Regulation of Nitric Oxide Synthase by Calmodulin

Calmodulin and Signal Transduction

Volumn , Issue , 2012, Pages 287-345

  Hu, Jingru ^a   Van Eldik, Linda J ^a,b  

^a NORTHWESTERN UNIVERSITY   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 0345508424     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1016/B978-0-08-092636-0.50010-4     Document Type: Chapter

References (196)

1. Abu-Soud H.M., Stuehr D.J. Nitric oxide synthases reveal a role for calmodulin in controlling electron transfer. J. Biol. Chem. 1993, 269:32047-32050.
2. Abu-Soud H.M., Yoho L., Stuehr D.J. Calmodulin controls neuronal nitricoxide synthase by a dual mechanism. Proc. Nat. Acad. Sci. U.S.A. 1994, 90:10769-10772.
3. Albina J.E., Mills C.D., Henry W.L., Caldwell M.D. Temporal expression of different pathways of L-arginine metabolism in healing wounds. J. Immunol. 1990, 144:3877-3880.
4. Anagli J., Hofmann F., Quadroni M., Vorherr T., Carafoli E. The calmodulinbinding domain of the inducible (macrophage) nitric oxide synthase. Eur. J. Biochem. 1995, 233:701-708.
5. Arnold W.P., Mittal C.K., Katsuki S., Murad F. Nitric oxide activates guanylate cyclase and increases guanosine 3',5'-cyclic monophosphate levels in various tissue preparations. Proc. Natl. Acad. Sci. U.S.A. 1977, 74:3203-3207.
6. Baek K.J., Thiel B.A., Lucas S., Stuehr D.J. Macrophage nitric oxide synthase subunits. J. Biol. Chem. 1993, 268:21120-21129.
7. Berridge M.J. Inositol trisphosphate and calcium signalling. Nature (London) 1993, 361:315-325.
8. Bliss T.V.P., Collingridge G.L. A synaptic model of memory: Long-term potentiation in the hippocampus. Nature (London) 1993, 361:31-39.
9. Blumenthal D.K., Takio K., Edelman A.M., Charbonneau H., Titani K., Walsh K.A., Krebs E.G. Identification of the calmodulin-binding domain of skeletal muscle myosin light chain kinase. Proc. Natl. Acad. Sci. U.S.A. 1985, 82:3187-3191.
10. Bogdan C., Vodovotz Y., Paik J., Xie Q.W., Nathan C. Mechanism of ce:suppression of nitric oxide synthase expression by interleukin-4 in primary mouse macrophages. J. Leukocyte Biol. 1994, 55:227-233.
11. Bredt D.S., Snyder S.H. Isolation of nitric oxide synthetase, a calmodulinrequiring enzyme. Proc. Natl. Acad. Sci. U.S.A. 1990, 87:682-685.
12. Bredt D.S., Snyder S.H. Nitric oxide: A physiologic messenger molecule. Annu. Rev. Biochem. 1994, 63:175-195.
13. Bredt D.S., Hwang P.M., Glatt C., Lowenstein C., Reed R.R., Snyder S.H. Cloned and expressed nitric oxide synthase structurally resembles cytochrome P-450 reductase. Nature (London) 1991, 351:714-718.
14. Bredt D.S., Ferris C.D., Snyder S.H. Nitric oxide synthase regulatory sites: Phosphorylation by cyclic AMP-dependent protein kinase C, and calcium-calmodulin protein kinase; identification of flavin and calmodulin binding sites. J. Biol. Chem. 1992, 267:10976-10981.
15. Brenman J.E., Chao D.S., Xia H., Aldape K., Bredt D.S. Nitric oxide synthase complexed with dystrophin and absent from skeletal muscle sarcolemma in Duchenne muscular dystrophy. Cell (Cambridge, Mass.) 1995, 82:743-752.
16. Brenman J.E., Chao D.S., Gee S.H., McGee A.W., Craven S.E., Santillano D.R., Wu Z., Wang F., Xia H., Peters M.F., Froehner S.C., Bredt D.S. Interaction of nitric oxide synthase with the postsynaptic density protein PSD-95 and α-1 syntrophin mediated by PDZ motifs. Cell (Cambridge, Mass.) 1996, 84:757-767.
17. Brüne B., Lapetina E.G. Phosphorylation of nitric oxide synthase by protein kinase A. Biochem. Biophys. Res. Commun. 1991, 181:921-926.
18. Busconi L., Michel T. Endothelial nitric oxide synthase. N-terminal myristoylation determines subcellular localization. J. Biol. Chem. 1993, 268:8410-8413.
19. Busse R., Mülsch A. Calcium-dependent nitric oxide synthesis in endothelial cytosol is mediated by calmodulin. FEBS Lett. 1990, 265:133-136.
20. Cetkovic-Cvrlje M., Sandler S., Eizirik D.L. Nicotinamide and dexamethasone inhibit interleukin-1-induced nitric oxide production by RINm5F cells without decreasing messenger ribonucleic acid expression for nitric oxide synthase. Endocrinology (Baltimore) 1993, 133:1739-1743.
21. Chartrain N.A., Geller D.A., Koty P.P., Sitrin N.F., Nussler A.K., Hoffman E.P., Billiars T.R., Hutchinson N.I., Mudgett J.S. Molecular cloning, structure and chromosomal localization of the human inducible nitric oxide synthase gene. J. Biol. Chem. 1994, 269:6765-6772.
22. Chattopadhyaya R., Meador W.E., Means A.R., Quiocho F.A. Calmodulin structure refined at 1.7 Å resolution. J. Mol. Biol. 1992, 228:1177-1192.
23. Chen Y., Rosazza J.P.N. Oligopeptides as substrates and inhibitors for a new constitutive nitric oxide synthase from rat cerebellum. Biochem. Biophys. Res. Commun. 1996, 224:303-308.
