Abstract
Metabotropic glutamate receptors have recently been envisaged as involved in both potentiation and prevention of ischemic and excitotoxic neuronal damage. The release of the inhibitory amino acid taurine is markedly enhanced in ischemia in both the immature and mature mouse hippocampus. The modulation of [3H]taurine release by metabotropic receptor agonists and antagonists was studied in hippocampal slices from developing (7-day-old) and adult (3-month-old) mice using a superfusion system. Agonists of group I, II and III metabotropic glutamate receptors generally reduced the ischemia-induced release in adult animals. In the immature hippocampus the group I agonists (S)-3,5-dihydroxyphenylglycine and (1±)-1-aminocyclopentane-trans-1,3-dicarboxylate, which mainly enhance neuronal excitation, potentiated initial taurine release in ischemia. Ionotropic glutamate receptor agonists also enhance the ischemia-induced taurine release in developing mice. This glutamate-activated taurine release may thus constitute an important protective mechanism against excitotoxicity in the immature hippocampus.
Similar content being viewed by others
REFERENCES
Rothman, S. M. and Olney, J. W. 1988. Glutamate and pathology of hypoxic/ischemic brain damage. Ann. Neurol. 19:105-111.
Szatkowski, M. and Attwell, D. 1994. Triggering and execution of neuronal death in brain ischemia: two phases of glutamate release by different mechanisms. Trends Neurosci. 17:359-365.
Ozawa, S., Kamiya, H., and Tsuzuki, K. 1998. Glutamate receptors in the mammalian central nervous system. Prog. Neurobiol. 54:581-618.
Pellegrini-Giampietro, D. E., Cherici, G., Alesiani, M., Carlá, V., and Moroni, F. 1990. Excitatory amino acid release and free radical formation may cooperate in the genesis of ischemiainduced neuronal damage. J. Neurosci. 10:1035-1041.
Collard, K. J. and Menon-Johansson, A. S. 1993. Effects of short-term hypoxia on [3H]glutamate release from preloaded hippocampal and cortical synaptosomes. Neurochem. Res. 8:165-170.
Hagberg, H., Lehmann, A., Sandberg, M., Nyström, B., Jacobson, I., and Hamberger, A. 1985. Ischemia-induced shifts on inhibitory and excitatory amino acids in area CA1 of the rat hippocampus. Dev. Brain Res. 38:286-290.
Globus, M. Y.-T., Busto, R., Dietrich, W. D., Martinez, E., Valdes, I., and Ginsberg, M. 1988. Effect of ischemia on the in vivo release of striatal dopamine, glutamate and γ-aminobutyric acid studied by intracerebral microdialysis. J. Neurochem. 51: 1455-1464.
Conn, P. J. and Pin, J.-P. 1997. Pharmacology and functions of metabotropic glutamate receptors. Annu. Rev. Pharmacol. Toxicol. 37:205-237.
Pin, J.-P. and Duvoisin, R. 1995. The metabotropic glutamate receptors: structure and functions. Neuropharmacology 34:1-26.
Pellegrini-Giampietro, D. E., Torregrossa, S. A., and Moroni, F. 1996. Pharmacological characterization of metabotropic glutamate receptors coupled to phospholipase D in the rat hippocampus. Br. J. Pharmacol. 118:1035-1043.
Kontro, P. and Oja, S. S. 1987. Taurine and GABA release from mouse cerebral cortex slices: potassium stimulation releases more taurine than GABA from developing brain. Dev. Brain Res. 37:277-291.
Sturman, J. A. 1993. Taurine in development. Physiol. Rev. 73:119-147.
Solis, J. M., Herranz, A. S., Herreras, O., Lerma, J., and Martin del Rio, R. 1988. Low chloride-dependent release of taurine by a furosemide-sensitive process in the in vivo rat hippocampus. Neuroscience 24:885-891.
Oja, S. S. and Saransaari, P. 1996. Taurine as osmoregulator and neuromodulator in the brain. Metab. Brain Dis. 11:153-164.
