Role of neuronal and endothelial nitric oxide synthase in nitric oxide generation in the brain following cerebral ischemia

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1455, Issue 1, 1999, Pages 23-34

  Wei, Guo ^a   Dawson, Valina L ^b   Zweier, Jay L ^a  

^a Laboratory of Cellular and Molecular Biology   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cardiac arrest; Cerebral ischemia; Nitric oxide; Nitric oxide synthase; Transgenic mice

Indexed keywords

NITRIC OXIDE; NITRIC OXIDE SYNTHASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN ISCHEMIA; CONTROLLED STUDY; ELECTRON SPIN RESONANCE; ENZYME ACTIVITY; HEART ARREST; IN VITRO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; TRANSGENIC MOUSE; VASCULAR ENDOTHELIUM;

ANIMALS; BRAIN; BRAIN ISCHEMIA; ELECTRON SPIN RESONANCE SPECTROSCOPY; ENZYME INHIBITORS; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; NG-NITROARGININE METHYL ESTER; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE TYPE I; NITRIC OXIDE SYNTHASE TYPE II; NITRIC OXIDE SYNTHASE TYPE III; SPIN TRAPPING;

MUS MUSCULUS;

EID: 0032782417     PISSN: 09254439     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0925-4439(99)00051-4     Document Type: Article

References (56)