24. Cho H.J., Xie Q.-W., Calaycay J., Mumford R.A., Swiderek K.M., Lee T.D., Nathan C. Calmodulin is a subunit of nitric oxide synthase from macrophages. J. Exp. Med. 1992, 176:599-604.
25. Craescu C.T., Bouha A., Mispelter J., Diesis E., Popescu A., Chiriae M., Bârzu O. Calmodulin binding of a peptide derived from the regulatory domain of Bordetella pertussis adenylate cyclase. J. Biol. Chem. 1995, 270:7088-7096.
26. Dawson V.L., Dawson T.M., London E.D., Bredt D.S., Snyder S.H. Nitric oxide mediates glutamate neurotoxicity in primary cortical culture. Proc. Natl. Acad. Sci. U.S.A. 1991, 88:6368-6371.
27. Dawson T.M., Steiner J.P., Dawson V.L., Dinerman J.L., Uhl G.R., Snyder S.H. Immunoce:suppressant FK506 enhances phosphorylation of nitric oxide synthase and protects against glutamate neurotoxicity. Proc. Natl. Acad. Sci. U.S.A. 1993, 90:9808-9812.
28. Deguchi T., Yoshioka M. L-arginine identified as an endogenous activator for soluble guanylate cyclase from neuroblastoma cells. J. Biol. Chem. 1982, 257:10147-10152.
29. De Vera M.E., Shapiro R.A., Nussler A.K., Mudgett J.S., Simmons R.L., Morris S.M., Billiar T.R., Geller D.A. Transcriptional regulation of human inducible nitric oxide synthase (NOS2) gene by cytokines: Initial analysis of the human NOS2 promoter. Proc. Natl. Acad. Sci. U.S.A. 1996, 93:1054-1059.
30. Dinerman J.L., Steiner J.P., Dawson T.M., Dawson V., Snyder S.H. Cyclic nucleotide dependent phosphorylation of neuronal nitric oxide synthase inhibits catalytic activity. Neuropharmacology 1994, 33:1245-1251.
31. Fast D.J., Lynch R.C., Leu R.W. Cyclosporin A inhibits nitric oxide production by L929 cells in response to tumor necrosis factor and interferonγ. J. Interferon Res. 1993, 13:235-240.
32. Feinstein D.L., Galea E., Cermak J., Chugh P., Lyandvert L., Reis D.J. Nitric oxide synthase expression in glial cells: Suppression by tyrosine kinase inhibitors. J. Neurochem. 1994, 62:811-814.
33. Feron O., Belhassen B.L., Kobzik L., Smith T.W., Kleely R.A., Michel T. Endothelial nitric oxide synthase targeting to caveolae. Specific interactions with caveolin isoforms in cardiac myocytes and endothelial cells. J. Biol. Chem. 1996, 271:22810-22814.
34. Förstermann U., Gath I. Purification of nitric oxide synthase. Methods Enzymol. 1996, 268:334-339.
35. Förstermann U., Kleinert H. Nitric oxide synthase: Expression and expressional control of the three isoforms. Arch. Pharmacol. 1995, 352:351-364.
36. Förstermann U., Gorsky L.E., Pollock J.S., Ishii K., Schmidt H.H.H.W., Heller M., Murad F. Hormone-induced biosynthesis of endothelium-derived relaxing factor/nitric oxide-like material in N1E-115 neuroblastoma cells requires calcium and calmodulin. Mol. Pharmacol. 1990, 38:7-13.
37. Förstermann U., Gorsky L.E., Pollock J.S., Schmidt H.H.H.W., Heller M., Murad F. Regional distribution of EDRF/NO-synthesizing enzyme(s) in rat brain. Biochem. Biophys. Res. Commun. 1990, 168:727-732.
38. Förstermann U., Pollock J.S., Schmidt H.H.H.W., Heller M., Murad F. Calmodulin-dependent endothelium derived relaxing factor/nitric oxide synthase activity is present in the particulate and cytosolic fraction of bovine aortic endothelial cells. Proc. Natl. Acad. Sci. U.S.A. 1991, 88:1788-1792.
39. Förstermann U., Schmidt H.H.H.W., Kohlhaas K.L., Murad F. Induced RAW264.7 macrophages express soluble and particulate nitric oxide synthase: Inhibition by transforming growth factor-beta. Eur. J. Pharmacol. 1992, 225:161-165.
40. Fossetta J.D., Niu X.D., Lunn C.A., Zavodny P.J., Narula S.K., Lundell D. Expression of human inducible nitric oxide synthase in Escherichia coli. FEBS Lett. 1996, 379:135-138.
41. Fugisawa H., Ogura T., Jurashima Y., Yokoyama T., Yamashita J., Esumi H. Expression of two types of nitric oxide synthase mRNA in human neuroblastoma cell lines. J. Neurochem. 1994, 63:140-145.
42. Fukuto J.M., Chaudhuri G. Inhibition of constitutive and inducible nitric oxide synthase: Potential selective inhibition. Annu. Rev. Pharmacol. Toxicol. 1995, 35:165-194.
43. Furchgott R.F. Studies on relaxation of rabbit aorta by sodium nitrite: The basis for the proposal that the acid-activatable inhibitory factor from retracto penis is inorganic nitrite and the endothelium-derived relaxing factor is nitric oxide. "Vasodilation: Vascular Smooth Muscle, Peptides, Autonomic Nerves and Endothelium" 1988, 401-414. Raven, New York. P.M. Vanhoutte (Ed.).
44. Furchgott R.F., Zawadzki J.V. The obligatory role of endothelial cells in the relaxation of arterial smooth muscle by acetylcholine. Nature (London) 1980, 288:373-376.
