The role of 6R-tetrahydrobiopterin in the nervous system

Progress in Neurobiology

Volumn 61, Issue 4, 2000, Pages 415-438

  Koshimura, Kunio ^a   Murakami, Yoshio ^a   Tanaka, Junko ^a   Kato, Yuzuru ^a  

^a SHIMANE UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CHANNEL; DOPAMINE; MITOGEN ACTIVATED PROTEIN KINASE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; OXYGENASE; TETRAHYDROBIOPTERIN;

ALZHEIMER DISEASE; ANIMAL CELL; APOPTOSIS; AUTOOXIDATION; DOPAMINE RELEASE; MEMBRANE DEPOLARIZATION; MEMBRANE POTENTIAL; NERVOUS SYSTEM; NEUROPROTECTION; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; RAT; REVIEW;

ANIMALS; BIOPTERIN; CALCIUM CHANNELS; CELL SURVIVAL; DOPAMINE; NERVOUS SYSTEM; NITRIC OXIDE; PC12 CELLS; RATS;

EID: 0034015709     PISSN: 03010082     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0301-0082(99)00059-3     Document Type: Review

References (117)

1. Anastasidias P.Z., Kuhn D.M., Levine R.A. Tetrahydrobiopterin uptake into rat brain synaptosomes, cultured PC12 cells, and rat striatum. Brain Res. 665:1994;77-84.
2. Anastasidias P.Z., States J.C., Imerman B.A., Louie M.C., Kuhn D.M., Levine R.A. Mitogenic effects of tetrahydrobiopterin in PC12 cells. Mol Pharmacol. 49:1996;149-155.
3. Anastasidias P.Z., Bezin L., Imerman B.A., Kuhn D.M., Louie M.C., Levine R.A. Tetrahydrobiopterin as a mediator of PC12 cell proliferation induced by EGF and NGF. Eur. J. Neurosci. 9:1997;1831-1837.
4. Artalejo C.R., Ariano M.A., Perlman R.L., Fox A.P. Activation of facilitation calcium channels in chromaffin cells by D1 dopamine receptors through a cAMP/protein kinase A-dependent mechanism. Nature. 348:1990;239-242.
5. Bailey S.W., Dillard S.B., Ayling J.E. Role of C6 chirality of tetrahydrobiopterin cofactor in catalysis and regulation of tyrosine and phenylalanine hydroxylases. Biochemistry. 30:1991;10226-10235.
6. Batistatou A., Greene L.A. Internucleosomal DNA cleavage and neuronal cell survival/death. J. Cell Biol. 122:1993;523-532.
7. Bonfoco E., Krainc D., Ankarcrona M., Nicotera P., Lipton S.A. Apoptosis and necrosis: Two distinct events induced respectively by mild and intense insults with N-methyl-D-aspartate or nitric oxide/superoxide in cortical cell cultures. Proc. Natl. Acad. Sci. USA. 92:1995;7162-7166.
8. Brenneman A.R., Kaufman S. The role of tetrahydropteridines in the enzymatic conversion of tyrosine to 3,4-dihydroxyphenylalanine. Biochem. Biophys. Res. Commun. 17:1964;177-183.
9. Brüne B., Götz C., Meßmer U.K., Sandau K., Hirvonen M.-R., Lapetina E.G. Superoxide formation and macrophage resistance to nitric oxide-mediated apoptosis. J. Biol. Chem. 272:1997;7253-7258.
10. Bullard W.P., Guthrie P.B., Russo P.V., Mandell A.J. Regional and subcellular distribution and some factors in the regulation of reduced pterins in the brain. J. Pharmacol. Exp. Ther. 205:1978;4-20.
11. Chao C.C., Hu S., Molitor T.W., Shaskan E.G., Peterson P.K. Activated microglia mediate neuronal cell injury via a nitric oxide mechanism. J. Immunol. 149:1992;2736-2741.