1. Radomsky M.W., Palmer R.M.J., Moncada S. An L-arginine/nitric oxide pathway present in human platelets regulates aggregation. Proc. Natl. Acad. Sci. USA. 87:1990;5193-5197.
2. 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. USA. 86:1989;5159-5162.
3. Bredt D.S., Snyder S.H. Isolation of nitric oxide synthase, a calmodulin-requiring enzyme. Proc. Natl. Acad. Sci. USA. 86:1989;9030-9033.
4. Pollock J.S., Forstermann 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. USA. 88:1991;10480-10484.
5. Gulyaeva N.V., Stepanichev M.Yu., Onufriev M.V., Lazareva N.A., Zarzhetsky Y.V., Gurvitch A.M., Volkov A.V. Cardiac arrest induces decrease of nitric oxide synthase activity and increase of free radical generation in rat brain regions. Neurosci. Lett. 220:1996;147-150.
6. Beasley T.C., Bari F., Thore C., Thrikawala N., Louis T., Busija D. Cerebral ischemia/reperfusion increases endothelial nitric oxide synthase levels by an indomethacin-sensitive mechanism. J. Cereb. Blood Flow Metab. 18:1998;88-96.
7. Malinski T., Bailey F., Zhang Z.G., Chopp M. Nitric oxide measured by a porphyrinic microsensor in rat brain after transient middle cerebral artery occlusion. J. Cereb. Blood Flow Metab. 13:1993;355-358.
8. Stao S., Tominaga T., Ohnishi T., Ohnishi S.T. EPR spin trapping study of nitric oxide formation during bilateral carotid occlusion in the rat. Biochim. Biophys. Acta. 1181:1993;195-197.
9. Tominaga T., Stao S., Ohnishi T., Ohnishi S.T. Electron paramagnetic resonance detection of nitric oxide produced during focal ischemia in the rat. J. Cereb. Blood Flow Metab. 14:1994;715-722.
10. Kubrina L.N., Caldwell W.S., Mordvintcev P.I., Malenkova I.V., Vanin A.F. EPR evidence for nitric oxide production from guanidino nitrogens of L-arginine in animal tissues in vivo. Biochim. Biophys. Acta. 1099:1992;233-237.
11. Voevodskaya N.V., Vanin A.F. Gamma-irradiation potentiates L-arginine-dependent nitric oxide formation in mice. Biochem. Biophys. Res. Commun. 86:1992;1423-1428.
12. Kuppusamy P., Ohnishi S.T., Numagami Y., Ohnishi T., Zweier J.L. Three-dimensional imaging of nitric oxide production in the rat brain subjected to ischemia-hypoxia. J. Cereb. Blood. Flow. Metab. 15:1995;899-903.
13. Dalkara T., Moskowitz M.A. The complex role of nitric oxide in the pathophysiology of focal cerebral ischemia. Brain Pathol. 4:1994;49-57.
14. Nowicki J.P., Duval D., Poignet H., Scatton D. Nitric oxide mediates neuronal death after focal cerebral ischemia in the mouse. Eur. J. Pharmacol. 204:1991;339-340.
15. Fukuyama N., Takizawa S., Ishida H., Hoshiai K., Shinohara Y., Nakazawa H. Peroxynitrite formation in focal cerebral ischemia-reperfusion in rats occurs predominantly in the peri-infarct region. J. Cereb. Blood Flow Metab. 18:1996;123-129.
16. Wizemann T.M., Gardner C.R., Quniones S., Durham S.K., Goller N.L., Ohnishi S.T., Laskin D.L. Production of nitric oxide and peroxynitrite in the lung following acute endotoxemia. J. Leukocyte Biol. 56:1994;759-768.
17. Laskin D.L., Rodriguez del Valfe M., Heck D.E., Hwang S., Ohnishi S.T., Goller N.L., Durham S.K., Laskin J.D. Hepatic nitric oxide production following acute endotoxemia in rats is mediated by increased inducible nitric oxide synthase gene expression. Hepatology. 22:1995;223-234.
18. Hooper D.C., Ohnishi S.T., Rhonda K., Numagami Y., Koprowski H. Local nitric oxide production in vial and autoimmune diseases of central nervous system. Proc. Natl. Acad. Sci. USA. 92:1995;5312-5316.
19. Obolenskaya M.Yu., Vanin A.F., Mordvintcev P.I., Mülsch A., Decker K. EPR evidence of nitric oxide production by the regenerating rat liver. Biochem. Biophys. Res. Commun. 202:1994;571-576.
20. Huang P.L., Huang Z.H., Mashimo H., Bloch K.D., Moskowitz M.A., Bevan J.A., Fishman M.C. Hypertension in mice lacking the gene for endothelial nitric oxide synthase. Nature. 377:1995;239-242.
21. Huang P.L., Dawson T.M., Bredt D.S., Snyder S.H., Fishman M.C. Targeted disruption of the neuronal nitric oxide synthase gene. Cell. 75:1993;1273-1286.
22. Huang Z.H., Huang P.L., Panahian N., Dalkara T., Fishman M.C., Moskowitz M.A. Effect of cerebral ischemia in mice deficient in neuronal nitric oxide synthase. Science. 265:1994;1883-1885.
23. Kida E., Pluta R., Lossinsky A.S., Golabek A.A., Choi-Miura N.-H., Wisniewski H.M., Mossakowski M.J. Complete cerebral ischemia with short-term survival in rat induced by cardiac arrest. II. Extracellular and intracellular accumulation of apolipoproteins E and J in the brain. Brain Res. 674:1995;341-346.
24. Fujii M., Hara H., Meng W., Vonsattel J.P., Huang Z.H., Moskowitz M.A. Strain-related differences in susceptibility to transient forebrain ischemia in SV-129 and C57 black/6 mice. Stroke. 28:1997;1805-1811.
25. Zweier J.L., Wang P., Kuppusamy P. Direct measurement of nitric oxide generation in the ischemic heart using electron paramagnetic resonance spectroscopy. J. Biol. Chem. 270:1995;304-307.