45. Garry M.G., Richardson J.D., Hargreaves K.M. Sodium nitroprusside evokes the release of immunoreactive calcitonin gene-related peptide and substance P from dorsal horn slices via nitric oxide-dependent and nitric-independent mechanisms. J. Neurosci. 1994, 14:4329-4337.
46. Garthwaite J., Boulton C.L. Nitric oxide signaling in the central nervous system. Annu. Rev. Physiol. 1995, 57:683-706.
47. Garthwaite J., Charles S.J., Chess-Williams R. Endothelium-derived relaxing factor release on activation of NMDA receptors suggests role as intercellular messenger in the brain. Nature (London) 1988, 336:385-388.
48. Garvey E.P., Furfine E.S., Sherman P.A. Purification of nitric oxide synthase. Method Enzymol. 1996, 268:339-349.
49. Geng Y., Maier R., Lotz M. Tyrosine kinases are involved with the expression of inducible nitric oxide synthase in human articular chondrocytes. J. Cell. Physiol. 1995, 163:545-554.
50. George S.E., Su Z., Fan D., Means A.R. Calmodulin-cardiac troponin C chimeras. Effects of domain exchange on calcium binding and enzyme activation. J. Biol. Chem. 1993, 268:25213-25220.
51. George S.E., Su Z., Fan D., Wang S., Johnson J.D. The fourth EF-hand of calmodulin and its helix-helix components: Impact on calcium binding and enzyme activation. Biochemistry 1996, 35:8307-8313.
52. Graff J.M., Stumpo D.J., Blackshear P.J. Characterization of the phosphorylation sites in the chicken and bovine myristoylated alanine-rich C kinase substrate protein, a prominent cellular substrate for protein kinase C. J. Biol. Chem. 1989, 264:11912-11919.
53. Griffith O.W., Stuehr D.J. Nitric oxide synthases: Properties and catalytic mechanism. Annu. Rev. Physiol. 1995, 57:707-736.
54. Gross S.S., Wolin M.S. Nitric oxide: Pathophysiological mechanisms. Annu. Rev. Physiol. 1995, 57:737-769.
55. Guevara-Guzman R., Emson P.C., Kendrick K.M. Modulation of in vivo striatal transmitter release by nitric oxide and cyclic GMP. J. Neurochem. 1994, 62:807-810.
56. Haiech J., Kilhoffer M.C., Lukas T.J., Craig T.A., Roberts D.M., Watterson D.M. Restoration of the calcium binding activity of mutant calmodulins toward normal by the presence of a calmodulin binding structure. J. Biol. Chem. 1991, 266:3427-3431.
57. Hall A.V., Antoniou H., Wang Y., Cheung A.H., Arbus A.M., Olson S.L., Lu W.C., Kau C.L., Marsden P.A. Structural organization of the human neuronal nitric oxide synthase gene. J. Biol. Chem. 1994, 269:33082-33090.
58. Harrison D.G., Sayegh H., Ohara Y., Inoue N., Venema R.C. Regulation of expression of the endothelial cell nitric oxide synthase. Clin. Exp. Pharmacol. Physiol. 1996, 23:251-255.
59. Hecker M., Mülsch A., Busse R. Subcellular localization and characterization of neuronal nitric oxide synthase. J. Neurochem. 1994, 62:1524-1529.
60. Hellerman G.R., Solomonson L.P. Calmodulin promotes dimerization of the oxygenase domain of human endothelial nitric-oxide synthase. J. Biol. Chem. 1997, 272:12030-12034.
61. Herdegen T., Brecht S., Mayer B., Leah J., Kummer W., Vravo R., Zimmermann M. Long-lasting expression of JUN and KROX transcription factors and nitric oxide synthase in intrinsic neurons of the rat brain following axotomy. J. Neurosci. 1993, 13:4130-4145.
62. Hevel J.M., White K.A., Marietta M.A. Purification of the inducible macrophage nitric oxide synthase. J. Biol. Chem. 1991, 266:22789-22791.
63. Hibbs J.B., Tainer R.R., Vavrin Z. Macrophage cytotoxicity: Role for L-arginine deaminase and imino nitrogen oxidation to nitrite. Science 1987, 235:473-476.
64. Hiki K., Hattori R., Kawai C., Yui Y. Purification of insoluble nitric oxide synthase from rat cerebellum. J. Biochem. (Tokyo) 1992, 111:556-558.
65. Hope B.T., Michael G.J., Knigge K.M., Vincent S.R. Neuronal NADPH-diaphorase is a nitric oxide synthase. Proc. Natl. Acad. Sci. U.S.A. 1991, 88:2811-2814.
66. Hu J., El-Fakahany E.E. Role of intracellular and intercellular communication by nitric oxide in coupling of muscarinic receptors to activation of guanylate cyclase in neuronal cells. J. Neurochem. 1993, 61:578-585.
67. Hu J., El-Fakahany E.E. Intricate regulation of nitric oxide synthase in neurons. Cell. Signal. 1996, 8:185-189.
68. Hu J., Van Eldik L.J. S100β induces apoptotic cell death in cultured astrocytes via a nitric oxide-dependent pathway. Biochim. Biophys. Acta 1996, 1313:239-245.
69. Hu J., Lee J.-H., El-Fakahany E.E. Inhibition of neuronal nitric oxide synthase by antipsychotic drugs. Psychopharmacology 1994, 114:161-166.
70. Hu J., Castets F., Guevara J.L., Van Eldik L.J. S100β stimulates inducible nitric oxide synthase and expression of mRNA levels in rat cortical astrocytes. J. Biol. Chem. 1996, 271:2543-2547.
