Tetrahydrobiopterin, nitric oxide and regulation of cerebral arterial tone

Progress in Neurobiology

Volumn 52, Issue 4, 1997, Pages 295-302

  Kinoshita, Hiroyuki ^a   Tsutsui, Masato ^a   Milstien, Sheldon ^b   Katusic, Zvonimir S ^a  

^a MAYO CLINIC   (United States)

^b NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NITRIC OXIDE SYNTHASE; TETRAHYDROBIOPTERIN;

ANIMAL TISSUE; ARTERY TONE; BLOOD VESSEL TONE; BRAIN ARTERY; DOG; ENDOTHELIUM CELL; ENZYME ACTIVITY; GENE EXPRESSION REGULATION; GENETIC RECOMBINATION; MOLECULAR CLONING; NONHUMAN; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; REVIEW; VASCULAR DISEASE; VASCULAR ENDOTHELIUM;

ANIMALS; ANTIOXIDANTS; BIOPTERIN; CEREBRAL ARTERIES; NITRIC OXIDE;

EID: 0030798048     PISSN: 03010082     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0301-0082(97)00017-8     Document Type: Review

References (77)

1. Abu-Soud, H. M. and Stuehr, D. J. (1993) Nitric oxide synthases reveal a role for calmodulin in controlling electron transfer. Proc. natn. Acad. Sci. U.S.A. 90, 10769-10772.
2. Albakri, Q. A. and Stuehr, D. J. (1996) Intracellular assembly of inducible NO synthase is limited by nitric oxide-mediated changes in heme insertion and availability. J. Biol. Chem. 271, 5414-5421.
3. Auch-Schwelk, W., Katusic, Z. S. and Vanhoutte, P. M. (1989) Contractions to oxygen-derived free radicals are augmented in aorta of the spontaneously hypertensive rat. Hypertension 13, 859-864.
4. Baek, K. J., Thiel, B. A., Lucas, S. and Stuehr, D. J. (1993) Macrophage nitric oxide synthase subunits. Purification, characterization, and role of prosthetic groups and substrate in regulating their association into a dimeric enzyme. J. Biol. Chem. 268, 21120-21129.
5. Baker, H., Marcus, S. L., Frank, O., Petrylak, D. P., DeAngelis, B., Dutcher, J. P. and Wiernik, P. H. (1989) Interleukin-2 enhances biopterin and catecholamine production during adoptive immunotherapy for various cancers. Cancer 64, 1226-1231.
6. Bredt, D. S., Hwang, P. M., Glatt, C. E., Lowenstein, C., Reed, R. R. and Snyder, S. H. (1991) Cloned and expressed nitric oxide synthase structurally resembles cytochrome P-450 reductase. Nature 351, 714-718.
7. Campos, K. L., Giovanelli, J. and Kaufman, S. (1995) Characteristics of the nitric oxide synthase-catalyzed conversion of arginine to N-hydroxyarginine, the first oxygenation step in the enzymic synthesis of nitric oxide. J. Biol. Chem. 270, 1721-1728.
8. Charles, I. G., Palmer, R. M., Hickery, M. S., Bayliss, M. T., Chubb, A. P., Hall, V. S., Moss, D. W. and Moncada, S. (1993) Cloning, characterization, and expression of a cDNA encoding an inducible nitric oxide synthase from the human chondrocyte. Proc. natn. Acad. Sci. U.S.A. 90, 11419-11423.
9. Chen, A. F. Y., O'Brien, T., Tsutsui, M., Kinoshita, H., Pompili, V. J., Crotty, T. B., Spector, D. J. and Katusic, Z. S. (1997) Expression and function of recombinant endothelial nitric oxide synthase gene in canine basilar artery. Circ. Res. 80, 327-335.
10. Cho, H. J., Xie, Q. W., Calaycay, J., Mumford, R. A., Swiderek, K. M., Lee, T. D. and Nathan, C. (1992) Calmodulin is a subunit of nitric oxide synthase from macrophages. J. Expl Med. 176, 599-604.