12. Cho S., Volpe B.T., Bae Y., Hwang O., Choi H.J., Gal J., Park L.C.H., Chu C.K., Du J., Joh T.H. Blockade of tetrahydrobiopterin synthesis protects neurons after transient forebrain ischemia in rat: a novel role for the cofactor. J. Neurosci. 19:1999;878-889.
13. Collins F., Schmidt M.F., Guthrie P.B., Kater S.B. Sustained increase in intracellular calcium promotes neuronal survival. J. Neurosci. 11:1991;2582-2587.
14. Corrazilia I.M., Campo M.L., Fuentes J.M., Campos-Portuguez S., Soler G. Parallel induction of nitric oxide and glucose-6-phosphate dehydrogenase in activated bone marrow derived macrophages. Biochem. Biophys. Res. Commun. 196:1993;342-347.
15. Creedom D.J., Johnson E.M. Jr, Lawrence J.C. Jr. Mitogen-activated protein kinase-independent pathways medicate the effects of nerve growth factor and cAMP on neuronal survival. J. Biol. Chem. 271:1996;20713-20718.
16. Curtius, H.-C., Niederwieser, A., Levine, R.A., Lovenberg, W., Woggon, B., Angst, J., 1983. Successful treatment of depression with tetrahydrobiopterin, Lancet I 657-658.
17. Dawson V.L., Dawson T.M., London E.D., Bredt D.S., Snyder S.H. Nitric oxide mediates glutamate neurotoxicity in primary cortical cultures. Proc. Natl. Acad. Sci. USA. 88:1991;6368-6371.
18. Dawson T.M., Dawson V.L., Snyder S.H. Molecular mechanisms of nitric oxide actions in the brain. Ann. NY Acad. Sci. 738:1994;76-85.
19. Estévez A.G., Radi R., Barbeito L., Shin J.T., Thompson J.A., Beckman J.S. Peroxynitrite-induced cytotoxicity in PC12 cells: evidence for an apoptotic mechanism differentially modulated by neurotrophic factors. J. Neurochem. 65:1995;1543-1550.
20. Evans T.J., Buttery L.D.K., Carpenter A., Springall D.R., Polak J.M., Cohen J. Cytokine-treated human neutrophils contain inducible nitric oxide synthase that produces nitration of ingested bacteria. Proc. Natl. Acad. Sci. USA. 93:1996;9553-9558.
21. Ferrante R.J., Kowall N.W., Beal M.F., Richardson E.P. Jr, Bird E.D., Martin J.B. Selective sparing of a class of striatal neurons in Huntington's disease. Science. 230:1985;561-563.
22. 2+-dependent routes to ras: mechanisms for neuronal survival differentiation and plasticity? Neuron. 16:1996;233-236.
23. Fournier F., Bourinet E., Nargeot J., Charnet P. Cyclic AMP-dependent regulation of P-type calcium channels expressed in Xenopus oocytes. Pflüger Arch. Eur. J. Physiol. 423:1993;173-180.
24. Franklin J.L., Johnson E.M. Jr. Suppression of programmed neuronal death by sustained elevation of cytoplasmic calcium. Trends Neurosci. Carcia-Cardena, G. 15:1992;501-508.
25. Fujishiro K.-I., Hagihara M., Takahashi A., Nagatsu T. Concentrations of neopterin and biopterin in the cerebrospinal fluid of patients with Parkinson's disease. Biochem. Med. Metabol. Biol. 44:1990;97-100.
26. Fukuda M., Gotoh Y., Tachibana T., Dell K., Hattori S., Yoneda Y., Nishida E. Induction of neurite outgrowth by MAP kinase in PC12 cells. Oncogene. 11:1995;239-244.
27. Fukushima T., Nixon J.C. Analysis of reduced forms of biopterin in biological tissues and fluids. Anal. Biochem. 102:1980;176-188.
28. Furukawa Y., Kondo T., Nishi K., Yokochi F., Narabayashi H. Total biopterin levels in the ventricular CSF of patients with Parkinson's disease: a comparison between akineto-rigid and tremor types. J. Neurol. Sci. 103:1991;232-237.