71. Ignarro L.J., Byrns R.E., Wood K.S. Biochemical and pharmacological properties of endothelial-derived relaxing factor and its similarity to nitric oxide radical. "Vasodilation: Vascular Smooth Muscle, Peptides, Autonomic Nerves and Endothelium" 1988, 427-436. Raven, New York. P.M. Vanhoutte (Ed.).
72. Ignarro L.J. Biosynthesis and metabolism of endothelium-derived nitric oxide. Annu. Rev. Pharmacol. Toxicol. 1990, 30:535-560.
73. Ikeda J., Ochiai K., Morita I., Murota S.-I. Endogenous nitric oxide blocks calcium influx induced by glutamate in neurons containing NADPH diaphorase. Neurosci. Lett. 1993, 158:193-196.
74. Ikura M., Clore G.M., Gronenborn A.M., Zhu G., Klee C.B., Bax A. Solution structure of a calmodulin-target peptide complex by multidimensional NMR. Science 1992, 256:632-638.
75. Ito M. Long-term depression. Annu. Rev. Neurosci. 1989, 12:85-102.
76. Iyengar R., Stuehr D.J., Marietta M.A. Macrophage synthesis of nitrite, nitrate and N-nitrosamines: Precursors and roles of the repiratory burst. Proc. Natl. Acad. Sci. U.S.A. 1987, 84:6369-6373.
77. Jones N.M., Loiacono R.E., Beart P.M. Roles for nitric oxide as an intraand interneuronal messenger at NMDA release-regulating receptors: Evidence from studies of the NMDA-evoked release of [3H]noradrenaline and D-[3H]aspartate from rat hippocampal slices. J. Neurochem. 1995, 64:2057-2063.
78. Kadowaki K., Kishimoto J., Leng G., Emson P.C. Upregulation of nitric oxide synthase (NOS) gene expression together with NOS activity in the rat hypothalamo-hypophysial system after chronic salt loading-arginine vasopressin and oxytocin secretion. Endocrinology (Baltimore) 1994, 134:1011-1017.
79. Karanth S., Lyson K., McCann S.M. Role of nitric oxide in interleukin-2 induced corticotropin-releasing factor release from incubated hypothalami. Proc. Natl. Acad. Sci. U.S.A. 1993, 88:3383-3385.
80. Kim J., Shishido T., Jiang X., Aderem A., McLaughlin S. Phosphorylation, high ionic strength, and calmodulin reverse the binding of MARCKS to phospholipid vesicles. J. Biol. Chem. 1994, 269:28214-28219.
81. Knowles R.G., Palacios M., Palmer R.M.J., Moncada S. Formation of nitric oxide from L-arginine in the central nervous system: A transduction mechanism for stimulation of the soluble guanylate cyclase. Proc. Natl. Acad. Sci. U.S.A. 1989, 86:5159-5162.
82. Kobzik L., Reid M.B., Bredt D.S., Stamler J.S. Nitric oxide in skeletal muscle. Nature (London) 1994, 372:546-548.
83. Kolyada A.Y., Savikovsky N., Madias N.E. Transcriptional regulation of the human iNOS gene in vascular smooth muscle cells and macrophages: Evidence for tissue specificity. Biochem. Biophys. Res. Commun. 1996, 220:600-605.
84. Lamas S., Marsden P.A., Li G.K., Tempst P., Michel T. Endothelial nitric oxide synthase: Molecular cloning, characterization of a distinct constitutive enzyme isoform. Proc. Natl. Acad. Sci. U.S.A. 1992, 89:6348-6352.
85. Lei S.Z., Pan Z.-H., Aggarwal S.K., Chen H.-S.V., Hartman J., Sucher N.J., Lipton S.A. Effects of nitric oxide production on the redox modulatory site of the NMDA receptor-channel complex. Neuron 1992, 8:1087-1099.
86. Lepoivre M., Chenais B., Yapo A., Lemaire G., Thelander L., Tenu J.P. Alterations of ribonucleotide reductase activity following induction of the nitritegenerating pathway in adenocarcinoma cells. J. Biol. Chem. 1990, 265:14143-14149.
87. Lipton S.A., Stamler J.S. Actions of redox-related congeners of nitric oxide at the NMDA receptor. Neuropharmacology 1994, 33:1229-1233.
88. Lipton S.A., Choi Y.B., Pan Z.-H., Lei S.Z., Chen H.S.V., Sucher N.J., Loscalzo 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 (London) 1993, 364:626-632.
89. Liu J., Sessa W.C. Identification of covalently bound amino-terminal myristic acid in endothelial nitric oxide synthase. J. Biol. Chem. 1994, 269:11691-11694.
90. Lukas T.J., Burgess W.H., Prendergast F.G., Lau W., Watterson D.M. Calmodulin binding domains: Characterization of a phosphorylation and calmodulin binding site from myosin light chain kinase. Biochemistry 1986, 25:1458-1464.
91. Lukas T.J., Mirzoeva S., Watterson D.M. Calmodulin regulation of protein kinases. Calmodulin and Signal Transduction 1998, Academic Press, Orlando, FL, (this book).
92. Mcquillan L.P., Leung G.K., Marsden P.A., Kostyk S.K., Kourembanas S. Hypoxia inhibits expression of eNOS via transcriptional and posttranscriptional mechanisms. Am. J. Physiol. 1994, 36:H1921-H1927.
93. Manzoni O., Bockaert J. Nitric oxide synthase activity endogenously modulates NMDA receptors. J. Neurochem. 1993, 61:368-370.
94. Marin P., Lafon-Cazal M., Bockaert J. A nitric oxide synthase activity selectively stimulated by NMDA receptors depends on protein kinase C activation in mouse striatal neurons. Eur. J. Neurosci. 1992, 4:425-432.
95. Marietta M.A. Nitric oxide synthase structure and mechanism. J. Biol. Chem. 1993, 268:12231-12234.
96. Marietta M.A. Nitric oxide synthase: Aspects concerning structure and catalysis. Cell (Cambridge, Mass.) 1994, 78:927-930.