11. Cosentino, F. and Katusic, Z. S. (1995) Tetrahydrobiopterin and dysfunction of endothelial nitric oxide synthase in coronary arteries. Circulation 91, 139-144.
12. Cosentino, F., Moreau, P., d'Uscio, L. V. and Lüscher, T. F. (1995) Tetrahydrobiopterin and endothelial nitric oxide synthase dysfunction in spontaneously hypertensive rats. Circulation 92, 1565.
13. Davis, M. D. and Kaufman, S. (1993) Products of the tyrosine-dependent oxidation of tetrahydrobiopterin by rat liver phenylalanine hydroxylase. Arch. Biochem. Biophys. 304, 9-16.
14. Faraci, F. M. and Brian, J. E. Jr. (1994) Nitric oxide and the cerebral circulation. Stroke 25, 692-703.
15. Forstermann, U. and Kleinert, H. (1995) Nitric oxide synthase: expression and expressional control of the three isoforms. Naunyn-Schmied. Arch. Pharmacol. 352, 351-364.
16. Giovanelli, J., Campos, K. L. and Kaufman, S. (1991) Tetrahydrobiopterin, a cofactor for rat cerebellar nitric oxide synthase, does not function as a reactant in the oxygenation of arginine. Proc. natn. Acad. Sci. U.S.A. 88, 7091-7095.
17. Griscavage, J. M., Fukuto, J. M., Komori, Y. and Ignarro, L. J. (1994) Nitric oxide inhibits neuronal nitric oxide synthase by interacting with the heme prosthetic group: role of tetrahydrobiopterin in modulating the inhibitory action of nitric oxide. J. Biol. Chem. 269, 21644-21649.
18. Gross, S. S., Jaffe, E. A., Levi, R. and Kilbourn, R. G. (1991) 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.
19. Gross, S. S. and Levi, R. (1992) Tetrahydrobiopterin synthesis: An absolute requirement for cytokine-induced nitric oxide generation by vascular smooth muscle. J. Biol. Chem. 267, 25722-25729.
20. Gryglewski, R. J., Palmer, R. M. J. and Moncada, S. (1986) Superoxide anion is involved in the breakdown of endothelium-derived vascular relaxing factor. Nature 320, 454-456.
21. Hattori, Y. and Gross, S. S. (1993) GTP cyclohydrolase I mRNA is induced by LPS in vascular smooth muscle: characterization, sequence and relationship to nitric oxide synthase. Biochem. Biophys. Res. Commun. 195, 435-441.
22. +/calmodulin-dependent formation of hydrogen peroxide by brain nitric oxide synthase. Biochemistry 281, 627-630.
23. Hevel, J. M. and Marletta, M. A. (1992) Macrophage nitric oxide synthase: relationship between enzyme-bound tetrahydrobiopterin and synthase activity. Biochemistry 31, 7160-7165.
24. Hevel, J. M., White, K. A. and Marletta, M. A. (1991) Purification of the inducible murine macrophage nitric oxide synthase. Identification as a flavoprotein. J. Biol. Chem. 266, 22789-22791.
25. Higman, D. J., Strachan, A. M. J., Buttery, L., Hicks, R. C. J., Springall, D. R., Greenhalgh, R. M. and Powell, J. T. (1996) Smoking impairs the activity of endothelial nitric oxide synthase in saphenous vein. Arterioscler. Thromb. Vasc. Biol. 16, 546-552.
26. Iadecola, C., Pelligrino, D. A., Moskowitz, M. A. and Lassen, N. A. (1994) Nitric oxide synthase inhibition and cerebrovascular regulation. J. Cereb. Blood Flow Metab. 14, 175-192.
27. Janssens, S. P., Bloch, K. D., Nong, Z., Gerard, R. D., Zoldhelyi, P. and Collen, D. (1996) Adenoviral-mediated transfer of the human endothelial nitric oxide synthase gene reduces acute hypoxic pulmonary vasoconstriction in rats. J. Clin. Invest. 98, 317-324.