26. Giraldez R.R., Zweier J.L. An improved assay for measurement of nitric oxide synthase activity in biological tissues. Anal. Biochem. 261:1998;29-35.
27. Moncada S., Palmer R.M.J. Jr., Higgs E.A. Nitric oxide: physiology, pathology, and pharmacology. Pharm. Rev. 43:1991;109-142.
28. Furchgott R.F., V Zawadzki J. The obligatory role of endothelial cells on the relaxation of arterial muscle by acetylcholine. Nature. 288:1980;373-376.
29. Palmer R.M. Jr., Ferridge A.G., Moncada S. Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor. Nature. 327:1987;524-526.
30. Ignarro L.J., Byrns R.E., Buga G.M., Wood K.S. Endothelium-derived relaxing factor from pulmonary artery and vein possesses pharmacologic and chemical properties. Circ. Res. 61:1987;866-879.
31. Furchgott R.F., Vanhoutte P.M. Endothelium-derived relaxing and contracting factors. FASEB J. 3:1989;2007-2018.
32. Marletta M.A., Yoon P.S., Iyengar R., Leaf C.D., Wishnok J.S. Macrophage oxidation of L-arginine to nitrite and nitrate: nitric oxide is an intermediate. Biochemistry. 27:1988;8706-8711.
33. Bredt D.S., et al. Cloned and expressed nitric oxide synthase structurally resembles cytochrome P-450 reductase. Nature. 351:1991;714-718.
34. Bredt D.S., Synder S.H. Nitric oxide: a novel neuronal messenger. Neuron. 8:1992;3-11.
35. Moncada S., Palmer R.M.J., Higgs E.A. Biosynthesis of nitric oxide from L-arginine: a pathway for the regulation of cell function and communication. Biochem. Pharmacol. 38:1989;1709-1715.
36. Garthwaite J. Glutamate, nitric oxide and cell-cell signalling in the nervous system. Trends Neurosci. 14:1991;60-67.
37. Langrehr J.M., Hoffman R.A., Lancaster J.R. Jr., Simmons R.L. Nitric oxide, a new endogenous immunomodulator. Transplantation. 55:1993;1205-1212.
38. Beckman J.S., Beckman T.W., Chen J., Marshall P.A., Freeman B.A. Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and superoxide. Proc. Natl. Acad. Sci. USA. 87:1990;1620-1624.
39. Zweier J.L., Wang P., Samouilov A., Kuppusamy P. Enzyme independent formation of nitric oxide in biological tissues. Nat. Med. 1:1995;1796-1801.
40. Lancaster J.R. Jr., et al. Detection of nitric oxide by electron paramagnetic resonance spectroscopy during rejection of rat heart allograft. J. Biol. Chem. 267:1992;10994-10998.
41. Mikoyan V.D., Voevodskaya N.V., Kubrina L.N., Malenkova I.V., Vanin A.F. The influence of antioxidants and cycloheximide on the level of nitric oxide in the livers of mice in vivo. Biochim. Biophys. Acta. 1269:1995;19-24.
42. Kubrina L.N., Mikoyan V.D., Mordvintcev P.I., Vanin A.F. Iron potentiates bacterial lipoolysaccharide-induced nitric oxide formation in animal organs. Biochim. Biophys. Acta. 1176:(2):1993;40-44.
43. Mikoyan V.D., Kubrina L.N., Vanin A.F. Detection by electron spin resonance of nitric oxide formed from L-arginine in the mouse brain in vivo. Biophysics. 39:1995;953-957.
44. Kuppusamy P., Ohnishi S.T., Numagami Y., Ohnishi T., Zweier J.L. Imaging of nitric oxide generation in the rat brain. Res. Chem. Interm. 22:1996;605-613.
45. Iadecola C. Bright and dark sides of nitric oxide in ischemic brain injury. Trends Neurosci. 20:1997;132-139.
46. Nowicki J.P., Duval D., Poiwnet H., Scatton B. Nitric oxide mediates neuronal death after focal cerebral ischemia in the mouse. Eur. J. Pharmacol. 204:1991;339-340.
47. Zhang F., Iadecola C. Reduction of focal cerebral ischemic damage by delayed treatment with nitric oxide donors. J. Cereb. Blood Flow Metab. 14:1994;574-580.
48. Lipton S.A., Chol 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. 364:1993;626-628.
49. Choi D.W. Glutamate receptors and the induction of excitotoxic neuronal death. Prog. Brain Res. 100:1994;47-51.
50. 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.
51. Dawson V.L., Kizushhi V.M., L Huang P., Snyder S.H., Dawson T.M. Resistance to neurotoxicity in cortical cultures from neuronal nitric oxide synthase-dependent mice. J. Neurosci. 16:1996;2479-2487.
52. Huang Z.H., Huang P.L., Ma J.Y., Meng W., Ayata C., Fishman M.C., Moskowitz M.A. Enlarged infarcts in endothelial nitric oxide synthase knockout mice are attenuated by nitro-L-arginine. J. Cerebral. Blood Flow Metab. 16:1996;981-987.
53. 2+/Calmodulin-dependent and tetrahydrobiopterin regulatory process. J. Biol. Chem. 273:1998;25804-25808.
54. Xia Y., Roman L.J., Masters B.S.S., Zweier J.L. Inducible nitric-oxide synthase generates superoxide from the reductase domain. J. Biol. Chem. 273:1998;22635-22639.
55. Xia Y., Dawson V.L., Dawson T.M., Snyder S.H., Zweier J.L. Nitric oxide synthase generates superoxide and nitric oxide in arginine-depleted cells leading to peroxynitrite-mediated cellar injury. J. Biol. Chem. 93:1996;6770-6774.
56. Jaffrey S.R., Snyder S.H. Pin: an associated protein inhibitor of neuronal nitric oxide synthase. Science. 274:1996;774-777.