97. Marsden P.A., Schappert K.T., Chen H.S., Flowers M., Sundell C.L., Wilcox J.N., Lamas S., Michel T. Molecular cloning and characterization of human endothelial nitric oxide synthase. FEBS Lett. 1992, 307:287-293.
98. Marsden P.A., Heng H.H., Scherer S.W., Stewart R.J., Hall A.V., Shi X.M., Tsui L.C., Schappert K.T. Structure and chromosomal localization of the human constitutive endothelial nitric oxide synthase gene. J. Biol. Chem. 1993, 268:17478-17488.
99. Marsden P.A., Heng H.H.Q., Duff C.L., Shi X.M., Tsui L.C., Hall A.V. Localization of the human gene for inducible nitric oxide synthase (NOS2) to chromosome 17Q11.2 -Q12. Genomics 1994, 19:183-185.
100. Martinson E.A., Trilivas I., Brown J.H. Rapid protein kinase C-dependent activation of phospholipid D leads to delayed 1,2-diglyceride accumulation. J. Biol. Chem. 1990, 265:22282-22287.
101. Martzen M.R., Slemmon J.R. The dentritic peptide neurogranin can regulate a calmodulin-dependent target. J. Neurochem. 1995, 64:92-100.
102. Matsubara M., Titani K., Taniguchi H. Interaction of calmodulin-binding domain peptides of nitric oxide synthase with membrane phospholipids: Regulation by protein phosphorylation and Ca2+-calmodulin. Biochemistry 1996, 35:14651-14658.
103. Matsumoto T., Pollock J.S., Nakane M., Förstermann U. Developmental changes of cytosolic and particulate nitric oxide synthase in rat brain. Dev. Brain Res. 1993, 73:199-203.
104. Matsuoka A., Stuehr D.J., Olson J.S., Clark P., Ikeda-Saito M. L-Arginine and calmodulin regulation of the heme iron reactivity in neuronal nitric oxide synthase. J. Biol. Chem. 1994, 269:20335-20339.
105. Mayer B., John M., Böhme E. Purification of a Ca2+/calmodulin-dependent nitric oxide synthase from porcine cerebellum. FEBS Lett. 1990, 277:215-219.
106. Meador W.E., Means A.R., Quiocho F.A. Target enzyme recognition by calmodulin: 2.4 Å structure of a calmodulin-peptide complex. Science 1992, 257:1251-1255.
107. Meador W.E., Means A.R., Quiocho F.A. Modulation of calmodulin plasticity in molecular recognition on the basis of x-ray structures. Science 1993, 262:1718-1721.
108. Michel J.B., Feron O., Sacks D., Michel T. Reciprocal regulation of endothelial nitric oxide synthase by Ca2+-calmodulin and caveolin. J. Biol. Chem. 1997, 272:15583-15586.
109. Michel T., Li G.K., Busconi L. Phosphorylation and subcellular translocation of endothelial nitric oxide synthase. Proc. Natl. Acad. Sci. U.S.A. 1993, 90:6252-6256.
110. Moncada S., Higgs A. Mechanisms of disease: The L-arginine-nitric oxide pathway. N. Engl. J. Med. 1993, 329:2002-2012.
111. Moncada S., Higgs A., Furchgott R. XIV. International union of pharmacology nomenclature in nitric oxide research. Pharmacol. Rev. 1997, 49:137-142.
112. Montague P.R., Gancayco C.D., Winn M.J., Marchase R.B., Friedlander M.J. Role of NO production in NMDA receptor-mediated neurotransmitter release in cerebral cortex. Science 1994, 263:973-977.
113. Moore P.K., Handy R.L.C. Selective inhibitors of neuronal nitric oxide synthase-is no NOS really good NOS for the nervous system?. Trends Pharmacol. Sci. 1997, 18:204-211.
114. Murphy S., Grzybicki D. Glial NO: Normal and pathological roles. Neuroscientist 1996, 2:90-99.
115. Nadaud S., Bonnardeaux A., Lahrop M., Soubrier F. Gene structure, polymorphism, and mapping of the human endothelial nitric oxide synthase gene. Biochem. Biophys. Res. Commun. 1994, 198:1027-1033.
116. Nakane M., Mitchell J., Förstermann U., Murad F. Phosphorylation by calcium calmodulin-dependent protein kinase II and protein kinase C modulates the activity of nitric oxide synthase. Biochem. Biophys. Res. Commun. 1991, 180:1396-1402.
117. Nakane M., Schmidt H.H.H.W., Pollock J.S., Förstermann U., Murad F. Cloned human brain nitric oxide synthase is highly expressed in skeletal muscle. FEBS Lett. 1993, 316:175-180.
118. Nathan C., Xie Q.-W. Regulation of biosynthesis of nitric oxide. J. Biol. Chem. 1994, 269:13725-13728.
119. Nathan C., Xie Q.-W. Nitric oxide synthase: Roles, tolls, and controls. Cell (Cambridge, Mass.) 1994, 78:915-918.
120. Nishida K., Harrison D.G., Navas J.P., Fisher A.A., Dockery S.P., Uematsu M., Nerem R.M., Alexander R.W., Murphy T.J. Molecular cloning and characterization of the constitutive bovine aortic endothelial cell nitric oxide synthase. J. Clin. Invest. 1992, 90:2092-2096.
121. Nishizuka Y. Intracellular signaling by hydrolysis of phospholipids and activation of protein kinase C. Science 1992, 258:607-614.
122. O'Dell T.J., Hawkins R.D., Kandel E.R., Arancio O. Tests of the roles of two diffusible substances in long-term potentiation: Evidence for nitric oxide as a possible early retrograde messenger. Proc. Natl. Acad. Sci. U.S.A. 1991, 88:11285-11289.