28. Katusic, Z. S. (1996) Superoxide anion and endothelial regulation of arterial tone. Free Radical Biol. Med. 20, 443-448.
29. Katusic, Z. S. and Stelter, A. M. (1994) Expression of GTP cyclohydrolase I gene in human aortic endothelial cells. Can. J. Physiol. Pharmacol. 72, 473.
30. Kaufman, S. (1993) New tetrahydrobiopterin-dependent systems. Annu. Rev. Nutr. 13, 261-286.
31. Kinoshita, H. and Katusic, Z. S. (1996) Exogenous tetrahydrobiopterin causes endothelium-dependent contractions in isolated canine basilar artery. Am. J. Physiol. 271, H738-H743.
32. Klatt, P., Schmidt, K. and Mayer, B. (1992a) Brain nitric oxide synthase is a haemoprotein. Biochem. J. 288, 15-17.
33. -/calmodulin-dependent cytochrome c reductase activity of brain nitric oxide synthase. J. Biol. Chem. 267, 11374-11378.
34. ω-hydroxy-L-arginine as an intermediate. J. Biol. Chem. 268, 14781-14787.
35. Klatt, P., Schmid, M., Leopold, E., Schmidt, K., Werner, E. R. and Mayer, B. (1994) The pteridine binding site of brain nitric oxide synthase. Tetrahydrobiopterin binding kinetics, specificity, and allosteric interaction with the substrate domain. J. Biol. Chem. 269, 13861-13866.
36. Klatt, P., Schmidt, K., Lehner, D., Glatter, O., Bachinger, H. P. and Mayer, B. (1995) Structural analysis of porcine brain nitric oxide synthase reveals a role for tetrahydrobiopterin and L-arginine in the formation of an SDS-resistant dimer. EMBO J. 14, 3687-3695.
37. Klatt, P., Pfeiffer, S., List, B. M., Lehner, D., Glatter, O., Bachinger, H. P., Werner, E. R., Schmidt, K. and Mayer, B. (1996) Characterization of heme-deficient neuronal nitric oxide synthase reveals a role for heme in subunit dimerization and binding of the amino acid substrate and tetrahydrobiopterin. J. Biol. Chem. 271, 7336-7342.
38. Knowles, R. G. and Moncada, S. (1994) Nitric oxide synthases in mammals. Biochem. J. 298, 249-258.
39. Kukor, Z., Meszaros, G., Hertelendy, F. and Toth, M. (1996) Calcium-dependent nitric oxide synthesis is potently stimulated by tetrahydrobiopterin in human primordial placenta. Placenta 17, 69-73.
40. Lamas, S., Marsden, P. A., Li, G. K., Tempst, P. and Michel, T. (1992) Endothelial nitric oxide synthase: molecular cloning and characterization of a distinct constitutive enzyme isoform. Proc. natn. Acad. Sci. U.S.A. 89, 6348-6352.
41. Marletta, M. A. (1993) Nitric oxide synthase structure and mechanism. J. Biol. Chem. 268, 12231-12234.
42. 2+/calmodulin-dependent nitric oxide synthase from porcine cerebellum: cofactor-role of tetrahydrobiopterin. FEBS Lett. 277, 215-219.
43. Mayer, B. and Werner, E. R. (1995b) In search of a function for tetrahydrobiopterin in the biosynthesis of nitric oxide. Naunyn-Schmied. Arch. Pharmacol. 351, 453-463.
44. Mayer, B., John, M., Heinzel, B., Werner, E. R., Wachter, H., Schultz, G. and Bohme, E. (1991) Brain nitric oxide synthase is a biopterin- and flavin-containing multi-functional oxido-reductase. FEBS Lett. 288, 187-191.
45. Mayer, B., Klatt, P., Werner, E. R. and Schmidt, K. (1995a) Kinetics and mechanism of tetrahydrobiopterin-induced oxidation of nitric oxide. J. Biol. Chem. 270, 655-659.