29. Galli C., Meucci O., Scorziello A., Werge T.M., Calissano P., Schettini G. Apoptosis in cerebellar granule cells is blocked by high KCl forskoline and IGF-1 through distinct mechanisms of action: the involvement of intracellular calcium and RNA synthesis. J. Neurosci. 15:1995;1172-1179.
30. Gallo V., Kingsbury A., Balázs R., Jørgensen O.S. The role of depolarization in the survival and differentiation of cerebellar granule cells in culture. J. Neurosci. 7:1987;2203-2213.
31. Hasegawa H., Imaizumi S., Ichiyama A., Sugimoto T., Matsuura S., Oka K., Kato T., Nagatsu T., Akino M. Cofactor activity of diastereoisomers of tetrahydrobiopterin. Kisliuk R.L., Brown G.M. Chemistry and Biology of Pteridines. 1979;183-188 Elsevier-North Holland, New York.
32. 2+/calmodulin-dependent protein kinase activity. Neuroscience. 57:1993;9-20.
33. Jacobson M.D. Reactive oxygen species and programmed cell death. Trends Biochem. Sci. 21:1996;83-86.
34. Johnson E.M. Jr, Koike T., Franklin J. A "calcium set-point hypothesis" of neuronal dependence on neurotrophic factor. Exp. Neurol. 115:1992;163-166.
35. Kaufman S. Studies on the mechanism of the enzymatic conversion of phenylalanine to tyrosine. J. Biol. Chem. 234:1959;2677-2682.
36. Kay A.D., Milstien S., Kaufman S., Creasey H., Hazby J.U., Cutler N.R., Rapoport S.I. Cerebrospinal fluid biopterin is decreased in Alzheimer's disease. Arch. Neurol. 43:1986;996-999.
37. Kew J.N.C., Smith D.W., Sofroniew M.V. Nerve growth factor withdrawal induces the apoptotic death of developing septal cholinergic neurons in vitro protection by cyclic AMP analogue and high potassium. Neuroscience. 70:1996;329-339.
38. Klatt P., Schmid M., Leopold E., Schmidt K., Werner E.R., Mayer B. The pteridine binding site of brain nitric oxide synthase - tetrahydrobiopterin binding kinetics specificity and allosteric interaction with the substrate domain. J. Biol. Chem. 269:1994;13861-13866.
39. 2+ determine nerve growth factor dependence of sympathetic ganglion cells. Proc. Natl. Acad. Sci. USA. 86:1989;6421-6425.
40. 2+. Proc. Natl. Acad. Sci. USA. 88:1991;3892-3896.
41. Koshimura K., Miwa S., Lee K., Fujiwara M., Watanabe Y. Enhancement of dopamine release in vivo from the rat striatum by dialytic perfusion of 6R-L-erythro-5,6,7,8-tetrahydrobiopterin. J. Neurochem. 54:1990;1391-1397.
42. 4: direct stimulation of dopamine release in the brain. Blau N., Curtius H.-C., Levine R.A., Cotton R.G.H. Pteridines and Biogenic Amines in Neurology, Pediatrics, and Immunology. 1991;299-312 Lakeshore Publishing Company, Grosse Pointe.
43. Koshimura K., Miwa S., Watanabe Y. Dopamine releasing action of 6R-L-erythro-tetrahydrobiopterin: analysis of its action site using sepiapterin. J. Neurochem. 63:1994;649-654.
44. Koshimura K., Takagi Y., Miwa S., Kido T., Watanabe Y., Murakami Y., Kato Y., Masaki T. Characterization of a dopamine releasing action of 6R-L-erythro-tetrahydrobiopterin: comparison with a 6S-form. J. Neurochem. 65:1995;827-830.
45. Koshimura K., Murakami Y., Tanaka J., Kato Y. Self-protection of PC12 cells by 6R-tetrahydrobiopterin from nitric oxide toxicity. J. Neurosci. Res. 54:1998;664-672.