123. O'Neil K.T., DeGrado W.F. How calmodulin binds its targets: Sequence independent recognition of amphiphilic alpha-helices. Trends Biochem. Sci. 1990, 15:59-64.
124. Ohshima H., Oguchi S., Adachi H., Iida S., Suzuki H., Sugimura T., Esumi H. Purification of nitric oxide synthase from bovine brain: Immunological characterization and tissue distribution. Biochem. Biophys. Res. Commun. 1992, 183:238-244.
125. Okada O. Protein kinase C modulates calcium sensitivity of nitric oxide synthase in cerebellar slices. J. Neurochem. 1995, 64:1298-1304.
126. Palmer R.M.J., Ferrige A.G., Moncada S. Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor. Nature (London) 1987, 327:524-526.
127. Palmer R.M.J., Ashton D.S., Moncada S. Vascular endothelial cells synthesize nitric oxide from L-arginine. Nature (London) 1988, 333:664-666.
128. Pan J., Burgher K.L., Szczepanik A.M., Ringheim G.E. Tyrosine phosphorylation of inducible nitric oxide synthase: Implication for potential post-translational regulation. Biochem. J. 1996, 314:889-894.
129. Paul A., Pendreigh R.H., Plevin R. Protein kinase C and tyrosine kinase pathways regulate lipopolysaccharide-induced nitric oxide synthase activity in RAW 264.7 murine macrophage. Br. J. Pharmacol. 1995, 114:482-488.
130. Persechini A., Gansz K., Paresi R.J. Activation of myosin light chain kinase and nitric oxide synthase activities by engineered calmodulin with duplicated or exchanged EF hand pairs. Biochemistry 1996, 35:224-228.
131. Persechini A., Gansz K.J., Paresi R.J. A role in enzyme activation for the N-terminal leader sequence in calmodulin. J. Biol. Chem. 1996, 271:19279-19282.
132. Persechini A., White H.D., Gansz K.J. Different mechanisms for Ca2+ dissociation from complexes of calmodulin with nitric oxide synthase or myosin light chain kinase. J. Biol. Chem. 1996, 271:62-67.
133. Pollock J.S., Förstermann U., Mitchell J.A., Warner T.D., Schmidt H.H.H.W., Nakane M., Murad F. Purification and characterization of particulate endothelium-derived relaxing factor synthase from cultured and native bovine aortic endothelial cells. Proc. Natl. Acad. Sci. U.S.A. 1991, 88:10480-10484.
134. Rafferty S., Malech H.L. High reductase activity of recombinant NOS2 flavoprotein domain lacking the calmodulin binding regulatory sequence. Biochem. Biophys. Res. Commun. 1996, 220:1002-1007.
135. Rand M.J., Li C.B. Nitric oxide as a neurotransmitter in peripheral nerves: Nature of transmitter and mechanism of transmission. Annu. Rev. Physiol. 1995, 57:659-682.
136. Reiser G. Nitric oxide formation caused by Ca2+ release from internal stores in neuronal cell line is enhanced by cyclic AMP. Eur. J. Pharmacol. 1992, 227:89-93.
137. Rettori V., Gimeno M., Lyson K., McCann S.M. Nitric oxide mediates norepinephrine-induced prostaglandin E2 release from the hypothalamus. Proc. Natl. Acad. Sci. U.S.A. 1992, 89:11543-11546.
138. Robinson L.J., Weremowicz S., Morton C.C., Michel T. Isolation and chromosomal localization of the human endothelial nitric oxide synthase (NOS3) gene. Genomics 1994, 19:350-357.
139. Robinson L.J., Busconi L., Michel T. Agonist-modulated palmitoylation of endothelial nitric oxide synthase. J. Biol. Chem. 1995, 270:995-998.
140. Rodriguez J., Quignard J.-F., Fagni L., Lafon-Cazal M., Bockaert J. Blockade of nitric oxide synthesis by tyrosine kinase inhibitors in neurons. Neuropharmacology 1994, 33:1267-1274.
141. Ruan J., Xie Q.-W., Hutchinson N., Cho H., Wolfe G.C., Nathan C. Inducible nitric oxide synthase requires both the canonical calmodulin-binding domain and additional sequences in order to bind calmodulin and produce nitric oxide in the absence of free Ca2+. J. Biol. Chem. 1996, 271:22679-22686.
142. Schmidt H.H.H.W., Murad F. Purification and characterization of a human NO synthase. Biochem. Biophys. Res. Commun. 1991, 181:1372-1377.
143. Schmidt H.H.H.W., Wilke P., Evers B., Böhme E. Enzymatic formation of nitrogen oxides from L-arginine in bovine brain cytosol. Biochem. Biophys. Res. Commun. 1989, 165:284-291.
144. Schmidt H.H.H.W., Pollack J.S., Nakane M., Gorsky L.D., Förstermann U., Murad F. Purification of a soluble isoform of guanylyl cyclase-activating factor synthase. Proc. Natl. Acad. Sci. U.S.A. 1991, 88:365-369.
145. Schmidt H.H.H.W., Lohmann S.M., Walter U. The nitric oxide and cGMP signal transduction system: Regulation and mechanism of action. Biochim. Biophy. Acta 1993, 1178:153-175.
146. Schuman E.M., Madison D.V. A requirement for the intercellular messenger nitric oxide in long-term potentiation. Science 1991, 254:1503-1506.
147. Sessa W.C., Harrison J.K., Barber C.M., Zeng D., Durieux M.E., D'Angelo D.D., Lynch K.R., Peach M.J. Molecular cloning and expression of a cDNA encoding endothelial cell nitric oxide synthase. J. Biol. Chem. 1992, 27:15274-15276.
