, 102(18):2172-2179.
75. Toth M., Kukor Z., Sahin-Toth M. Activation and dimerization of type III nitric oxide synthase by submicromolar concentrations of tetrahydrobiopterin in microsomal preparations from human primordial placenta. Placenta 1997, 18(2-3):189-196.
76. Tsai P., Weaver J., Cao G.L., Pou S., Roman L.J., Starkov A.A., et al. l-arginine regulates neuronal nitric oxide synthase production of superoxide and hydrogen peroxide. Biochemical Pharmacology 2005, 69(6):971-979.
77. Tzima E., Irani-Tehrani M., Kiosses W.B., Dejana E., Schultz D.A., Engelhardt B., et al. A mechanosensory complex that mediates the endothelial cell response to fluid shear stress. Nature 2005, 437(7057):426-431.
78. Uematsu M., Ohara Y., Navas J.P., Nishida K., Murphy T.J., Alexander R.W., et al. Regulation of endothelial cell nitric oxide synthase mRNA expression by shear stress. The American Journal of Physiology 1995, 269(6 Pt 1):C1371-C1378.
79. Vasquez-Vivar J. Tetrahydrobiopterin, superoxide, and vascular dysfunction. Free Radical Biology & Medicine 2009, 47(8):1108-1119.
80. 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. Arteriosclerosis, Thrombosis, and Vascular Biology 2002, 22(10):1655-1661.
81. 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. The Biochemical Journal 2002, 362(Pt 3):733-739.
82. Wei C.C., Crane B.R., Stuehr D.J. Tetrahydrobiopterin radical enzymology. Chemical Reviews 2003, 103(6):2365-2383.
83. Wei C.C., Wang Z.Q., Tejero J., Yang Y.P., Hemann C., Hille R., et al. Catalytic reduction of a tetrahydrobiopterin radical within nitric-oxide synthase. The Journal of Biological Chemistry 2008, 283(17):11734-11742.
84. Wenzel P., Daiber A., Oelze M., Brandt M., Closs E., Xu J., et al. Mechanisms underlying recoupling of eNOS by HMG-CoA reductase inhibition in a rat model of streptozotocin-induced diabetes mellitus. Atherosclerosis 2008, 198(1):65-76.
85. Werner E.R., Werner-Felmayer G., Mayer B. Tetrahydrobiopterin, cytokines, and nitric oxide synthesis. Proceedings of the Society for Experimental Biology and Medicine 1998, 219(3):171-182.
86. Widder J.D., Chen W., Li L., Dikalov S., Thony B., Hatakeyama K., et al. Regulation of tetrahydrobiopterin biosynthesis by shear stress. Circulation Research 2007, 101(8):830-838.
87. Zhang H., Bhargava K., Keszler A., Feix J., Hogg N., Joseph J., et al. Transmembrane nitration of hydrophobic tyrosyl peptides. Localization, characterization, mechanism of nitration, and biological implications. The Journal of Biological Chemistry 2003, 278(11):8969-8978.