French, E. D., Vezzani, A., Whetsell, W. O., Jr, and Schwarcz, R. 1986. Antiexcitotoxic actions of taurine in the rat hippocampus studied in vivo and in vitro. Adv. Exp. Med. Biol. 203:349-362.
Trenkner, E. 1990. The role of taurine and glutamate during early postnatal cerebellar development of normal and weaver mutant mice. Adv. Exp. Med. Biol. 268:239-244.
Tang, X. W., Deupree, D. L., Sun, Y., and Wu, J.-Y. 1996. Biphasic effect of taurine on excitatory amino acid-induced neurotoxicity. Adv. Exp. Med. Biol. 403:499-505.
Schurr, A., Tseng, M. T., West, C. A., and Rigor, B. M. 1987. Taurine improves the recovery of neuronal function following cerebral hypoxia: an in vitro study. Life Sci. 40:2059-2066.
Oja, S. S. and Kontro, P. 1983. Free amino acids in epilepsy: possible role of taurine. Acta Neurol. Scand. 67, Suppl 95:5-20.
Boldyrev, A. A., Johnson, P., Wei, Y., Tan, Y., and Carpenter, D. O. 1999. Carnosine and taurine protect rat cerebellar granular cells from free radical damage. Neurosci. Lett. 263:169-172.
Magnusson, K. R., Koerner, J. F., Larson, A. A., Smullin, D. H., Skilling, S. R., and Beitz, A. J. 1991. NMDA-, kainate-and quisqualate-stimulated release of taurine from electrophysiologically monitored rat hippocampal slices. Brain Res. 549:1-8.
Saransaari, P. and Oja, S. S. 1997. Taurine release from the developing and ageing hippocampus: stimulation by agonists of ionotropic glutamate receptors. Mech. Ageing Dev. 99:219-232.
Saransaari, P. and Oja, S. S. 1999. Involvement of metabotropic glutamate receptors in taurine release in the adult and developing mouse hippocampus. Amino Acids 16:165-179.
Lekieffre, D., Callebert, J., Plotkine, M., and Boulu, R. G. 1992. Concomitant increases in the extracellular concentrations of excitatory and inhibitory amino acids in the rat hippocampus during forebrain ischemia. Neurosci. Lett. 137:78-82.
Ooboshi, H., Sadoshima, S., Yao, H., Ibayashi, S., Matsumoto, T., Uchimura, H., and Fujishima, M. 1995. Ischemia-induced release of amino acids in the hippocampus of aged hypertensive rats. J. Cereb. Blood Flow Metab. 15:227-234.
Saransaari, P. and Oja, S. S. 1997. Enhanced taurine release in cell-damaging conditions in the developing and ageing mouse hippocampus. Neuroscience 79:847-854.
Saransaari, P. and Oja, S. S. 1998. Release of endogenous glutamate, aspartate, GABA and taurine from hippocampal slices from adult and developing mice in cell-damaging conditions. Neurochem. Res. 23:567-574.
Saransaari, P. and Oja, S. S. 1998. Mechanisms of ischemiainduced taurine release in mouse hippocampal slices. Brain Res. 807:118-124.
Saransaari, P. and Oja, S. S. 1999. Characteristics of ischemiainduced taurine release in the developing mouse hippocampus. Neuroscience 94:949-954.
Saransaari, P. and Oja, S. S. 1997. Glutamate-agonist-evoked taurine release from the adult and developing mouse hippocampus in cell-damaging conditions. Amino Acids 13:323-335.
Owen, D. B. 1962. Handbook of Statistical Tables, pp. 384-387. Addison-Wesley, Reading, MA.
Fotuhi, M., Standaert, D. G., Testa, C. M., Penney, J. J., and Young, A. B. 1994. Differential expression of metabotropic glutamate receptors in the hippocampus and entorhinal cortex of the rat. Mol. Brain Res. 21:283-292.
Shigemoto, R., Kinoshita, A., Wada, E., Nomura, S., Ohishi, H., Takada, M., Flor, P. J., Neki, A., Nakanishi, S., and Mizuno, N. 1997. Differential presynaptic localization of metabotropic glutamate receptor subtypes in the rat hippocampus. J. Neurosci. 17:7503-7522.
