Nitric oxide reduces Ca2+ and Zn2+ influx through voltage-gated Ca2+ channels and reduces Zn2+ neurotoxicity

Neuroscience

Volumn 100, Issue 3, 2000, Pages 651-661

  Snider, B J ^a   Choi, J ^a   Turetsky, D M ^a   Canzoniero, L M T ^a   Sensi, S L ^a   Sheline, C T ^a   Wang, X ^a   Yu, S P ^a   Choi, D W ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

cGMP; Iischemia; Neurotoxicity; Nitric oxide synthase; Redox modulation

Indexed keywords

2 AMINO 5 PHOSPHONOVALERIC ACID; 2,2' DITHIODIPYRIDINE; 4 (3 PHOSPHONOPROPYL) 2 PIPERAZINECARBOXYLIC ACID; 7 NITROINDAZOLE; CALCIUM; CYCLIC GMP; DIZOCILPINE; N ETHYLMALEIMIDE; N(G) NITROARGININE; NIMODIPINE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; THIOMERSAL; ZINC;

ANIMAL TISSUE; ARTICLE; BRAIN CELL; BRAIN ISCHEMIA; CALCIUM CHANNEL; CONTROLLED STUDY; DEPOLARIZATION; ENZYME ACTIVITY; FLUORESCENCE; MOUSE; NEOCORTEX; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL;

ANIMAL; CALCIUM; CALCIUM CHANNELS; ELECTROPHYSIOLOGY; ENZYME INHIBITORS; MICE; NEURONS; NEUROTOXINS; NITRIC OXIDE; NITRIC OXIDE DONORS; NITRIC-OXIDE SYNTHASE; OXIDATION-REDUCTION; SOLUTIONS; SUPPORT, U.S. GOV'T, P.H.S.; ZINC;

EID: 0034721574     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(00)00311-0     Document Type: Article

References (105)

