Abstract
1. Our method of real-time monitoring of dopamine release from rat striatal slices revealed that endothelin (ET)-3-induced dopamine release was inhibited by N G-methyl-L-arginine (L-NMMA; 1 mM), an inhibitor of nitric oxide (NO) synthase, while N G-methyl-D-arginine (D-NMMA; 1 mM), an inactive isomer of L-NMMA, had no effect.
2. The inhibition of L-NMMA (0.1 mM) became apparent when tissues were pretreated with tetrodotoxin (1 μM) for 30 min and subsequently exposed to ET-3 (4 μM).
3. L-NMMA (0.1 and 1 mM) dose dependently protected against ET-3-triggered hypoxic/hypoglycemic impairment of striatal responses to high K+.
4. Thus, NO may work as a promoter in mediation of the stimulatory and neurotoxic action of ET-3 on the striatal dopaminergic system, presumably by interacting with interneurons in the striatum.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
REFERENCES
Akaike, A., Tanimura, Y., Terada, K., and Nakata, N. (1994). Regulation by neuroprotective factors of NMDA receptor mediated nitric oxide synthesis in the brain and retina. Prog. Brain Res. 103:391–403.
Dawson, V. L., Dawson, T. M., London, E. D., Bredt, D. S., and Snyder, S. H. (1991). Nitric oxide mediates glutamate neurotoxicity in primary cortical cultures. Proc. Natl. Acad. Sci. USA 88:6368–6371.
Dawson, V. L., Dawson, T. M., Bartley, D. A., Uhl, G. R., and Snyder, S. H. (1993). Mechanisms of nitric oxide-mediated neurotoxicity in primary brain cultures. J. Neurosci. 13:2651–2661.
Garthwaite, J. (1991). Glutamate, nitric oxide and cell-cell signalling in the nervous system. Trends Neurosci. 14:60–67.
Garthwaite, J., Charles, S. L., and Ghess, W. R. (1988). Endothelium-derived relaxing factor release on activation of NMDA receptors suggests role as intercellular messenger in the brain. Nature 336:385–388.
Hanbauer, I., Wink, D., Osawa, Y., Edelman, G. M., and Gally, J. A. (1992). Role of nitric oxide in NMDA-evoked release of [3H]-dopamine from striatal slices. Neuroreport 3:409–412.
Hirata, Y., Emori, T., Eguchi, S., Kanno, K., Imai, T., Ohta, K., and Marumo, F. (1993). Endothelin receptor subtype B mediates synthesis of nitric oxide by cultured bovine endothelial cells. J. Clin. Invest. 91:1367–1373.
Inoue, A., Yanagisawa, M., Kimura, S., Kasuya, Y., Miyauchi, T., Goto, K., and Masaki, T. (1989). The human endothelian family: Three structurally and pharmacologically distinct isopeptides predicted by three separate genes. Proc. Natl. Acad. Sci. USA 86:2863–2867.
Izumi, Y., Clifford, D. B., and Zorumski, C. F. (1992). Inhibition of long-term potentiation by NMDA-mediated nitric oxice release. Science 257:1273–1276.
Kataoka, Y., Koizumi, S., Kumakura, K., Kurihara, M., Niwa, M., and Ueki, S. (1989). Endothelintriggered brain damage under hypoglycemia evidenced by real-time monitoring of dopamine release from rat striatal slices. Neurosci. Lett. 107:75–80.
Kataoka, Y., Koizumi, S., Niwa, M., Shibaguchi, H., Shigematsu, K., Kudo, Y., and Taniyama, K. (1994). Endothelin-3 stimulates inositol 1,4,5-trisphosphate production and Ca2+ influx to produce biphasic dopamine release from rat striatal slices. Cell. Mol. Neurobiol. 14:271–280.
Kataoka, Y., Koizumi, S., Kohzuma, M., Shibaguchi, H., Shigematsu, K., Niwa, M., and Taniyama, K. (1995). NMDA receptor involvement in endothelin neurotoxicity in rat striatal slices. Eur. J. Pharmacol. 273:285–289.
Kohzuma, M., Kataoka, Y., Koizumi, S., Shibaguchi, H., Nakashima, M. N., Yamashita, K., Niwa, M., and Taniyama, K. (1994). ETB receptor involvement in stimulatory and neurotoxic action of endothelin on dopamine neurones. Neuroreport 5:2653–2656.
Koizumi, S., Kataoka, Y., Niwa, M., and Kumakura, K. (1992). Endothelin-3 stimulates the release of catecholamine from cortical and striatal slices of the rat. Neurosci. Lett. 134:219–222.