46. Koshimura K., Tanaka J., Murakami Y., Kato Y. Enhancement of neuronal survival by 6R-tetrahydrobiopterin. Neuroscience. 88:1999;561-569.
47. Koshimura K., Tanaka J., Murakami Y., Kato Y. Effect of tetrahydrobiopterin on dopamine release from PC12 cells. Biomed. Res. 20:1999;141-144.
48. Koshimura K., Murakami Y., Sohmiya M., Tanaka J., Kato Y. Effects of erythropoietin on neuronal activity. J. Neurochem. 72:1999;2565-2572.
49. Kowall N.W., Beal M.F. Cortical somatostatin, neuropeptide Y, and NADPH diaphorse neurons: Normal anatomy and alterations in Alzheimer's disease. Ann. Neurol. 23:1988;105-114.
50. Kwon N.S., Nathan C.F., Stuehr D.J. Reduced biopterin as a cofactor in the generation of nitrogen oxides by murine macrophages. J. Biol. Chem. 264:1989;20496-20501.
51. 2+ channels. Nature. 335:1988;249-251.
52. Lasher R.S., Zagon L.S. The effect of potassium on neuronal differentiation in cultures of dissociated newborn rat cerebellum. Brain Res. 41:1972;482-488.
53. Lassmann H., Bancher C., Breitschopf H., Wegiel J., Bobinski M., Jellinger K., Wisniewski H.M. Cell death in Alzheimer's disease evaluated by DNA fragmentation in situ. Acta Neuropathologica. 89:1995;35-41.
54. Levine R.A., Miller L.P., Lovenberg W. Tetrahydrobiopterin in striatum localization in dopamine nerve terminals and role in catecholamine synthesis. Science. 214:1981;919-921.
55. Levine R.A. Tetrahydrobiopterin and biogenic amine metabolism in neuropsychiatry immunology and aging. Ann. NY Acad. Sci. 521:1988;129-139.
56. Levine R.A., Zoephel G.P., Niederwieser A., Curtius H.C. Entrance of tetrahydrobiopterin derivatives in brain after peripheral administration effect on biogenic metabolism. J. Pharmacol. Exp. Ther. 242:1987;514-522.
57. Lewis R.S., Tamir S., Tannenbaum S.R., Deen W.M. Kinetic analysis of the fate of nitric oxide synthesized by macrophages in vitro. J. Biol. Chem. 270:1995;29350-29355.
58. LeWitt P.A., Miller L.P., Levine R.A., Lovenberg W., Newman R.P., Papavasiliou A., Rayes A., Eldridge R., Burns R.S. Pterin abnormalities in dystonia: A metabolic marker with therapeutic implications. Adv. Neurol. 50:1988;193-201.
59. Liang L.P., Kaufman S. The regulation of dopamine release from striatum slices by tetrahydrobiopterin and L-arginine-derived nitric oxide. Brain Res. 800:1998;181-186.
60. Lipton S.A., Choi Y.B., Pan Z.H., Lei S.Z., Chen H.S.V., Sucher N.J., Lascalzo J., Singel D.J., Stamler J.S. A redox-based mechanism for the neuroprotective and neurodestructive effects of nitric oxide and related nitroso-compounds. Nature. 364:1993;626-631.
61. Lovenberg W., Jequier E., Sjoerdsma A. Tryptophan hydroxylation: measurement in pineal gland brainstem and carcinoid tumor. Science. 155:1967;217-219.
62. Lovenberg W., Levine R.A., Robinson D.S., Ebert M., Kalne A.C., Kalne D.B. Hydroxylase cofactor activity in cerebrospinal fluid of normal subjects and patients with Parkinson's disease. Science. 204:1979;624-626.
63. Lowenstein C.J., Snyder S.H. Nitric oxide, a novel biogenic messenger. Cell. 70:1992;705-707.
64. Mataga N., Imamura K., Watanabe Y. 6R-tetrahydrobiopterin perfusion enhances dopamine, serotonin, and glutamate outputs in dialysate from rat striatum and frontal cortex. Brain Res. 551:1991;64-71.
