Skip to main content
SpringerLink
Log in

Glutamate-agonist-evoked taurine release from the adult and developing mouse hippocampus in cell-damaging conditions

  • Review Article
  • Published:
Amino Acids Aims and scope Submit manuscript

Summary

Taurine is a neuromodulator and osmoregulator in the central nervous system, also protecting neural cells against excitotoxicity. The effects of the ionotropic glutamate receptor agonists N-methyl-D-aspartate (NMDA), kainate and 2-amino-3-hydroxy-5-methyl-4-imidazolepropionate (AMPA) on [3H]taurine release from hippocampal slices from 3-month-old and 7-day-old mice were studied in cell-damaging conditions. Neural cell injury was induced by superfusing the slices in hypoxic, hypoglycemic and ischemic conditions and by exposing them to metabolic poisons, free radicals and oxidative stress. The release of taurine was greatly enhanced in these conditions at both ages, except in oxidative stress. In normal conditions the three glutamate agonists potentiated taurine release in the immature hippocampus in a receptor-mediated manner, but kainate receptors did not participate in the regulation in the adults. The ability of the agonists to evoke taurine release varied in the cell-damaging conditions, but the glutamate-receptor-activated release was generally operating in the immature hippocampus. This glutamate-receptor-evoked massive release of taurine could have significant neuroprotective effects, particularly in the developing hippocampus, countering the harmful actions of the simultaneously liberated excitatory amino acids.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Agostinho P, Duarte CB, Carvalho AP, Oliveira CR (1994) Effect of oxidative stress on the release of [3H]GABA in cultured chick retina cells. Brain Res 655: 213–221

    PubMed  Google Scholar 

  • Ben-Ari Y, Tremblay E, Berger M, Nitecka L (1984) Kainic acid seizure syndrome and binding sites in developing rats. Dev Brain Res 14: 284–288

    Google Scholar 

  • Benveniste H, Grejer J, Schousboe A, Diemer NH (1984) Elevation of the extracelfular concentrations of glutamate and aspartate in rat hippocampus during transient cerebral ischemia monitored by intracerebral microdialysis. J Neurochem 43: 1369–1374

    PubMed  Google Scholar 

  • Cherici G, Alesiani M, Pellegrini-Giampiertro DE, Moroni F (1991) Ischemia does not induce the release of excitotoxic amino acids from the hippocampus of newborn rats. Dev Brain Res 60: 235–240

    Google Scholar 

  • Cherubini E, Ben-Ari Y, Krnjevic K (1989) Anoxia produces smaller changes in synaptic transmission, membrane potential and input resistance in immature rat hippocampus. J Neurophysiol 62: 882–895

    PubMed  Google Scholar 

  • Choi DW, Rothman SM (1990) The role of glutamate neurotoxicity in hypoxic-ischemic neuronal death. Annu Rev Neurosci 13: 171–182

    PubMed  Google Scholar 

  • Collard KJ, Menon-Johansson AS (1993) Effects of short-term hypoxia on [3H]glutamate release from preloaded hippocampal and cortical synaptosomes. Neurochem Res 8: 165–170

    Google Scholar 

  • Cook TM, Crutcher KA (1986) Intrahippocampal injection of kainic acid produces significant pyramidal cell loss in neonatal rats. Neuroscience 18: 79–92

    PubMed  Google Scholar 

  • Coyle IT, Puttfarcken P (1993) Oxidative stress, glutamate and neurodegenerative disorders. Science 262: 689–695

    PubMed  Google Scholar 

  • Ferriero DM, Arcavi LJ, Simon RP (1990) Ontogeny of excitotoxic injury to nicotinamide adenine dinucleotide phosphate diaphorase reactive neurons in the neonatal rat striatum. Brain Res 304: 417–424

    Google Scholar 

  • French ED, Vezzani A, Whetsell Jr WO, Schwarcz R (1986) Antiexcitotoxic actions of taurine in the rat hippocampus studied in vivo and in vitro. Adv Exp Med Biol 203: 349–362

    PubMed  Google Scholar 

  • Gilman SC, Bonner MJ, Pellmar TC (1994) Free radicals enhance basal release of D-[3H]aspartate from cerebral cortical synaptosomes. J Neurochem 62: 1757–1763

    PubMed  Google Scholar 

  • Globus MY-T, Busto R, Dietrich WD, Martinez E, Valdes I, Ginsberg MD (1988) Effect of ischemia on the in vivo release of striatal dopamine, glutamate andγ-aminobutyric acid studied by intracerebral microdialysis. J Neurochem 51: 1455–1464

