Summary
1. Real-time monitoring of dopamine (DA) release from rat striatal slices demonstrated that endothelin (ET)-3 (0.1–10μM) produced a biphasic DA release consisting of transient and sustained components. When extracellular Ca2+ was removed, the sustained but not transient response remarkably decreased.
2. ET-3 (1–10μM) stimulated an increase in the intracellular Ca2+ concentration ([Ca2+]i), which also consisted of two components. The external Ca2+ depletion inhibited primarily the sustained component of the Ca2+ response to ET-3.
3. ET-3 increased inositol 1,4,5-trisphosphate (IP3) concentrations in striatal slices. This response peaked at 10 to 20 sec and returned to the basal level 2 min after stimulation, an event which was in good accord with a prompt and transient phase of both cytosolic Ca2+ activity and DA release evoked by ET-3.
4. Thus, ET-3 produces a transient and a sustained release of DA from striatal slices by stimulating intracellular Ca2+ mobilization via IP3 formation and extracellular Ca2+ influx, respectively.
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Arai, H., Hori, S., Aramori, I., Ohkubo, H., and Nakanishi, S. (1990). Cloning and expression of a cDNA encoding an endothelin receptor.Nature 348:730–732.
Chan, J., and Greenberg, D. A. (1991). Endothelin and calcium signaling in NG108-15 neuroblastoma × glioma cells.J. Pharmacol. Exp. Ther. 258:524–530.
Crawford, M. L. A., Hiley, C. R., and Young, J. M. (1990). Characteristics of endothelin-1 and endothelin-3 stimulation of phosphoinositide breakdown differ between regions of guinea pig and rat brain.Nauyn-Schmiedebergs Arch. Pharmacol. 341:268–271.
Fuxe, K., Änggárd, E., Lundgren, K., Cintra, A., Agnati, L. F., Galton, S. and Vane, J. (1988a). Localization of [125I] endothelin-1 and [125I]endothelin-3 binding sites in the rat brain.Acta Physiol. Scand. 137:563–564.
Fuxe, K., Cintra, A., Andbjer, B., Ánggärd, E., Goldstein, M., and Agnati, L. F. (1989b). Centrally administered endothelin-1 produces lesions in the brain of the male rat.Acta Phyiol. Scand. 137:155–156.
Fuxe, K., Tinner, B., Staines, W., Hemsén, A., Hersh, L., and Lundberg, J. M. (1991). Demonstration and nature of endothelin-3-like immunoreactivity in somatostatin and choline acetyltransferase-immunoreactive nerve cells of the neostriatum of the rat.Neurosci. Lett. 123:107–111.
Fuxe, K., Kurosawa, N., Cintra, A., Hallström, Á., Goiny, M., Rosen, L., Agnati, L. F., and Ungerstedt, U. (1992). Involvement of local ischemia in endothelin-1 induced lesions of the neostriatum of the anaesthetized rat.Exp. Brain Res. 88:131–139.
Giaid, A., Gibson, S. J., Herrero, M. T., Gentleman, S., Legon, S., Yanagisawa, M., Masaki, T., Ibrahim, N. B. N., Roberts, G. W., Rossi, M. L., and Polak, J. M. (1991). Topographical localisation of endothelin mRNA and peptide immunoreactivity in neurons of the human brain.Histochemistry 95:303–314.
Goldman, R. S., Finkbeiner, S. M., and Smith, S. J. (1991). Endothelin induces a sustained rise in intracellular calcium in hippocampal astrocytes.Neurosci. Lett. 123:4–8.
Goto, K., Kasuya, Y., Matsuki, N., Takuwa, Y., Kurihara, H., Ishikawa, T., Kimuar, S., Yanagisawa, M., and Masaki, T. (1989). Endothelin activates the dihydropyridine-sensitive voltage-dependent Ca+2 channel in vascular smooth muscle.Proc. Natl. Acad. Sci. USA 86:3915–3918.
Kataoka, Y., Koizumi, S., Kumarura, K., Kurihara, M., Niwa, M., and Ueki, S. (1989). Endothelin-triggered 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., and Niwa, M. (1991). Is an endothelin a neurotoxic factor?Neurochem. Int. 18:503–506.
Kohzuki, M., Chai, S. Y., Paxinos, G., Karavas, A., Casley, D. J., Johnson, C. I., and Mendelsohn, D. A. O. (1991). Localization and characterization of endothelin receptor binding sites in the rat brain visualized by in vitro autoradiography.Neuroscience 42:245–260.
Koizumi, S., Kataoka, Y., Shigematsu, K., Niwa, M., and Ueki, S. (1990). Evaluation of the neuroprotective action of WEB 1881 FU on hypoglycemia/hypoxia-induced neuronal damage using rat striatal slices.Jap. J. Pharmacol. 53:175–183.
Koizumi, S., Kataoka, Y., Niwa, M., and Kumakura, K. (192). Endothelin stimulates the release of catecholamine from cortical and striatal slices.Neurosci. Lett. 134:219–222.
Koizumi, S., Inoue, K., Kataoka, Y., Niwa, M. and Takanaka, A. (1994a). Endothelin-3 activates a voltage-gated Ca channel via a pertussis toxin sensitive mechanism leading to dopamine release from PC12 cells.Neurosci. Lett. 166:191–194.
Koizumi, S., Kataoka, Y., Niwa, M., Yamashita, K., Taniyama, K., and Kudo, Y. (1994b). Endothelin increased [Ca+2] in cultured neurons and slices of rat hippocampus.Neuro Report 5:1077–1080.