Koizumi, S., Kataoka, Y., Niwa, M., Yamashita, K., Taniyama, K., and Kudo, Y. (1994a). Endothelin increased [Ca2+]i in cultured neurones and slices of rat hippocampus. Neuroreport 5:1077–1080.
Koizumi, S., Kataoka, Y., Niwa, M., Watanabe, S., and Taniyama, K. (1994b). Two distinct pathway are involved in the endothelin-3-evoked dopamine release from rat striatal slices. Eur. J. Pharmacol. 259:195–201.
Koizumi, S., Kataoka, Y., Inoue, K., Kohzuma, M., Niwa, M., and Taniyama, K. (1995). Contribution of L-type Ca2+ channels to long-term enhancement of high K+-evoked release of dopamine from rat striatal slices. Neurosci. Lett. 187:123–126.
Kumakura, K., Ohara, M., and Sato, G. P. (1986). Real-time monitoring of the secretory function of cultured adrenal chromaffin cells. J. Neurochem. 50:1765–1768.
Kuo, H., Grant, S., Muth, N., Hengemihle, J., and Ingram, D. K. (1994). The correlation between neuron counts and optical density of NADPH-diaphorase histochemistry in the rat stratum: A quantitative study. Brain Res. 660:57–65.
Lipton, S. A., Choi, Y. B., Pan, Z. H., Lei, S. Z., Chen, H. S., Sucher, N. J., Loscalzo, J., Singel, D. J., and Stamler, J. S. (1993). A redox-based mechanism for the neuroprotective and neurodestructive effects of nitric oxide and related nitroso-compounds. Nature 364:626–632.
Nakashima, N. M., Yamashita, K., Kataoka, Y., Yamashita, S. Y., and Niwa, M. (1995). Time course of nitric oxide synthase activity in neuronal, glial, endothelian cells of rat striatum following focal cerebral ischemia. Cell. Mol. Neurobiol. 15:341–349.
Sakurai, Y. Y. Kataoka, Y., Yamashita, K., Miyazaki, A., Ushio, M., Mine, K., Niwa, M., and Ueki, S. (1989). Conflict behavior and dynamics of monoamines of various brain nuclei in rats. Neuropharmacology 28:1067–1073.
Shibata, S., Yamamoto, Y., Tanaka, T., and Watanabe, S. (1995). N G-Nitro-L-arginine protects against hypoxia/hypoglycemia-induced decrease in CA1 presynaptic spikes in rat hippocampal slices. Eur. J. Pharmacol. 273:223–228.
Yamashita, K., Kataoka, Y., Niwa, M., Shigematsu, K., Himeno, A., Koizumi, S., and Taniyama, K. (1993). Increase production of endothelins in the hippocampus of stroke-prone spontaneously hypertensive rats following transient forebrain ischemia. Cell. Mol. Neurobiol. 13:15–23.
Yamashita, K., Niwa, M., Kataoka, Y., Shigematsu, K., Himeno, A., Tsutsumi, K., N-Nakashima, M., S-Yamashita, Y., Shibata, S., and Taniyama, K. (1994). Microglia with an endothelin ETB receptor aggregate in rat hippocampus CA1 subfields following transient forebrain ischemia. J. Neurochem. 63:1042–1051.
Yanagisawa, M., Kurihara, H., Kimura, S., Tomobe, Y., Kobayashi, M., Mitsui, Y., Yazaki, Y., Goto, K., and Masaki, T. (1988). A novel potent vasoconstrictor peptide produced by bascular endothelial cells. Nature 332:411–415.
Yoshizawa, T., Kimura, S., Kanazawa, I., Uchiyama, Y., Yanagisawa, M., and Masaki, T. (1989). Endothelian localizes in the dorsal horn and acts on the spinal neurones: possible involvement of dihydrophyridine-sensitive calcium channels and substance P release. Neurosci. Lett. 102:179–184.
Zhu, X. Z., and Luo, L. G. (1992). Effect of nitorprusside (nitric oxide) on endogenous dopamine release from rat striatal slices. J. Neurochem. 59:932–935.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Shibaguchi, H., Kataoka, Y., Koizumi, S. et al. Nitric Oxide Participates in the Stimulatory and Neurotoxic Action of Endothelin on Rat Striatal Dopaminergic Neurons. Cell Mol Neurobiol 17, 471–481 (1997). https://doi.org/10.1023/A:1026354720732
Issue Date:
DOI: https://doi.org/10.1023/A:1026354720732