    PubMed  Google Scholar 

  • Haddad GG, Jiang C (1993) O2 deprivation in the central nervous system: on mechanisms of neuronal response, differential sensitivity and injury. Prog Neurobiol 40: 277–318

    PubMed  Google Scholar 

  • Hagberg H, Lehmann A, Sandberg M, Nyström B, Jacobson I, Hamberger A (1985) Ischemic-induced shifts of inhibitory and excitatory amino acids in area CA1 of the rat hippocampus. Dev Brain Res 38: 286–290

    Google Scholar 

  • Halliwell B (1992) Reactive oxygen species and the central nervous system. J Neurochem 59:1609–1623

    PubMed  Google Scholar 

  • Hara H, Sukamoto T, Kogure K (1993) Mechanism and pathogenesis of ischemia-induced neuronal damage. Prog Neurobiol 40: 645–670

    PubMed  Google Scholar 

  • Huxtable RJ (1992) The physiological actions of taurine. Physiol Rev 72: 101–163

    PubMed  Google Scholar 

  • Ikonomidou C, Price MT, Mosinger JL, Friedrich G, Labruyere J, Salles KS, Olney J (1989) Hypobaric-ischemic conditions produce glutamate-like cytopathology in infant rat brain. J Neurosci 9: 1693–1700

    PubMed  Google Scholar 

  • Insel TR, Miller LP, Gelhard RE (1990) The ontogeny of excitatory amino acid receptors in rat forebrain. I. N-methyl-D-aspartate and quisqualate receptors. Neuroscience 35: 31–43

    PubMed  Google Scholar 

  • Janáky R, Saransaari P, Oja SS (1993) Release of GABA from rat hippocampul slices: involvement of quisqualate/N-methyl-D-aspartate-gated ionohpores and extracellular magnesium. Neuroscience 53: 779–785

    PubMed  Google Scholar 

  • Kontro P, Oja SS (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

    Google Scholar 

  • Kontro P, Oja SS (1988) Effects of taurine on the influx and efflux of calcium in brain slices of adult and developing mice. Int J Neurosci 38: 103–109

    PubMed  Google Scholar 

  • Kontro P, Marnela K-M, Oja SS (1980) Free amino acids in the synaptosome and synaptic vesicle fractions of different bovine brain areas. Brain Res 184: 129–141

    PubMed  Google Scholar 

  • Korpi ER, Oja SS (1983) Characteristics of taurine release from cerebral cortex slices induced by sodium-deficient media. Brain Res 289: 197–204

    PubMed  Google Scholar 

  • Laakso M-L, Oja SS (1976) Factors influencing the inulin space in cerebral cortex slices from adult and 7-day-old rats. Acta Physiol Scand 97: 486–494

    PubMed  Google Scholar 

  • Le Grevés P, Hoogendoorn K, Synnergren B, Meyerson B, Nyberg F (1996) The relationship between the NMDA receptor NR1 subunit mRNA and [3H]MK-801 binding in the embryonic and early postnatal rat CNS. Neurosci Res Commun 19: 145–152

    Google Scholar 

  • Lekieffre D, Callebert J, Plotkine M, Boulu RG (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

    PubMed  Google Scholar 

  • Lombardini JB (1976) Regional and subcellular studies on taurine in the rat central nervous system. In: Huxtable R, Barbeau A (eds) Taurine. Raven Press, New York, pp 311–326

    Google Scholar 

  • Magnusson KR, Clements JR, Wu J-Y, Beitz AJ (1989) Colocalization of taurine- and cysteine sulfinic acid decarboxylase-like immunoreactivity in the hippocampus of the rat. Synapse 4: 55–69

    PubMed  Google Scholar 

  • Magnusson KR, Koerner JF, Larson AA, Smullin DH, Skilling SR, Beitz AJ (1991) NMDA-, kainate- and quisqualate-stimulated release of taurine from electrophysiologically monitored rat hippocampal slices. Brain Res 549: 1–8

    PubMed  Google Scholar 

  • McDonald JW, Johnston MV (1990) Physiological and pathophysiological roles of excitatory amino acids during central nervous system development. Brain Res Rev 15: 41–70

    PubMed  Google Scholar 

  • McDonald JW, Johnston MV, Young AB (1990) Differential ontogeny development of three receptors comprising the NMDA receptor/channel complex in the rat hippocampus. Exp Neurol 110: 237–247

    PubMed  Google Scholar 

  • Miller LP, Johnson AE, Gelhard RE, Insel TR (1990) The ontogeny of excitatory amino acid receptors in the rat forebrain — II. Kainic acid receptors. Neuroscience 35: 45–51