Koizumi, S., Kataoka, Y., Niwa M., Watanabe, S., and Taniyama, K. (1994c). Two distinct pathways are involved in the endothelin-3-evoked dopamine release from rat striatal slicesEur. J. Pharmacol. 259:195–201.
Kudo, Y., Nakamura, T. and Ito, E. (1991). A “macro” image analysis of fura-2 fluorescence to visualize the distribution of functional glutamate receptor subtypes in hippocampal slices.Neurosci. Res. 12:412–420.
Kudo, Y., Akita, K., Nakamura, T., Ogura, A., Makino, T., Tamagawa, A., Ozaki, K. and Miyakawa, A. (1992). A single optical fiber fluorometric device for measurement of intracellular Ca+2 concentration: Its application to hippocampal neurons in vitro and in vivo.Neuroscience 50:619–625.
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.
Lin, W. W., Lee, C. Y., and Chung, D. M. (1991). Endothelin-and Sarafotoxin- induced phosphoinositide hydrolysis in cultured cerebellar granule cells: Biochemical and pharmacological characterization.J. Pharmacol. Exp. Ther. 257:1053–1061.
MacCumber, M. W., Ross, C. A., and Snyder, S. H. (1990). Endothelin in the brain: Receptors, mitogenesis, and biosynthesis in glial cells.Proc. Natl. Acad. Sci. USA 87:2359–2363.
Marin, P., Dejumeaue, J. C., Durieu-Trautmann, O., Nguyen, D. L., Premont, J., Strosberg, A. D., and Couraud, P. O. (199). Are several G proteins involved in the different effects of endothelin-1 in mouse striatal astrocytes?J. Neurochem. 56:1270–1275.
Masaki, T. (1993). Endothelins: Homeostatic and compensatory actions in the circulatory and endocrine systems.Endocrine Rev. 14:256–268.
Niwa, M., Kawaguchi, T., Yamashita, K., Maeda, T., Kurihara, M., Katoaka, Y., and Ozaki, M. (1991). Specific 125I-endothelin-1 binding sites in the central nervous system.Clin. Exp. Hypertens. A13:799–806.
Niwa, M., Kawaguchi, T., Himeno, A., Fujimoto, M., Kurihara, M., Yamashita, K., Kataoka, Y., Shigematsu, and Taniyama, T. (1992). Specific binding sites for125I-endothelin-1 in the procine and human spinal cord.Eur. J. Pharmacol. Mol. Pharmacol. 225:281–289.
Ohara-Imaizumi, M., and Kumakura, K. (1991). Dynamics of the secretory response evoked by endothelin-1 in adreal chromaffin cells.J. Cardiovasc. Pharmacol. 17 (Suppl. 7):S156-S158.
Pulsinelli, W. A. (1985). Selective vulnerbility: Morphological and molecular characteristics. In K. Kogure, K.-A. Hossmann, B. K. Siesjö, and F. A. Welsh, (Eds.),Progress in Brain Research, Vol. 63, Elsevier, New York, pp. 29–37.
Reiser, G., and Donié, F. (1990). Endothelin induces a rise of inositol 1,4,5-triphosphate, inositol 1,3,4,5-tetrakisphophate levels and of cytosolic Ca+2 activity in neural cell lines.Eur. J. Neurosci. 2:769–775.
Sakurai, T., Yanagisawa, M., Takuwa, Y., Miyazaki, H., Kimura, S., Goto, K., and Masaki, T. (1990). Cloning of a cDNA encoding a non-isopeptide-selective subtype of the endothelin receptor.Nature 348:732–735.
Supattapone, S., Simpson, A. W. M., and Ashley, C. C. (1989). Free calcium rise and mitogenesis in glial cells caused by endothelin.Biochem. Biophys. Res. Commun. 165:1115–1122.
Tani, Y., Kataoka, Y., Sakurai, Y., Yamashita, K., Ushio, M., and Ueki, S. (1987). Changes of brain monomaine contents in three models of experimentally induced muricide in rats.Pharmacol. Biochem. Behav. 26:725–729.
Van Renterghem, C., Vigne, P., Barhain, J., Schmid-Alliana, A., Frelin, C., and Lazadunski, M. (1988). Molecular mechanism of action of the vasoconstrictor peptide endothelin.Biochem. Biphys. Res. Commun. 157:977–985.
Vigne, P., Breittmayer, J.-P. Marsault, R., and Frelin, C. (1990). Endothelin mobilizes Ca+2 from a caffeine- and ryanodine- insensitive intracellular pool in rat atrial cells.J. Biol. Chem. 265:6782–6787.
Yamashita, K., Kataoka, Y., Niwa, M., Shigematsu, K., Himeno, A., Koizumi, S., and Taniyama, K. (1993). Increased 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 vascular endothelial cells.Nature 322:411–415.
Yoshizawa, T., Kimura, S., Kanazawa, I., Uchiyama, Y., Yanagisawa, M., and Masaki, T. (1989). Endothelin localizes in the dorsal horn and acts on the spinal neurons: Possible involvement of dihydropyridine-sensitive calcium channels and substance P release.Neurosci. Lett. 102:179–184.
Yoshizawa, T., Shinmi, O., Giaid, A., Yanagisawa, M., Gibson, S., Kimura, S., Ushiyama, Y., Polak, J. M., Masaki, T., and Kanazawa, I. (1990). Endothelin: A novel peptide in the posterior pituitary system.Science 247:462–464.
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Kataoka, Y., Koizumi, S., Niwa, M. et al. 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 (1994). https://doi.org/10.1007/BF02088325
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DOI: https://doi.org/10.1007/BF02088325