DOI: 10.1111/j.1471-4159.1990.tb01226.x. Glutamate‐Evoked Release of Endogenous Adenosine from Rat Cortical Synaptosomes Is Mediated by Glutamate Uptake and Not by Receptors

Glutamate‐Evoked Release of Endogenous Adenosine from Rat Cortical Synaptosomes Is Mediated by Glutamate Uptake and Not by Receptors

10.1111/j.1471-4159.1990.tb01226.x

Crossref journal-article

Wiley

Journal of Neurochemistry (311)

Abstract

Abstract: L‐Glutamate (10 μM–1 mM) released endogenous adenosine from rat cortical synaptosomes. Studies with excitatory amino acid antagonists, (+)‐5‐methyl‐16, 11,dihydro‐5H‐dibenzo[a,d]cyclohepten‐5, 10‐imine maleate (MK‐801), 6,7‐dinitroquinoxaline‐2,3‐dione (DNQX), Mg2+, and agonists N‐methyl‐D‐aspartate (NMDA), kainate, and quisqualate, indicated that this release was not receptor mediated. D,L‐2‐Amino‐4‐phosphonobutanoic acid (APB) also did not affect glutamate‐evoked adenosine release. Inhibition of glutamate uptake by dihydrokainate or replacement of extracellular Na+ blocked glutamate‐evoked adenosine release. D‐aspartate, which is a substrate for the glutamate transporter but is not metabolized, also released adenosine, suggesting that release was due to amino acid transport and not to its subsequent metabolism. D‐Glutamate, a relatively poor substrate for the transporter, was correspondingly less potent than L‐glutamate at releasing adenosine. Glutamate‐evoked adenosine release was not Ca2+ dependent or tetrodotoxin sensitive and did not appear to occur on the bidirectional nucleoside transporter. Inhibition of ecto‐5′‐nucleotidase virtually abolished glutamate‐evoked adenosine release, indicating that adenosine was derived from extracellular metabolism of released nucleotide(s). However, L‐glutamate did not release ATP and did not appear to release cyclic AMP. Therefore, transport of glutamate into presynaptic terminals releases some other nucleotide which is converted extracellularly to adenosine. This adenosine could act at P1‐purinoceptors to modulate glutamatergic neurotransmission.

Bibliography

Hoehn, K., & White, T. D. (1990). GlutamateâEvoked Release of Endogenous Adenosine from Rat Cortical Synaptosomes Is Mediated by Glutamate Uptake and Not by Receptors. Journal of Neurochemistry, 54(5), 1716â1724. Portico.

Authors 2

Katja Hoehn (first)
Thomas D. White (additional)