    PubMed  Google Scholar 

  • Obrenovitch TP, Urenjak J (1997) Altered glutamatergic transmission in neurological disorders: from high extracellular glutamate to excessive synaptic efficacy. Prog Neurobiol 51: 39–87

    PubMed  Google Scholar 

  • Oja SS (1971) Exchange of taurine in brain slices of adult and 7-day-old rats. J Neurochem 18: 1847–1852

    PubMed  Google Scholar 

  • Oja SS, Kontro P (1981) Oxidation of hypotaurine in vitro by mouse liver and brain tissues. Biochim Biophys Acta 677: 350–357

    PubMed  Google Scholar 

  • Oja SS, Kontro P (1983) Taurine. In: Lajtha A (ed) Handbook of neurochemistry, vol 3, 2nd edn. Plenum Press, New York, pp 501–533

    Google Scholar 

  • Oja SS, Karvonen M-L, Lähdesmäki P (1973) Biosynthesis of taurine and enhancement of decarboxylation of cysteine sulphinate and glutamate by the electrical stimulation of rat brain slices. Brain Res 55: 173–178

    PubMed  Google Scholar 

  • Oja SS, Lehtinen I, Lähdesmäki P (1976) Taurine transport rates between plasma and tissues in adult and 7-day-old mice. Q J Exp Physiol 61: 133–143

    Google Scholar 

  • Oja SS, Korpi ER, Saransaari P (1990) Modification of chloride flux across brain membranes by inhibitory amino acids in developing and adult mice. Neurochem Res 15: 797–804

    PubMed  Google Scholar 

  • O'Regan MH, Smith-Barbour M, Perkins LM, Phillis JW (1995) A possible role for phospholipases in the release of neurotransmitter amino acids from ischemic rat cerebral cortex. Neurosci Lett 185: 191–194

    PubMed  Google Scholar 

  • Pasantes-Morales H, Alavez S, Sánchez Olea R, Morán J (1993) Contribution of organic and inorganic osmolytes to volume regulation in rat brain cells in culture. Neurochem Res 18: 445–452

    PubMed  Google Scholar 

  • Pellmar TC, Neel KL, Lee KH (1989) Free radicals mediate peroxidative damage in the guinea pig hippocampus in vitro. J Neurosci Res 24: 437–444

    PubMed  Google Scholar 

  • Pellegrini-Giampietro DE, Cherici G, Alesiani M, Carlá V, Moroni F (1988) Excitatory amino acid release from rat hippocampal slices as a consequence of free-radical formation. J Neurochem 51: 1960–1963

    PubMed  Google Scholar 

  • Pellegrini-Giampietro DE, Cherici G, Alesiani, M, Carlá V, Moroni F (1990) Excitatory amino acid release and free radical formation may cooperate in the genesis of ischemia-induced neuronal damage. J Neurosci 10: 1035–1041

    PubMed  Google Scholar 

  • Pittaluga A, Raiteri M (1992a) N-Methyl-D-aspartic acid (NMDA) and non-NMDA receptors regulating hippocampal norepinephrine release. III. Changes in the NMDA receptor complex induced by their functional cooperation. J Pharmacol Exp Ther 263: 327–333

    PubMed  Google Scholar 

  • Pittaluga A, Raiteri M (1992b) N-Methyl-D-aspartic acid (NMDA) and non-NMDA receptors regulating hippocampal norepinephrine release. I. Location on axon terminals and pharmacological characterization. J Pharmacol Exp Ther 260: 232–237

    PubMed  Google Scholar 

  • Pokorny J, Yamamoto T (1981a) Postnatal ontogenesis of hippocampal CA1 area in rats. I. Development of dendritic arborization in pyramidal neurons. Brain Res Bull 7: 113–120

    PubMed  Google Scholar 

  • Pokorny J, Yamamoto T (1981b) Postnatal ontogenesis of hippocampal CA1 area in rats. II. Development of ultrastructure in stratum lacunosum and moleculare. Brain Res Bull 7: 121–130

    PubMed  Google Scholar 

  • Pulsinelli WA, Brierley JB, Plum F (1982) Temporal profile of neuronal damage in a model of transient forebrain ischemia. Ann Neurol 11: 491–498

    PubMed  Google Scholar 

  • Represa A, Tremblay E, Ben-Ari Y (1989) Transient increase of NMDA-binding sites in human hippocampus during development. Neurosci Lett 99: 61–66