46. McCord, J. M. and Fridovich, I. (1969) Superoxide dismutase: an enzymic function for erythrocuprein (hemocuprein). J. Biol. Chem. 144, 6049-6055.
47. McMillan, K., Bredt, D. S., Hirsch, D. J., Snyder, S. H., Clark, J. E. and Masters, B. S. (1992) Cloned, expressed rat cerebellar nitric oxide synthase contains stoichiometric amounts of heme, which binds carbon monoxide. Proc. natn. Acad. Sci. U.S.A. 89, 11141-11145.
48. Nathan, C. F. and Hibbs, J. B. Jr. (1991) Role of nitric oxide synthesis in macrophage antimicrobial activity. Curr. Opin. Immunol. 3, 65-70.
49. Nichol, C. A., Smith, G. K. and Duch, D. S. (1985) Biosynthesis and metabolism of tetrahydrobiopterin and molybdopterin. Annu. Rev. Biochem. 54, 729-764.
50. Nussler, A. K., Di Silvio, M., Billiar, T. R., Hoffman, R. A., Geller, D. A., Selby, R., Madariaga, J. and Simmons, R. L. (1992) Stimulation of the nitric oxide synthase pathway in human hepatocytes by cytokines and endotoxin. J. Expl Med. 176, 261-264.
51. Pollock, J. S., Forstermann, U., Mitchell, J. A., Warner, T. D., Schmidt, H. H., Nakane, M. and Murad, F. (1991) Purification and characterization of particulate endothelium-derived relaxing factor synthase from cultured and native bovine aortic endothelial cells. Proc. natn. Acad. Sci. U.S.A. 88, 10480-10484.
52. Rodriguez-Crespo, I., Gerber, N. C. and Ortiz de Montellano, P. R. (1996) Endothelial nitric oxide synthase. Expression in escherichia coli, spectroscopic characterization, and role of tetrahydrobiopterin in dimer formation. J. Biol. Chem. 271, 11462-11467.
53. Rosenblum, W. I. (1997) Tetrahydrobiopterin, a cofactor for nitric oxide synthase, produces endothelium-dependent dilation of mouse pial arterioles. Stroke 28, 186-189.
54. Rosenkranz-Weiss, P., Sessa, W. C., Milstien, S., Kaufman, S., Watson, C. A. and Pober, J. S. (1994) Regulation of nitric oxide synthesis by proinflammatory cytokines in human umbilical vein endothelial cells. J. Clin. Invest. 93, 2236-2243.
55. Rubanyi, G. M. and Vanhoutte, P. M. (1986) Superoxide anions and hyperoxia inactivate endothelium-derived relaxing factor. Am. J. Physiol. 250, H822-H827.
56. Sakai, N., Kaufman, S. and Milstien, S. (1993) Tetrahydrobiopterin is required for cytokine-induced nitric oxide production in a murine macrophage cell line (RAW 264). Mol. Pharmacol. 43, 6-10.
57. 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. Biochem. J. 281, 297-300.
58. Scott-Burden, T., Elizondo, E., Ge, T., Boulanger, C. M. and Vanhoutte, P. M. (1994) Simultaneous activation of adenylyl cyclase and protein kinase C induces production of nitric oxide by vascular smooth muscle cells. Molec. Pharmacol. 46, 274-282.
59. Snyder, S. H. (1992) Nitric oxide: first in a new class of neurotransmitters. Science 257, 494-496.
60. Stroes, E., Kastelein, J., Cosentino, F., Erkelens, W., Wever, R., Koomans, H., Lüscher, T. and Rabelink, T. (1997) Tetrahydrobiopterin restores endothelial function in hypercholesterolemia. J. Clin. Invest. 99, 41-46.
61. Stuehr, D. J. and Ikeda-Saito, M. (1992) Spectral characterization of brain and macrophage nitric oxide synthases. Cytochrome P-450-like hemeproteins that contain a flavin semiquinone radical. J. Biol. Chem. 267, 20547-20550.