65. 2+/calmodulin-dependent nitric oxide synthase from porcine cerebellum. Cofactor-role of tetrahydrobiopterin. FEBS Lett. 227:1990;215-219.
66. Mayer B., John M., Heinzel B., Werner E.R., Wachter H., Schltz G., Böhme E. Brain nitric oxide synthase is a biopterin- and flavin-containing multi-functional oxide-reductase. FEBS Lett. 288:1991;187-191.
67. Mayer B., Klatt P., Werner E.R., Schmidt K. Kinetics and mechanism of tetrahydrobiopterin-induced oxidation of nitric oxide. J. Biol. Chem. 270:1995;665-669.
68. McCall T., Vallance P. Nitric oxide takes centre-stage with newly defined roles. Trends Pharmacol Sci. 13:1992;1-6.
69. McMillian M., Kong L.-Y., Sawin S.-M., Wilson B., Das K., Hudson P., Hong J.-S., Bing G. Selective killing of cholinergic neurons by microglial activation in basal forebrain mixed neuronal/glial cultures. Biochem. Biophys. Res. Commun. 215:1995;572-577.
70. Mensner P.W., Winters T.R., Greeen S.H. Nerve Growth factor withdrawal-induced cell death in neuronal PC12 cells resembles that in sympathetic neurons. J. Cell Biol. 119:1992;1669-1680.
71. Minami M., Takahashi T., Maruyama W., Takahashi A., Nagatsu T., Naoi M. Allosteric effect of tetrahydrobiopterin cofactors on tyrosine hydroxylase activity. Life Sci. 50:1992;15-20.
72. Miwa S., Watanabe Y., Hayaishi O. 6R-L-erythro-Tetrahydrobiopterin as a regulator of dopamine and serotonin biosynthesis in the rat brain. Arch. Biochem. Biophys. 239:1985;234-241.
73. + and cyclic AMP in the presence or absence of NGF. Eur. J. Neurosci. 5:1993;1261-1272.
74. Nagatsu T., Levitt M., Udenfriend S. Tyrosine hydroxylase. The initial step in norepinephrine biosynthesis. J. Biol. Chem. 239:1964;2910-2917.
75. Nagatsu Y., Yamaguchi T., Katyo T., Sugimoto T., Matsuura S., Akino M., Nagatsu I., Iizuka R., Narabayashi H. Biopterin in human brain and urine from control and Parkinsonism patients: application of a new radioimmunoassay. Clin. Chim. Acta. 661:1981;45-53.
76. Nagatsu T., Yamaguchi T., Rahman M.K., Trocewicz J., Oka K., Hirota Y., Nagatsu I., Narabayashi H., Kondo T., Iizuka R. Catecholamine-related enzymes and the biopterin cofactor in Parkinson's disease and related extrapyramidal diseases. Hassler R.G., Christ J.F. Advanced in Neurology. 1984;467-473 Raven Press, New York.
77. Naruse H., Hayashi T., Takesada M., Nakane A., Yamazaki K., Noguchi T., Watanabe Y., Hayaishi O. Therapeutic effect of tetrahydrobiopterin in infantile autism. Proc. Japan Acad. 63:(B):1987;231-233.
78. Niederwieser A., Blau N., Wang M., Joller P., Atares M., Cardesa-Garcia J. GTP cyclohydrolase I deficiency a new enzyme defect causing hyperphenylalaninemia with neopterin, biopterin, dopamine, and serotonin deficiencies and muscular hypotonia. Eur. J. Pediatr. 141:1984;208-214.
79. Niederwieser A., Leimbacher W., Curtius H.-C., Pronzone A., Rey F., Leupold D. Atypical phenylketonuria with "dihydrobiopterin synthase" deficiency absence of phosphate-eliminating enzyme activity demonstrated in liver. Eur. J. Pediatr. 144:1985;13-16.