1. Aizenman E., Brimecombe J.C., Potthoff W.K., Rosenberg P.A. Why is the role of nitric oxide in NMDA receptor function and dysfunction so controversial? Prog. Brain Res. 118:1998;53-71.
2. Aizenman E., Potthoff W.K. Lack of interaction between nitric oxide and the redox modulatory site of the NMDA receptor. Br. J. Pharmac. 126:1999;296-300.
3. 2+ from brain tissue during activity. Nature. 308:1984;734-736.
4. Atar D., Backx P.H., Appel M.M., Gao W.D., Marban E. Excitation-transcription coupling mediated by zinc influx through voltage-dependent calcium channels. J. biol. Chem. 270:1995;2473-2477.
5. Baudier J., Gerard D. Ions binding to S100 proteins: structural changes induced by calcium and zinc on S100a and S100b proteins. Biochemistry. 22:1983;3360-3369.
6. Baudier J., Haglid K., Haiech J., Gerard D. Zinc ion binding to human brain calcium binding proteins, calmodulin and S100b protein. Biochem. biophys. Res. Commun. 114:1983;1138-1146.
7. Biagi B.A., Enyeart J.J. Gadolinium blocks low- and high-threshold calcium currents in pituitary cells. Am. J. Physiol. 259:1990;C515-520.
8. Bredt D.S., Snyder S.H. Nitric oxide: a physiologic messenger molecule. A. Rev. Biochem. 63:1994;175-195.
9. Brimecombe J.C., Potthoff W.K., Aizenman E. A critical role of the N-methyl-D-aspartate (NMDA) receptor subunit (NR) 2A in the expression of redox sensitivity of NR1/NR2A recombinant NMDA receptors. J. Pharmac. exp. Ther. 291:1999;785-792.
10. 2+ homeostasis in hippocampal neurons. J. Neurochem. 68:1997;95-105.
11. i homeostasis contributes to the toxicity of nitric oxide in cultured hippocampal neurons. J. Neurochem. 69:1997;1882-1889.
12. Campbell D.L., Stamler J.S., Strauss H.C. Redox modulation of L-type calcium channels in ferret ventricular myocytes. Dual mechanism regulation by nitric oxide and S-nitrosothiols. J. gen. Physiol. 108:1996;277-293.
13. Canzoniero L.M.T., Turetsky D.M., Choi D.W. Measurement of intracellular free zinc concentrations accompanying zinc-induced neuronal death. J. Neurosci. 19:1999;RC31.
14. Chao S.-H., Suzuki Y., Zysk J.R., Cheung W.Y. Activation of calmodulin by various metal cations as a function of ionic radius. Molec. Pharmac. 26:1984;75-82.
15. 2+ in the hippocampal mossy fiber zone of the rat in situ. Expl Brain Res. 58:1985;202-205.
16. 2+ channel currents in rat sympathetic neurons. Eur. J. Pharmac. 243:1993;83-86.
17. 2+ current inhibition in rat sympathetic neurons. J. Physiol. (Lond.). 482:1995;521-531.
18. + channels. Circ. Res. 76:1995;325-334.
19. 2+ channel currents through protein phosphorylation in rat pinealocytes. J. Neurosci. 15:1995;3104-3109.
20. Choi D.W., Koh J.Y. Zinc and brain injury. A. Rev. Neurosci. 21:1998;347-375.
21. Choi D.W., Yokoyama M., Koh J.-Y. Zinc neurotoxicity in cortical cell culture. Neuroscience. 24:1988;67-79.
22. Choi Y.B., Tenneti L., Le D.A., Ortiz J., Bai G., Chen H.S.V., Lipton S.A. Molecular basis of NMDA receptor-coupled ion channel modulation by S-nitrosylation. Nat. Neurosci. 3:2000;15-21.
23. Christine C.W., Choi D.W. Effect of zinc on NMDA receptor-mediated channel currents in cortical neurons. J. Neurosci. 10:1990;108-116.
24. Cornell N.W., Crivaro K.E. Stability constant for the zinc-dithiothreitol complex. Analyt. Biochem. 47:1972;203-208.
25. Dawson V.L., Dawson T.M., Bartley D.A., Uhl G.R., Snyder S.H. Mechanisms of nitric oxide-mediated neurotoxicity in primary brain cultures. J. Neurosci. 13:1993;2651-2661.
26. 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. natn. Acad. Sci. USA. 88:1991;6368-6371.
27. Fagni L., Olivier M., Lafon-Cazal M., Bockaert J. Involvement of divalent ions in the nitric oxide-induced blockade of N-methyl-D-aspartate receptors in cerebellar granule cells. Molec. Pharmac. 47:1995;1239-1247.
28. 1C subunits by redox agents and hypoxia. J. Physiol. (Lond). 514:1999;629-637.
29. Fedele E., Jin Y., Varnier G., Raiteri M. In vivo microdialysis study of a specific inhibitor of soluble guanylyl cyclase on the glutamate receptor/nitric oxide/cyclic GMP pathway. Br. J. Pharmac. 119:1996;590-594.
30. Frederickson C.J. Neurobiology of zinc and zinc-containing neurons. Int. Rev. Neurobiol. 31:1989;145-238.