148. Sessa W.C., Barber C.M., Lynch K.R. Mutation of N-myristoylation site converts endothelial cell nitric oxide synthase from a membrane to a cytosolic protein. Circ. Res. 1993, 72:921-924.
149. Shaul P.W., Smart E.J., Robinson L.J., German Z., Yuhanna I.S., Ying Y, Anderson R.G.W., Michel T. Acylation targets endothelial nitric-oxide synthase to plamalemmal caveolae. J. Biol. Chem. 1996, 271:6518-6522.
150. Sheta E.A., McMillan K., Masters B.S.S. Evidence for a bidomain structure of constitutive cerebellar nitric oxide synthase. J. Biol. Chem. 1994, 269:15147-15153.
151. Shibuki K., Okada D. Endogenous nitric oxide release required for longterm synaptic depression in the cerebellum. Nature (London) 1991, 349:326-328.
152. Surichamorn W., Forray C., El-Fakahany E.E. Role of intracellular Ca2+ mobilization in muscarinic and histamine receptor-mediated activation of guanylate cyclase in N1E-115 neuroblastoma cells: Assessment of the arachidonic acid release hypothesis. Mol. Pharmacol. 1990, 37:860-869.
153. Singh K., Balligand J.-L., Fischer T.A., Smith T.W., Kelly R.A. Regulation of cytokine-inducible nitric oxide synthase in cardiac myocytes and microvascular endothelial cells. J. Biol. Chem. 1996, 271:1111-1117.
154. Slemmon J.R., Martzen M.R. Neuromodulin (GAP-43) can regulate a calmodulin-dependent target in vitro. Biochemistry 1994, 33:5653-5660.
155. Spitsin S.V., Koprowski H., Michaels F.H. Characterization and functional analysis of the human inducible nitric oxide synthase gene promoter. Mol. Med. 1996, 2:226-235.
156. Stamler J.S. Redox signaling: Nitrosylation and related target interactions of nitric oxide. Cell (Cambridge, Mass.) 1994, 78:931-936.
157. Stamler J.S., Singel D.J., Loscalzo J. Biochemistry of nitric oxide and its redox-active forms. Science 1992, 258:1898-1902.
158. Steiner J.P., Dawson T.M., Fotuhi M., Glatt C.E., Snowman A.M., Cohen N., Snyder S.H. High brain densities of the immunophilin FKBP colocalized with calcineurin. Nature (London) 1992, 358:584-587.
159. Stevens-Truss R., Marietta M.A. Interaction of calmodulin with the inducible murine macrophage nitric oxide synthase. Biochemistry 1995, 34:15638-15645.
160. Stuehr D.J. Purification and properties of nitric oxide synthase. Methods Enzymol. 1996, 268:324-333.
161. Stuehr D.J., Cho H.J., Kwon N.S., Weise M.F., Nathan C.F. Purification and characterization of the cytokine-induce macrophage nitric oxide synthase: An FAD- and FMN-containing flavoprotein. Proc. Natl. Acad. Sci. U.S.A. 1991, 88:7773-7777.
162. Su Z., Blazing M.A., Fan D., Gorge S.E. The calmodulin-nitric oxide synthase interaction. J. Biol. Chem. 1995, 270:29117-29122.
163. Suschek C., Fehsel K., Kröncke K.D., Sommer A., Kolb-Bachofen V. Primary cultures of rat islet capillary endothelial cells-constitutive and cytokineinducible macrophage-like nitric oxide synthases are expressed and activities regulated by glucose concentration. Am. J. Pathol. 1994, 145:685-695.
164. Toms N.J., Roberts P. NMDA receptor-mediated stimulation of rat cerebellar nitric oxide formation is modulated by cyclic AMP. Eur. J. Pharmacol. 1994, 266:63-66.
165. Umans J.G., Levi R. Nitric oxide in the regulation of blood flow and arterial pressure. Annu. Rev. Physiol. 1995, 57:771-790.
166. Venema R.C., Nishida K., Alexander R.W., Harrison D.G., Murphy T.J. Organization of the bovine gene encoding the endothelial nitric oxide synthase. Biochim. Biophys. Acta 1994, 1218:413-420.
167. Venema R.C., Sayegh H.S., Arnal J.-F., Harrison D.G. Role of the enzyme calmodulin-binding domain in membrane association and phospholipid inhibition of endothelial nitric oxide synthase. J. Biol. Chem. 1995, 270:14705-14711.
168. Venema R.C., Sayegh H.S., Kent J.D., Harrison D.G. Identification, characterization, and comparison of the calmodulin-binding domains of the endothelial and inducible nitric oxide synthases. J. Biol. Chem. 1996, 271:6435-6440.
169. Venema R.C., Ju H., Zou R., Ryan J.W., Venema V.J. Subunit interactions of endothelial nitric-oxide synthase. Comparison to the neuronal and inducible nitricoxide synthase isoforms. J. Biol. Chem. 1997, 272:1276-1282.
170. Vincent S.R. Nitric oxide: a radical neurotransmitter in the central nervous system. Prog. in Neurobiol. 1994, 42:129-160.
171. Vodovotz Y., Bogdan C., Paik J., Xie Q.-W., Nathan C. Mechanisms of ce:suppression of macrophage nitric oxide release by transforming growth factor β. J. Exp. Med. 1993, 178:605-613.
172. Vogel H.J. The Merck Frosst Award Lecture 1994. Calmodulin: a versatile calcium mediator protein. Biochem. Cell Biol. 1994, 72:357-376.
173. Vorherr T., Knöpfel L., Hofmann F., Mollner S., Pfeuffer T., Carafoli E. The calmodulin binding domain of nitric oxide synthase and adenylyl cyclase. Biochemistry 1993, 32:6081-6088.