80. Numata T., Kato T., Nagatsu T., Sugimoto T., Matsuura S. Effects of stereochemical structures of tetrahydrobiopterin on tyrosine hydroxylase. Biochim. Biophys. Acta. 480:1977;104-112.
81. 2+ antagonist in bovine cultured adrenal chromaffin cells. Br. J. Pharmacol. 103:1991;1889-1892.
82. Ohue T., Koshimura K., Lee K., Watanabe Y., Miwa S. A novel action of 6R-L-erythro-tetrahydrobiopterin a cofactor for hydroxylases of phenylalanine tyrosine and tryptophan: enhancement of acetylcholine release in vivo in the rat hippocampus. Neurosci. Lett. 128:1991;93-96.
83. Ohue T., Koshimura K., Akiyama Y., Ito A., Kido T., Takagi Y., Miwa S. Regulation of acetylcholine release in vivo from rat hippocampus by monoamines as revealed by novel column-switching HPLC with electrochemical detection. Brain Res. 572:1992;340-344.
84. Ohue T., Koshimura K., Akiyama Y., Watanabe Y., Miwa S. Monoamine-mediated enhancement of acetylcholine release in rat hippocampus by 6R-L-erythro-tetrahydrobiopterin. Brain Res. 570:1992;173-179.
85. Oka K., Kato T., Sugimoto T., Matsuura S., Nagatsu T. Kinetic properties of tyrosine hydroxylase with natural tetrahydropterin as a cofactor. Biochem. Biophys. Acta. 661:1981;45-53.
86. Palmer R.M.J., Ferrige A.G., Moncada S. Nitric oxide release acounts for the biological activity of endothelium-derived relaxing factor. Nature. 327:1987;524-526.
87. Portera-Cailliau C., Hedreen J.C., Price D.L., Koliatsos V.E. Evidence for apoptotic cell death in Huntington disease and excitotoxic animal models. J. Neurosci. 15:1995;3775-3787.
88. Pryor W.A., Squadrito G.L. The chemistry of peroxynitrite: A product from the reaction of nitric oxide and superoxide. Am. J. Physiol. 268:1995;L699-L722.
89. Reid J.J., Beart P.M., Marley P.D. NO problems down-under. Trends Pharmacol. Sci. 17:1996;205-208.
90. Rosen L.B., Ginty D.D., Weber M.J., Greenberg M.E. Membrane depolarization and calcium influx stimulate MEK and MAP kinase via activation of Ras. Neuron. 12:1994;1207-1221.
91. Rosen L.B., Greenberg M.E. Stimulation of growth factor receptor signal transduction by activation of voltage-sensitive calcium channels. Proc. Natl. Acad. Sci. USA. 93:1996;1113-1118.
92. Rusanescu G., Qi H., Thomas S.M., Brugge J.S., Halegoua S. Calcium influx induces neurite growth through a Src-Ras signaling cassette. Neuron. 15:1995;1415-1425.
93. Sakai N., Kaufman S., Milstein S. Tetrahydrobiopterin is required for cytokine-induced nitric oxide production in a murine macrophage cell line (RAW 264). Mol. Pharmacol. 43:1993;6-10.
94. Sakai N., Kaufman S., Milstein S. Parallel induction of nitric oxide and tetrahydrobiopterin synthesis by cytokines in rat glial cells. J. Neurochem. 65:1995;895-902.
95. Schmidt H.H.H.W., Walter U. NO at work. Cell. 78:1994;919-925.
96. Schreiber S.S., Baudry M. Selective neuronal vulnerability in the hippocampus - a role for gene expression. Trends Neurosci. 18:1995;446-451.
97. 2+ channels due to phosphorylation by cAMP-dependent protein kinase. Nature. 364:1993;240-243.
98. 2+ channels in neurons of rat dorsal motor nucleus of the vagus. Biochem. Biophys. Res. Comm. 221:1996;181-185.