31. Frederickson C.J., Hernandez M.D., Goik S.A., Morton J.D., McGinty J.F. Loss of zinc staining from hippocampal mossy fibers during kainic acid induced seizures: a histofluorescence study. Brain Res. 446:1988;383-386.
32. Frederickson C.J., Hernandez M.D., McGinty J.F. Translocation of zinc may contribute to seizure-induced death of neurons. Brain Res. 480:1989;317-321.
33. 2+-induced neurotoxicity in rat primary cortical cultures:involvement of L-type calcium channels. Brain Res. 654:1994;257-264.
34. Garthwaite J., Southam E., Boulton C.L., Nielsen E.B., Schmidt K., Mayer B. Potent and selective inhibition of nitric oxide-sensitive guanylyl cyclase by 1H-[1,2,4]oxadiazolo[4,3-a]quinoxalin-1-one. Molec. Pharmac. 48:1995;184-188.
35. 2+ indicators with greatly improved fluorescence properties. J. biol. Chem. 260:1985;3440-3450.
36. Hara H., Huang P.L., Panahian N., Fishman M.C., Moskowitz M.A. Reduced brain edema and infarction volume in mice lacking the neuronal isoform of nitric oxide synthase after transient MCA occlusion. J. cereb. Blood Flow Metab. 16:1996;605-611.
37. Haug F.-M.S. Electron microscopical localization of the zinc in hippocampal mossy fibre synapses by a modified sulfide silver procedure. Histochemie. 8:1967;355-368.
38. Hewett S.J., Corbett J.A., McDaniel M.L., Choi D.W. Inhibition of nitric oxide formation does not protect murine cortical cell cultures from N-methyl-D-aspartate neurotoxicity. Brain Res. 625:1993;337-341.
39. Hewett S.J., Corbett J.A., McDaniel M.L., Choi D.W. Interferon-gamma and interleukin-1 beta induce nitric oxide formation from primary mouse astrocytes. Neurosci. Lett. 164:1993;229-232.
40. Hewett S.J., Csernansky C.A., Choi D.W. Selective potentiation of NMDA-induced neuronal injury following induction of astrocytic iNOS. Neuron. 13:1994;487-494.
41. Hewett S.J., Muir J.K., Lobner D., Symons A., Choi D.W. Potentiation of oxygen-glucose deprivation-induced neuronal death after induction of iNOS. Stroke. 27:1996;1586-1591.
42. Howell G.A., Welch M.G., Frederickson C.J. Stimulation-induced uptake and release of zinc in hippocampal slices. Nature. 308:1984;736-738.
43. 2+ channels by S-nitrosothiol nitric oxide donors. Circ. Res. 81:1997;742-752.
44. Huang Z., Huang P.L., Panahian N., Dalkara T., Fishman M.C., Moskowitz M.A. Effects of cerebral ischemia in mice deficient in neuronal nitric oxide synthase. Science. 265:1994;1883-1885.
45. Iadecola C., Zhang F., Casey R., Nagayama M., Ross M.E. Delayed reduction of ischemic brain injury and neurological deficits in mice lacking the inducible nitric oxide synthase gene. J. Neurosci. 17:1997;9157-9164.
46. Iadecola C., Zhang F., Xu X. Inhibition of inducible nitric oxide synthase ameliorates cerebral ischemic damage. Am. J. Physiol. 268:1995;R286-292.
47. 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 identical to those of nitric oxide radical. Circ. Res. 61:1987;866-879.
48. Izumi Y., Benz A.M., Clifford D.B., Zorumski C.F. Nitric oxide inhibitors attenuate N-methyl-D-aspartate excitotoxicity in rat hippocampal slices. Neurosci. Lett. 135:1992;227-230.
49. 45Ca uptake in the smooth muscle of rabbit aorta, rat aorta and guinea-pig taenia coli. Br. J. Pharmac. 81:1984;393-400.
50. 2+ entry produces oxidative neuronal necrosis in cortical cell cultures. Eur. J. Neurosci. 11:1999;327-334.
51. Koh J.-Y., Choi D.W. Quantitative determination of glutamate mediated cortical neuronal injury in cell culture by lactate dehydrogenase efflux assay. J. Neurosci. Meth. 20:1987;83-90.
52. Koh J.-Y., Choi D.W. Zinc toxicity on cultured cortical neurons: involvement of N-methyl-D-aspartate receptors. Neuroscience. 60:1994;1049-1057.
53. Koh J.-Y., Suh S.W., Gwag B.J., He Y.Y., Hsu C.Y., Choi D.W. The role of zinc in selective neuronal death after transient global cerebral ischemia. Science. 2 72:1996;1013-1016.
54. Kreye V.A., Baron G.D., Luth J.B., Schmidt-Gayk H. Mode of action of sodium nitroprusside on vascular smooth muscle. Naunyn Schmiedebergs Arch. Pharmac. 288:1975;381-402.
55. Kurenny D.E., Moroz L.L., Turner R.W., Sharkey K.A., Barnes S. Modulation of ion channels in rod photoreceptors by nitric oxide. Neuron. 13:1994;315-324.
56. Lacampagne A., Duittoz A., Bolaños P., Peineau N., Argibay J.A. Effect of sulfhydryl oxidation on ionic and gating currents associated with L-type calcium channels in isolated guinea-pig ventricular myocytes. Cardiovasc. Res. 30:1995;799-806.