Lombardi, G., Leonardi, P., and Moroni, F. 1996. Metabotropic glutamate receptors, transmitter output and fatty acids: studies in rat brain slices. Br. J. Pharmacol. 117:189-195.
East, S. J., Hill, M. P., and Brotchie, J. M. 1995. Metabotropic glutamate receptor agonists inhibit endogenous glutamate release from rat striatal synaptosomes. Eur. J. Pharmacol. 277: 117-121.
Schoepp, D. and Conn, P. J. 1993. Metabotropic glutamate receptors in brain function and pathology. Trends Pharmacol. Sci. 14:13-20.
Schaffhauser, H., de Barry, J., Muller, H., Heitz, M.-P., Gombos, G., and Mutel, V. 1997. Involvement of cyclic-AMP pathway in group I metabotropic glutamate receptor responses in neonatal rat cortex. Eur. J. Pharmacol. 344:289-297.
Herrero, I., Miras-Portugal, M. T., and Sánchez-Prieto, J. 1998. Functional switch from facilitation to inhibition in the control of glutamate release by metabotropic glutamate receptors. J. Biol. Chem. 273:1951-1958.
Thomsen, C., Boel, E., and Suzdak, P. D. 1994. Actions of phenylglycine analogs at subtypes of the metabotropic glutamate receptor family. Eur. J. Pharmacol. 267:77-84.
Sacaan, A. I., Santori, E. M., and Rao, T. S. 1998 (S)-4-Carboxy-3-hydroxyphenylglycine activates phosphatidyl inositol linked metabotropic glutamate receptors in different brain regions of the neonatal rat. Neurochem. Int. 32:77-85.
Shigemoto, R., Nakanishi, S., and Mizuno, N. 1992. Distribution of the mRNA for a metabotropic glutamate receptor (mGluR1) in the central nervous system: an in situ hybridization study in adult and developing rat. J. Comp. Neurol. 322:121-135.
Minakami, R., Iida, K., Hirakawa, N., and Sugiyama, H. 1995. The expression of two splice variants of metabotropic glutamate receptor subtype 5 in the rat brain and neuronal cells during development. J. Neurochem. 65:1536-1542.
Nicoletti, F., Bruno, V., Copani, A., Casabona, G., and Knöpfel, T. 1996. Metabotropic glutamate receptors: a new target for the therapy of neurodegenerative disorders? Trends Neurosci. 19:267-271.
McDonald, J. W. and Schoepp, D. D. 1992. The metabotropic excitatory amino acid receptor agonist 1S,3R-ACPD selectively potentiates N-methyl-D-aspartate-induced brain injury. Eur. J. Pharmacol. 215:353-354.
Strasser, U., Lobner, D., Behrens, M. M., Canzoniero, L. M. T., and Choi, D. W. 1998. Antagonists for group I mGluRs attenuate excitotoxic neuronal death in cortical cultures. Eur. J. Neurosci. 10:2848-2855.
Buisson, A. and Choi, D. W. 1995. The inhibitory mGluR agonist, S-4-carboxy-3-hydroxyphenylglycine selectively attenuates NMDA neurotoxicity and oxygen-glucose deprivationinduced neuronal death. Neuropharmacology 34:1081-1087.
Montoliu, C., Llansola, M., Cucarella, C., Grilolía, S., and Felipo, V. 1997. Activation of the metabotropic glutamate receptor mGluR5 prevents glutamate toxicity in primary cultures of cerebellar neurons. J. Pharmacol. Exp. Ther. 281:643-647.
Koh, J. Y., Palmer, E., and Cotman, C. W. 1991. Activation of the metabotropic glutamate receptor attenuates N-methyl-Daspartate neurotoxicity in cortical cultures. Proc. Natn. Acad. Sci. USA 88:9431-9435.