99. Smith, I., Clayton, B.E., Wolff, O.H., 1975. New variant of phenylketonuria with progressive neurological illness unresponsive to phenylalanine restriction, Lancet I 1108-1111.
100. Snyder S.H., Bredt D.S. Nitric oxide as a neuronal messenger. Trends Pharmacol. Sci. 12:1991;125-128.
101. Stamler J.S. Redox signaling: nitrosylation and related target interactions of nitric oxide. Cell. 78:1994;931-936.
102. Su J.H., Anderson A.J., Cummings B.J., Cotman C.W. Immunohistochemical evidence for apoptosis in Alzheimer's disease. Neuroreport. 5:1994;2529-2533.
103. Tanaka J., Koshimura K., Murakami Y., Sohmiya M., Yanaihara N., Kato Y. Neuronal protection from apoptosis by pituitary adenylate cyclase activating polypeptide. Regulat. Pept. 72:1997;1-8.
104. Thompson C.B. Apoptosis in the pathogenesis and treatment of disease. Science. 267:1995;1456-1462.
105. Troy C.M., Derossi D., Prochiantz A., Greene L.A., Shelanski M.L. Down regulation of Cu/Zn superoxide dismutase leads to cell death via the nitric oxide-peroxynitrite pathway. J. Neurosci. 16:1996;253-261.
106. Uemura Y., Kowall N.W., Beal M.F. Selective sparing of NADPH-diaphorase-somatostatin-neuropeptide Y neurons in ischemic gerbil striatum. Ann. Neurol. 27:1990;620-625.
107. 2+ current in smooth muscle cells by diacylglycerol and acetylcholine. FASEB J. 2:1988;2497-2504.
108. + and phorbol ester activate protein kinase C and support the survival of chick sympathetic neurons in culture. J. Neurochem. 51:1988;975-983.
109. Walter R., Schffner A., Blau N., Kierat L., Schoedon G. Tetrahydrobiopterin is a secretary product of murine vascular endothelial cells. Biochem. Biophys. Res. Commun. 203:1994;1522-1526.
110. Wang Y., Townsend C., Rosenberg R.L. Regulation of cardiac L-type Ca channels in planar lipid bilayers by G proteins and protein phosphorylation. Am. J. Physiol. 264:1993;C1473-C1479.
111. Wheeler, M.A., Smith, S.D., Garcia-Cardena, Nathan, C.F., Weiss, R.M., Sessa, W.C., 1997. Bacterial infection induces nitric oxide synthase in human neutrophils, J. Clin. Invest. 99, 110-116.
112. Williams, A.C., Eldridge, R., Levine, R.A., Lovenberg, W., Paulson, G., 1979. Low CSF hydroxylase cofactor (tetrahydrobiopterin) levels in inherited dystonia. Lancet II 410-411.
113. Williams A.C., Levine R.A., Calne D.B., Chase T.N., Lovenberg W. CSF hydroxylase cofactor levels in some neurological diseases. J. Neurol. Neurosurg. Psychiatry. 43:1980;735-738.
114. Wolf W.A., Ziaja E., Arthur R.A. Jr, Anastasidias P.Z., Levine R.A., Kuhn D.M. Effect of tetrahydrobiopterin on serotonin synthesis release and metabolism in superfused hippocampal slices. J. Neurochem. 57:1991;1191-1197.
115. Yang J., Tsien R.W. Enhancement of N- and L-type calcium currents by protein kinase C in frog sympathetic neurons. Neuron. 10:1993;127-136.
116. Zhu X.-Z., Luo L.-G. Effect of nitroprusside (nitric oxide) on endogenous dopamine release from rat striatal slices. J. Neurochem. 59:1992;932-935.
117. Zirrgiebel U., Ohga Y., Carter B., Berninger B., Inagaki N., Thonene H., Lindholm D. Characterization of Trk Breceptor-mediated signaling pathways in rat cerebellar granule neurons: involvement of protein kinase C in neuronal survival. J. Neurochem. 65:1995;2241-2250.