174. Wang Y., Goligorsky M.S., Lin M., Wilcox J.N., Marsden P.A. A novel, testis-specific mRNA transcript encoding an NH2-terminal truncated nitric-oxide synthase. J. Biol. Chem. 1997, 272:11392-11401.
175. Watanabe Y., Terachima K., Hidaka H. Neuronal nitric oxide synthase specific autophosphorylation in baculovirus/sf9 insect cell system. Biochem. Biophys. Res. Commun. 1996, 219:638-643.
176. Weiner C.P., Lizasoain I., Baylis S.A., Knowles R.G., Charles I.G., Moncada S. Induction of calcium-dependent nitric oxide synthases by sex hormones. Proc. Natl. Acad. Sci. U.S.A. 1994, 91:5212-5216.
177. Weisz A., Oguichi S., Cicatiello L., Esumi H. Dual mechanism for the control of inducible-type NO synthase gene expression in macrophages during activation by interferon-gamma and bacterial lipopolysaccharide-transcriptional and posttranscriptional regulation. J. Biol. Chem. 1994, 269:8324-8333.
178. Wu W., Liuzzi F.J., Schinco F.P., Depto A.S., Li Y., Mong J.A., Dawson T.M., Snyder S.H. Neuronal nitric oxide synthase is induced in spinal neurons by traumatic injury. Neuroscience (Oxford) 1994, 61:719-726.
179. Wu C., Zhang J., Abu-Soud H., Ghosh D., Stuehr D.H. High-level expression of mouse inducible nitric oxide synthase in Escherichia coli requires coexpression with calmodulin. Biochem. Biophys. Res. Commun. 1996, 222:439-444.
180. Xie Q.-W., Nathan C. The high-output nitric oxide pathway: Role and regulation. J. Leukocyte Biol. 1994, 56:576-582.
181. Xie Q.-W., Cho H.J., Calaycay J., Mumford R.A., Swiderek K.M., Lee T.D., Ding A., Troso T., Nathan C. Cloning and characterization of inducible nitric oxide synthase from mouse macrophages. Science 1992, 256:225-228.
182. Xie Q.-W., Whisnant R., Nathan C. Promoter of the mouse gene encoding calcium-independent nitric oxide synthase confers inducibility by interferon gamma and bacterial lipopolysaccharide. J. Exp. Med. 1993, 177:1779-1784.
183. Xie J.L., Roddy P., Rife T.K., Murad F., Young A.P. Two closely linked but separable promoters for human neuronal nitric oxide synthase gene transcription. Proc. Natl. Acad. Sci. U.S.A. 1995, 92:1242-1246.
184. Xu W.M., Gorman P., Sheer D., Bates G., Kishimoto J., Lizhi L., Emson P. Regional localization of the gene coding for human brain nitric oxide synthase (NOS1) to 12q24.2-24.31 by fluorescent in situ hybridization. Cytogenet. Cell Genet. 1993, 64:62-63.
185. Xu W.M., Charles I.G., Moncada S., Gorman P., Sheer D., Liu L.Z., Emson P. Mapping of the genes encoding human inducible and endothelial nitric oxide synthase (NOS2 and NOS3) to the pericentric region of chromosome 17 and to chromosome 7, respectively. Genomics 1994, 21:419-422.
186. Xu X., Star R., Tortorici G., Muallem S. Depletion of intracellular Ca2+ stores activates nitric oxide synthase to generate cGMP and regulate Ca2+ influx. J. Biol. Chem. 1994, 269:12645-12653.
187. Yoshizumi M., Perrella M.A., Burnett J.C., Lee M.E. Tumor necrosis factor downregulates an endothelial nitric oxide synthase messenger RNA by shortening its half-life. Circ. Res. 1993, 73:205-209.
188. Yui Y., Hattori R., Kosuga K., Eizawa H., Hiki K., Ohkawa S., Ohnishi K., Terao S., Kawai C. Calmodulin-independent nitric oxide synthase from rat polymorphonuclear neutrophils. J. Biol. Chem. 1991, 266:3369-3371.
189. Yui Y., Hattori R., Kosuga K., Eizawa H., Hiki K., Kawai C. Purification of nitric oxide synthase from rat macrophages. J. Biol. Chem. 1991, 266:12544-12547.
190. Zhang J., Snyder S.H. Nitric oxide in the nervous system. Annu. Rev. Pharmacol. Toxicol. 1995, 35:213-233.
191. Zhang M., Vogel H.J. Characterization of the calmodulin-binding domain of rat cerebellar nitric oxide synthase. J. Biol. Chem. 1994, 269:981-985.
192. Zhang M., Fabian H., Mantsch H.H., Vogel H.J. Isotope-edited Fourier transform infrared spectroscopy studies of calmodulin's interaction with its target peptides. Biochemistry 1994, 33:10883-10888.
193. Zhang M., Yuan T., Aramini J., Vogel H.J. Interaction of calmodulin with its binding domain of rat cerebellar nitric oxide synthase. J. Biol. Chem. 1995, 270:20907-29901.
194. Zhang R., Min W., Sessa W.C. Functional analysis of the human endothelial nitric oxide synthase promoter. Sp1 and GATA factors are necessary for basal transcription in endothelial cells. J. Biol. Chem. 1995, 270:15320-15326.
195. Zhang Z.G., Chopp M., Gautam S., Zaloga C., Zhang R.L., Schmidt H.H.H.W., Pollock J.S., Förstermann U. Upregulation of neuronal nitric oxide synthase and mRNA, and selective sparing of nitric oxide synthase-containing neurons after focal cerebral ischemia in rat. Brain Res. 1994, 654:85-95.
196. Zorumski C.F., Izumi Y. Nitric oxide and hippocampal synaptic plasticity. Biochem. Pharmacol. 1993, 46:777-785.