57. Lei S.Z., Pan Z.-H., Aggarwal S.K., Chen H.-S.V., Hartman J., Sucher N.J., Lipton S.A. Effect of nitric oxide production on the redox modulatory site of the NMDA receptor-channel complex. Neuron. 8:1992;1087-1099.
58. Lipton S.A., Choi Y.-B., Pan Z.-H., Lei S.Z., Chen H.-S.V., Sucher N., 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;626-632.
59. Lipton S.A., Choi Y.B., Sucher N.J., Chen H.S. Neuroprotective versus neurodestructive effects of NO-related species. Biofactors. 8:1998;33-40.
60. Lipton S.A., Rayudu P.V., Choi Y.B., Sucher N.J., Chen H.S. Redox modulation of the NMDA receptor by NO-related species. Prog. Brain Res. 118:1998;73-82.
61. 2+ influx underlies potent induction of injury. J. Neurosci. 16:1996;5457-5465.
62. Manev H., Kharlamov E., Uz T., Mason R.P., Cagnoli C.M. Characterization of zinc-induced neuronal death in primary cultures of rat cerebellar granule cells. Expl Neurol. 146:1997;171-178.
63. Manzoni O., Bockaert J. Nitric oxide synthase activity endogenously modulates NMDA receptors. J. Neurochem. 61:1993;368-370.
64. Maragos C.M., Morley D., Wink D.A., Dunams T.M., Saavedra J.E., Hoffman A., Bove A.A., Isaac L., Hrabie J.A., Keefer L.K. Complexes of.NO with nucleophiles as agents for the controlled biological release of nitric oxide. Vasorelaxant effects. J. med. Chem. 34:1991;3242-3247.
65. Maragos C.M., Wang J.M., Hrabie J.A., Oppenheim J.J., Keefer L.K. Nitric oxide/nucleophile complexes inhibit the in vitro proliferation of A375 melanoma cells via nitric oxide release. Cancer Res. 53:1993;564-568.
66. McCarthy K., deVellis J. Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue. J. Cell Biol. 85:1980;890-902.
67. Mittal C.K., Harrell W.B., Mehta C.S. Interaction of heavy metal toxicants with brain constitutive nitric oxide synthase. Molec. Cell Biochem. 149/150:1995;263-265.
68. Moncada C., Lekieffre D., Arvin B., Meldrum B. Effect of NO synthase inhibition on NMDA-and ischaemia-induced hippocampal lesions. NeuroReport. 3:1992;530-532.
69. Moncada S., Palmer R.M.J., Higgs E.A. Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmac. Rev. 43:1991;109-142.
70. Moore P.K., Bland-Ward P.A. 7-Nitroindazole: an inhibitor of nitric oxide synthase. Meth. Enzym. 268:1996;393-398.
71. Moore P.K., Wallace P., Gaffen Z., Hart S.L., Babbedge R.C. Characterization of the novel nitric oxide synthase inhibitor 7-nitro indazole and related indazoles: antinociceptive and cardiovascular effects. Br. J. Pharmac. 110:1993;219-224.
72. Nathan C., Xie Q.-w. Nitric oxide synthases: roles, tolls, and controls. Cell. 78:1994;915-918.
73. Panahian N., Yoshida T., Huang P.L., Hedley-Whyte E.T., Dalkara T., Fishman M.C., Moskowitz M.A. Attenuated hippocampal damage after global cerebral ischemia in mice mutant in neuronal nitric oxide synthase. Neuroscience. 72:1996;343-354.
74. Paoletti P., Ascher P., Neyton J. High-affinity zinc inhibition of NMDA NR1-NR2A receptors. J. Neurosci. 17:1997;5711-5725.
75. Perez-Clausell J., Danscher G. Intravesicular localization of zinc in rat telencephalic boutons. A histochemical study. Brain Res. 337:1985;91-98.
76. Perez-Clausell J., Danscher G. Release of zinc sulphide accumulations into synaptic clefts after in vivo injection of sodium sulphide. Brain Res. 362:1986;358-361.
77. 2+ ion. Biochemistry. 34:1995;15,091-15,095.
78. Quignard J.-F., Frapier J.M., Harricane M.-C., Albat B., Nargeot J., Richard S. Voltage-gated calcium channel currents in human coronary myocytes. Regulation by cyclic GMP and nitric oxide. J. clin. Invest. 99:1997;185-193.
79. Regan R.F., Renn K.E., Panter S.S. NMDA neurotoxicity in murine cortical cell cultures is not attenuated by hemoglobin or inhibition of nitric oxide synthesis. Neurosci. Lett. 153:1993;53-56.
80. Reynolds I.J., Miller R.J. Multiple sites for the regulation of the N-methyl-D-aspartate receptor. Molec. Pharmac. 33:1988;581-584.
81. Rose K., Choi D. W. and Goldberg M. P. (1993) Cytotoxicity in murine neocortical cell culture. In In Vitro Biological Methods (eds Tyson C. and Frazier J.). Academic, San Diego, CA.