Pizzi, M., Consolandi, O., Memo, M., and Spano, P. E. 1996. Activation of multiple metabotropic glutamate receptor subtypes prevents NMDA-induced excitotoxicity in rat hippocampal slices. Eur. J. Neurosci. 8:1516-1521.
Small, D. L., Monette, R., Chakravarthy, B., Durkin, J., Barbe, G., Mealing, G., Morley, P., and Buchan, A. M. 1996. Mechanisms of 1S,3R-ACPD-induced neuroprotection in rat hippocampal slices subjected to oxygen and glucose deprivation. Neuropharmacology 35:1037-1048.
Gereau R. W., IV and Conn, P. J. 1995. Multiple presynaptic metabotropic glutamate receptors modulate excitatory and inhibitory synaptic transmission in hippocampal area CA1. J. Neurosci. 15:6879-6889.
Manzoni, O. and Bockaert, J. 1995. Metabotropic glutamate receptors inhibiting excitatory synapses in the CA1 area of rat hippocampus. Eur. J. Neurosci. 7:2518-2523.
Sánchez-Prieto, J., Budd, D. C., Herrero, I., Vázquez, E., and Nicholls. D. G. 1996. Presynaptic receptors and the control of glutamate exocytosis. Trends Neurosci. 19:235-239.
Cozzi, A., Attucci, S., Peruginelli, F., Marinozzi, M., Luneia, R., Pellicciari, R., and Moroni, F. 1997. Type 2 metabotropic glutamate (mGlu) receptors tonically inhibit transmitter release in rat caudate nucleus: in vivo studies with (2S,1'S,2'S,3'R)-2-(2'-carboxy-3'-phenylcyclopropyl)glycine, a new potent and selective antagonist. Eur. J. Neurosci. 9:1350-1355.
Bruno, V., Battaglia, G., Copani, A., Giffard, R. G., Raciti, G., Shinozaki, H., and Nicoletti, F. 1995. Activation of class II or III metabotropic glutamate receptors protects cultured cortical neurons against excitotoxic degeneration. Eur. J. Neurosci. 7:1906-1913.
Uyama, Y., Ishida, M., and Shinozaki, H. 1997. DCG-IV, a potent metabotropic glutamate receptor agonist, as an NMDA receptor agonist in the rat cortical slice. Brain Res. 752:327-330.
Lafon-Cazal, M., Fagni, L., Guiraud, M.-J., Mary, S., Lerner-Natoli, M., Pin, J.-P., Shigemoto, R., and Bockaert, J. 1999. mGluR7-like metabotropic glutamate receptors inhibit NMDA-mediated excitotoxicity in cultured mouse cerebellar granule neurons. Eur. J. Neurosci. 11:663-672.
Jones, P. G. and Roberts, P. J. 1990. Ibotenate stimulates glutamate release from guinea pig cerebrocortical synaptosomes: inhibition by L-2-amino-4-phosphonobutyrate (L-AP4). Neurosci. Lett. 111:228-232.
Vázquez, E., Herrero, I., Miras-Portugal, M. T., and Sánchez-Prieto, J. 1995. Developmental change from inhibition to facilitation in the presynaptic control of glutamate exocytosis by metabotropic glutamate receptors. Neuroscience 68:117-124.
Baskys, A. and Malenka, R. C. 1991. Agonists at metabotropic glutamate receptors presynaptically inhibit EPSCs in neonatal rat hippocampus. J. Physiol. (Lond) 444:687-701.
Herrero, I., Vázquez, E., Miras-Portugal, M. T., and Sánchez-Prieto, J. 1996. A decrease in [Ca2+]c but not in cAMP mediates L-AP4 inhibition of glutamate release: PKC-mediated suppression of this inhibitory pathway. Eur. J. Neurosci. 8:700-709.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Saransaari, P., Oja, S.S. Involvement of Metabotropic Glutamate Receptors in Ischemia-Induced Taurine Release in the Developing and Adult Hippocampus. Neurochem Res 25, 1067–1072 (2000). https://doi.org/10.1023/A:1007677610714
Issue Date:
DOI: https://doi.org/10.1023/A:1007677610714