62. Stuehr, D. J., Cho, H. J., Kwon, N. S., Weise, M. F. and Nathan, C. F. (1991a) Purification and characterization of the cytokine-induced macrophage nitric oxide synthase: an FAD- and FMN-containing flavoprotein. Proc. natn. Acad. Sci. U.S.A. 88, 7773-7777.
63. Stuehr, D. J., Kwon, N. S., Nathan, C. F., Griffith, O. W., Feldman, P. L. and Wiseman, J. (1991b) N omega-hydroxy-L-arginine is an intermediate in the biosynthesis of nitric oxide from L-arginine. J. Biol. Chem. 266, 6259-6263.
64. Suzuki, K., Tatsumi, H., Satoh, S., Senda, T., Nakata, T., Fujii, J. and Taniguchi, N. (1993) Manganese superoxide dismutase in endothelial cells: localization and mechanism of induction. Am. J. Physiol. 265, H1173-H1178.
65. Tiefenbacher, C. P., Chilian, W. M., Mitchell, M. and DeFily, D. V. (1996) Restoration of endothelium-dependent vasodilation after reperfusion injury by tetrahydrobiopterin. Circulation 94, 1423-1429.
66. Tsutsui, M., Milstien, S. and Katusic, Z. S. (1996) Effect of tetrahydrobiopterin on endothelial function in canine middle cerebral arteries. Circ. Res. 79, 336-342.
67. 4B promotes assembly of enzyme subunits into an active dimer. Proc. natn. Acad. Sci. U.S.A. 92, 11771-11775.
68. Tzeng, E., Shears II, L. L., Robbins, P. D., Pitt, B. R., Geller, D. A., Watkins, S. C., Simmons, R. L. and Billiar, T. R. (1996) Vascular gene transfer of the human inducible nitric oxide synthase: characterization of activity and effects on myointimal hyperplasia. Mol. Med. 2, 211-225.
69. Van Amsterdam, J. G. C. and Wemer, J. (1992) Tetrahydrobiopterin induces vasodilation via enhancement of cGMP level. Eur. J. Pharmacol. 215, 349-350.
70. Venema, R. C., Ju, H., Zou, R., Ryan, J. W. and Venema, V. J. (1997) Subunit interactions of endothelial nitric oxide synthase. Comparisons to the neuronal and inducible nitric oxide synthase isoforms. J. Biol. Chem. 272, 1276-1282.
71. Watkins, L. D. (1995) Nitric oxide and cerebral blood flow: an update. Cerebrovasc. Brain Metab. Rev. 7, 324-337.
72. Werner-Felmayer, G. and Gross, S. S. (1966) Analysis of tetrahydrobiopterin and its role in nitric oxide synthesis. In: Methods in Nitric Oxide Research, pp. 271-299. Eds M. Feelisch and J. S. Stamler. John Wiley and Sons: New York.
73. Werner-Felmayer, G., Werner, E. R., Fuchs, D., Hausen, A., Reibnegger, G., Schmidt, K., Weiss, G. and Wachter, H. (1993) Pteridine biosynthesis in human endothelial cells: impact on nitric oxide-mediated formation of cyclic GMP. J. Biol. Chem. 268, 1842-1846.
74. White, K. A. and Marletta, M. A. (1992) Nitric oxide synthase is a cytochrome P-450 type hemoprotein. Biochemistry 31, 6627-6631.
75. Wittenveen, C. F. B., Giovanelli, J. and Kaufman, S. (1996) Reduction of quinonoid dihydrobiopterin to tetrahydrobiopterin by nitric oxide synthase. J. Biol. Chem. 271, 4143-4147.
76. Wong, G. H. W. and Goeddel, D. V. (1988) Induction of manganous superoxide dismutase by tumor necrosis factor: possible protective mechanism. Science 242, 941-944.
77. Xie, Q. W., Cho, H. J., Calaycay, J., Mumford, R. A., Swiderek, K. M., Lee, T. D., Ding, A., Troso, T. and Nathan, C. (1992) Cloning and characterization of inducible nitric oxide synthase from mouse macrophages. Science 256, 225-228.