82. Sensi S.L., Canzoniero L.M.T., Yu S.P., Ying H.S., Koh J.-Y., Kerchner G.A., Choi D.W. Measurement of intracellular free zinc in living cortical neurons: routes of entry. J. Neurosci. 17:1997;9554-9564.
83. 2+-permeable AMPA/kainate channels triggers prolonged mitochondrial superoxide production. Proc. natn. Acad. Sci. USA. 96:1999;2414-2419.
84. Smart T.G., Xie X., Krishek B.J. Modulation of inhibitory and excitatory amino acid receptor ion channels by zinc. Prog. Neurobiol. 42:1994;393-441.
85. Snider B. J., Choi J., Turetsky D. M., Canzoniero L. M. T., Sensi S. L., Sheline C. T. and Choi D. W. (1999) Another facet of nitric oxide: reduction of toxic zinc influx through voltage-gated channels. In Maturation Phenomenon in Cerebral Ischemia III (eds Ito U., Fieschi C., Orzi F., Kuroiwa T. and Klatzo I.). Springer, New York.
86. Snider B.J., Choi J.Y., Turetsky D.M., Choi D.W. Nitric oxide (NO) donors or cGMP reduce zinc neurotoxicity by blocking voltage sensitive calcium channels. Soc. Neurosci. Abstr. 23:1997;2255.
87. Snider B.J., Turetsky D.M., Choi D.W. Nitric oxide donors or cGMP reduce neuronal injury caused by exposure to zinc. Neurology. 48:1997;A76-77.
88. Stamler J.S. Redox signaling: nitrosylation and related target interactions of nitric oxide. Cell. 78:1994;931-936.
89. Stamler J.S., Toone E.J., Lipton S.A., Sucher N.J. (S)NO signals: translocation, regulation, and a consensus motif. Neuron. 18:1997;691-696.
90. Strange K., Emma F., Jackson P.S. Cellular and molecular physiology of volume-sensitive anion channels. Am. J. Physiol. 270:1996;C711-730.
91. Suh S.W., Chen J.W., Motamedi M., Bell B., Listiak K., Pons N.F., Danscher G., Frederickson C.J. Evidence that synaptically-released zinc contributes to neuronal injury after traumatic brain injury. Brain Res. 852:2000;268-273.
92. Tang L.H., Aizenman E. Long-lasting modification of the N-methyl-D-aspartate receptor channel by a voltage-dependent sulfhydryl redox process. Molec. Pharmac. 44:1993;473-478.
93. Tatsumi T., Fliss H. Hypochlorous acid mobilizes intracellular zinc in isolated rat heart myocytes. J. molec. Cell Cardiol. 26:1994;471-479.
94. Tonder N., Johansen F.F., Frederickson C.J., Zimmer J., Diemer N.H. Possible role of zinc in the selective degeneration of dentate hilar neurons after cerebral ischemia in the adult rat. Neurosci. Lett. 109:1990;247-252.
95. Tsuji Y., Unno N., Menconi M.J., Smith M., Fink M.P. Nitric oxide donors increase cytosolic ionized calcium in cultured human intestinal epithelial cells. Shock. 6:1996;19-24.
96. Vega M.T., Villalobos C., Garrido B., Gandia L., Bulbena O., Garcia-Sancho J., Garcia A.G., Artalejo A.R. Permeation by zinc of bovine chromaffin cell calcium channels: relevance to secretion. Pflugers Arch. 429:1994;231-239.
97. Vogt K., Mellor J., Tong G., Nicoll R. The actions of synaptically released zinc at hippocampal mossy fiber synapses. Neuron. 26:2000;187-196.
98. Wallis R.A., Panizzon K., Wasterlain C.G. Inhibition of nitric oxide synthase protects against hypoxic neuronal injury. NeuroReport. 3:1992;645-648.
99. Weiss J.H., Hartley D.M., Koh J.-Y., Choi D.W. AMPA receptor activation potentiates zinc neurotoxicity. Neuron. 10:1993;43-49.
100. Winegar B.D., Lansman J.B. Voltage-dependent block by zinc of single calcium channels in mouse myotubes. J. Physiol. (Lond.). 425:1990;563-578.
101. Yang X.C., Sachs F. Block of stretch-activated ion channels in Xenopus oocytes by gadolinium and calcium ions. Science. 243:1989;1068-1071.
102. (2+) permeable AMPA/kainate channels and triggers selective neural injury. NeuroReport. 6:1995;2553-2556.
103. Yoshida T., Limmroth V., Irikura K., Moskowitz M.A. The NOS inhibitor, 7-nitroindazole, decreases focal infarct volume but not the response to topical acetylcholine in pial vessels. J. cereb. Blood Flow Metab. 14:1994;924-929.
104. Zhang F., Casey R.M., Ross M.E., Iadecola C. Aminoguanidine ameliorates and L-arginine worsens brain damage from intraluminal middle cerebral artery occlusion. Stroke. 27:1996;317-323.
105. Zhang Z.G., Reif D., Macdonald J., Tang W.X., Kamp D.K., Gentile R.J., Shakespeare W.C., Murray R.J., Chopp M. ARL 17477, a potent and selective neuronal NOS inhibitor decreases infarct volume after transient middle cerebral artery occlusion in rats. J. cereb. Blood Flow Metab. 16:1996;599-604.