References 54 Referenced 50

10.1111/j.1476-5381.1987.tb11273.x
10.1111/j.1471-4159.1972.tb01325.x
10.1042/bst0160881 / Biochem. Soc. Trans. / Presynaptic regulation of glutamate release from guinea‐pig cortical synaptosomes by Barrie A. (1988)
10.1111/j.1471-4159.1976.tb01493.x
10.1126/science.178.4064.997
10.1111/j.1471-4159.1989.tb07267.x
10.1016/0006-8993(80)90367-4
10.1016/0024-3205(89)90479-7
10.1038/330604a0
10.1523/JNEUROSCI.08-08-02948.1988 / J. Neurosci. / Glutamate positive corticocortical neurons in the somatic sensory areas I and II of cats by Conti F. (1988)
10.1016/0014-2999(84)90364-9
10.1111/j.1471-4159.1976.tb06485.x
10.1016/0304-3940(83)90127-1
10.1038/316148a0
{'key': 'e_1_2_2_16_1', 'first-page': '193', 'article-title': 'Neuroprotective effects of adenosine', 'volume': '9', 'author': 'Dragunow M.', 'year': '1988', 'journal-title': 'Trends Neurosci.'} / Trends Neurosci. / Neuroprotective effects of adenosine by Dragunow M. (1988)
10.1016/0006-8993(88)90553-7
{'key': 'e_1_2_2_18_1', 'first-page': '63', 'article-title': 'The physiological role of adenosine in the central nervous system', 'volume': '27', 'author': 'Dunwiddie T. V.', 'year': '1985', 'journal-title': 'Int. Rev. Biochem.'} / Int. Rev. Biochem. / The physiological role of adenosine in the central nervous system by Dunwiddie T. V. (1985)
10.1016/0006-2952(87)90001-3
10.1111/j.1471-4159.1989.tb10907.x
10.1111/j.1748-1716.1985.tb07698.x
10.1007/BF00167254
10.1111/j.1476-5381.1988.tb11680.x
10.1111/j.1471-4159.1984.tb09689.x
{'key': 'e_1_2_2_25_1', 'first-page': '791', 'article-title': "Glutamate autoreceptors reduce EPSC's in cultured hippocampal neurons", 'volume': '14', 'author': 'Forsythe I. D.', 'year': '1988', 'journal-title': 'Soc. Neurosci. Abstr.'} / Soc. Neurosci. Abstr. / Glutamate autoreceptors reduce EPSC's in cultured hippocampal neurons by Forsythe I. D. (1988)
10.1016/0165-6147(88)90194-0
10.1126/science.6302841
10.1016/0003-2697(72)90094-2
10.1038/249663a0
10.1016/0006-8993(76)90274-2
{'key': 'e_1_2_2_31_1', 'first-page': '1095', 'article-title': 'Adenosine inhibition of glutamate and dynorphin release from hippocampal mossy fibre synaptosomes', 'volume': '14', 'author': 'Hernandez P. G.', 'year': '1988', 'journal-title': 'Soc. Neurosci. Abstr.'} / Soc. Neurosci. Abstr. / Adenosine inhibition of glutamate and dynorphin release from hippocampal mossy fibre synaptosomes by Hernandez P. G. (1988)
{'key': 'e_1_2_2_32_1', 'first-page': '49', 'article-title': 'Evoked release of endogenous adenosine from rat cortical slices by K+ and glutamate', 'volume': '478', 'author': 'Hoehn K.', 'year': '1988', 'journal-title': 'Brain Res.'} / Brain Res. / Evoked release of endogenous adenosine from rat cortical slices by K+ and glutamate by Hoehn K. (1988)
Hoehn K.andWhite T. D.(1989)Glutamate‐evoked release of adenosine from rat cortical synaptosomes is not receptor‐mediated. (Abstr.)ISN Satellite Symposium on Adenosine Receptors in the Nervous System p.54. (10.1111/j.1471-4159.1990.tb01226.x)
10.1111/j.1471-4159.1990.tb13309.x
10.1111/j.1471-4159.1979.tb04518.x
{'key': 'e_1_2_2_36_1', 'first-page': '47', 'volume-title': 'Frontiers in Excitatory Amino Acid Research', 'author': 'Keith R. A.', 'year': '1988'} / Frontiers in Excitatory Amino Acid Research by Keith R. A. (1988)
10.1016/0304-3940(79)96172-X
10.1016/0006-8993(80)91211-1
10.1111/j.1471-4159.1985.tb04062.x
{'key': 'e_1_2_2_40_1', 'first-page': '80', 'article-title': 'Effects of dipyridamole and adenosine agonists on adenosine release', 'volume': '31', 'author': 'MacDonald W. F.', 'year': '1988', 'journal-title': 'Can. Fed. Biol. Sci.'} / Can. Fed. Biol. Sci. / Effects of dipyridamole and adenosine agonists on adenosine release by MacDonald W. F. (1988)
{'key': 'e_1_2_2_41_1', 'first-page': '323', 'volume-title': 'Physiological and Regulatory Functions of Adenosine and Adenine Nucleotides', 'author': 'Manery J. F.', 'year': '1979'} / Physiological and Regulatory Functions of Adenosine and Adenine Nucleotides by Manery J. F. (1979)
10.1016/0301-0082(87)90011-6
10.1111/j.1471-4159.1989.tb07296.x
10.1146/annurev.pa.29.040189.002053
{'key': 'e_1_2_2_45_1', 'first-page': '967', 'article-title': 'Ecto‐ATP‐ase of mammalian synaptosomes: identification and enzymatic characterization', 'volume': '47', 'author': 'Nagy A. K.', 'year': '1986', 'journal-title': 'J. Neurochem.'} / J. Neurochem. / Ecto‐ATP‐ase of mammalian synaptosomes: identification and enzymatic characterization by Nagy A. K. (1986)
10.1016/0014-2999(88)90607-3
10.1016/0014-2999(75)90214-9
10.1016/0306-4522(80)90207-9
10.1111/j.1748-1716.1975.tb05912.x
10.1016/0166-2236(87)90177-9
{'key': 'e_1_2_2_51_1', 'first-page': '563', 'article-title': 'Stimulatory effect of FSH in vitro on the extracellularly active cyclic AMP phosphodiesterase in the prepubertal rat ovary', 'volume': '81', 'author': 'Selstam G.', 'year': '1976', 'journal-title': 'Acta Endocrinol.'} / Acta Endocrinol. / Stimulatory effect of FSH in vitro on the extracellularly active cyclic AMP phosphodiesterase in the prepubertal rat ovary by Selstam G. (1976)
10.1111/j.1471-4159.1976.tb02624.x
10.1038/267067a0
10.1111/j.1471-4159.1978.tb06534.x
10.1073/pnas.83.18.7104

Dates

Type	When
Created	18 years, 11 months ago (Oct. 5, 2006, 8:33 p.m.)
Deposited	1 year, 11 months ago (Sept. 27, 2023, 4:10 a.m.)
Indexed	1 month, 4 weeks ago (July 7, 2025, 1:45 a.m.)
Issued	35 years, 4 months ago (May 1, 1990)
Published	35 years, 4 months ago (May 1, 1990)
Published Online	18 years, 11 months ago (Oct. 5, 2006)
Published Print	35 years, 4 months ago (May 1, 1990)

Funders 0

None

BibTeX

@article{Hoehn_1990, title={Glutamate‐Evoked Release of Endogenous Adenosine from Rat Cortical Synaptosomes Is Mediated by Glutamate Uptake and Not by Receptors}, volume={54}, ISSN={1471-4159}, url={http://dx.doi.org/10.1111/j.1471-4159.1990.tb01226.x}, DOI={10.1111/j.1471-4159.1990.tb01226.x}, number={5}, journal={Journal of Neurochemistry}, publisher={Wiley}, author={Hoehn, Katja and White, Thomas D.}, year={1990}, month=may, pages={1716–1724} }

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