    PubMed  Google Scholar 

  • Rothman SM, Olney JW (1988) Glutamate and pathology of hypoxic/ischemic brain damage. Ann Neurol 19:105–111

    Google Scholar 

  • Saransaari P, Oja SS (1991) Excitatory amino acids evoke taurine release from cerebral cortex slices from adult and developing mice. Neuroscience 45: 451–459

    PubMed  Google Scholar 

  • Saransaari P, Oja SS (1992) Taurine transport in the mouse cerebral cortex during development and ageing. Adv Exp Med Biol 315: 215–220

    PubMed  Google Scholar 

  • Saransaari P, Oja SS (1994) Taurine release from mouse hippocampal slices: effects of glutamatergic substances and hypoxia. Adv Exp Med Biol 359: 279–287

    PubMed  Google Scholar 

  • Saransaari P, Oja SS (1996) Taurine and neural cell damage: transport of taurine in adult and developing mice. Adv Exp Med Biol 403: 481–490

    PubMed  Google Scholar 

  • Saransaari P, Oja SS (1997a) Enhanced taurine release in cell-damaging conditions in the developing and ageing mouse hippocampus. Neuroscience 79: 847–854

    PubMed  Google Scholar 

  • Saransaari P, Oja SS (1997b) Enhanced GABA release in cell-damaging conditions in the adult and developing mouse hippocampus. Int J Dev Neurosci 15: 163–174

    PubMed  Google Scholar 

  • Schoepp DD, Smith CL, Lodge D, Millar JD, Leander JD, Sacaan AI, Lunn WHW (1991) D,L-(Tetrazol-5-yl)glycine: a novel and highly potent NMDA receptor agonist. Eur J Pharmacol 203: 237–243

    PubMed  Google Scholar 

  • Schousboe A, Morán J, Pasantes-Morales H (1990) Potassium-stimulated release of taurine from cultured cerebellar granule cells is associated with cell swelling. J Neurosci Res 27: 71–77

    PubMed  Google Scholar 

  • Schurr A, Tseng MT, West CA, Rigor BM (1987) Taurine improves the recovery of neuronal function following cerebral hypoxia: an in vitro study. Life Sci 40: 2059–2066

    PubMed  Google Scholar 

  • Smirnova T, Stinnakre J, Mallet J (1993) Characterization of a presynaptic glutamate receptor. Science 262: 430–433

    PubMed  Google Scholar 

  • Sturman JA (1993) Taurine in development. Physiol Rev 73: 119–147

    PubMed  Google Scholar 

  • Taber KH, Lin C-T, Liu J-W, Thalmann R, Wu J-Y (1986) Taurine in hippocampus: localization and postsynaptic action. Brain Res 386: 113–121

    PubMed  Google Scholar 

  • Tang XW, Deupree DL, Sun Y, Wu J-Y (1996) Biphasic effect of taurine on excitatory amino acid-induced neurotoxicity. Adv Exp Med Biol 403: 499–505

    PubMed  Google Scholar 

  • Tremblay E, Roisin MP, Represa A, Charriant-Marlangue C, Ben-Ari Y (1988) Transient increased density of NMDA binding sites in the developing rat hippocampus. Brain Res 461: 393–396

    PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Walz W, Allen AF (1987) Evaluation of the osmoregulatory function of taurine in brain cells. Exp Brain Res 68: 290–298

    PubMed  Google Scholar 

  • Wills ED (1969) Lipid peroxide formation in microsomes. General considerations. Biochem J 113: 315–324

    PubMed  Google Scholar 

  • Wu J-Y, Lin C-T, Johanssen FF, Liu J-W (1994) Taurine neurons in rat hippocampal formation are relatively inert to cerebral ischemia. Adv Exp Med Biol 359: 289–298

    PubMed  Google Scholar 

  • Zorumski CF, Olney JW (1993) Excitotoxic neuronal damage and neuropsychiatric disorders. Pharmacol Ther 59: 145–162

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Tampere Brain Research Center, University of Tampere Medical School, Box 607, FIN-33101, Tampere, Finland

    P. Saransaari & S. S. Ojal

  2. Department of Clinical Physiology, Tampere University Hospital, Tampere, Finland

    S. S. Ojal

Authors
  1. P. Saransaari
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. S. S. Ojal
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Saransaari, P., Ojal, S.S. Glutamate-agonist-evoked taurine release from the adult and developing mouse hippocampus in cell-damaging conditions. Amino Acids 13, 323–335 (1997). https://doi.org/10.1007/BF01372596

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01372596

Keywords

Search

Navigation