Presynaptic κ-opioid and muscarinic receptors inhibit the calcium- dependent component of evoked glutamate release from striatal synaptosomes

Journal of Neurochemistry

Volumn 73, Issue 3, 1999, Pages 1058-1065

  Rawls, Scott M ^a   McGinty, Jacqueline F ^a   Terrian, David M ^a,b  

^a EAST CAROLINA UNIVERSITY   (United States)

^b MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

D Pen2,5 enkephalin; Glutamate; L trans Pyrrolidine 2,4 dicarboxylic acid; Opioid receptors; Oxotremorine; Presynaptic; Striatum; U 69593

Indexed keywords

2,4 PYRROLIDINEDICARBOXYLIC ACID; 4 AMINOPYRIDINE; ENKEPHALIN[2,5 DEXTRO PENICILLAMINE]; EXCITATORY AMINO ACID; EXCITATORY AMINO ACID RECEPTOR; GLUTAMIC ACID; KAPPA OPIATE RECEPTOR; KAPPA OPIATE RECEPTOR AGONIST; MUSCARINIC AGENT; MUSCARINIC RECEPTOR; N METHYL N [7 (1 PYRROLIDINYL) 1 OXASPIRO[4.5]DEC 8 YL]BENZENEACETAMIDE; OXOTREMORINE; PRESYNAPTIC RECEPTOR;

ANIMAL TISSUE; ARTICLE; BASAL GANGLION; CONCENTRATION RESPONSE; CORPUS STRIATUM; EXOCYTOSIS; FEEDBACK SYSTEM; MALE; NERVE ENDING; NONHUMAN; PRESYNAPTIC INHIBITION; PRIORITY JOURNAL; RAT; SYNAPTOSOME;

4-AMINOPYRIDINE; ANIMALS; CALCIUM; CHELATING AGENTS; DICARBOXYLIC ACIDS; EGTAZIC ACID; ENKEPHALIN, D-PENICILLAMINE (2,5)-; ENKEPHALINS; GLUTAMIC ACID; MALE; MUSCARINIC AGONISTS; MUSCARINIC ANTAGONISTS; NALTREXONE; NARCOTIC ANTAGONISTS; NEOSTRIATUM; NERVE ENDINGS; NEUROTRANSMITTER UPTAKE INHIBITORS; POTASSIUM CHANNEL BLOCKERS; POTASSIUM CHANNELS; PYRROLIDINES; RATS; RATS, WISTAR; RECEPTORS, MUSCARINIC; RECEPTORS, OPIOID, KAPPA; RECEPTORS, PRESYNAPTIC; SYNAPTOSOMES;

EID: 0032840525     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.1999.0731058.x     Document Type: Article

References (61)

1. Acquas E., Meloni M., and Di Chiara G. (1993) Blockade of delta-opioid receptors in the nucleus accumbens prevents ethanol-induced stimulation of dopamine release. Eur. J. Pharmacol. 230, 239-241.
2. 2+ current in rat magnocellular cholinergic basal forebrain neurones. J. Physiol. (Lond.) 466, 173-189.
3. Bolam J. P., Wainer B. H., and Smith A. D. (1984) Characterization of cholinergic neurons in the rat neostriatum. A combination of choline acetyltransferase immunocytochemistry, Golgi impregnation and electron microscopy. Neuroscience 12, 711-725.
4. Bridges R. J., Stanley M. S., Anderson M. W., Cotman C. W., and Chamberlain A. R. (1991) Conformationally defined neurotransmitter analogues. Selective inhibition of glutamate uptake by the L-trans-pyrrolidine-2,4-dicarboxylate diastereomer. J. Med. Chem. 34, 717-725.
5. Calabresi P., Centonze D., Gubelline P., Pisani A., and Bernadi G. (1998) Blockade of M2-like muscarinic receptors enhances long-term potentiation at corticostriatal synapses. Eur. J. Neurosci. 10, 3020-3023.
6. Dourmap N., Michael-Titus A., and Costentin J. (1992) Differential effect of intrastriatal kainic acid on the modulation of dopamine release by μ and δ-opioid peptides: a microdialysis study. J. Neurochem. 58, 709-713.
7. 2+ channels in mammalian central neurons. Trends Neurosci. 18, 89-98.
8. Fonnum F., Storm-Mathisen J., and Divac L. (1981) Biochemical evidence for glutamate as a neurotransmitter in corticostriatal and corticothalamic fibers in rat brain. Neuroscience 6, 863-873.
9. Gannon R. L. and Terrian D. M. (1992) Kappa opioid agonists inhibit transmitter release from guinea pig hippocampal mossy fiber synaptosomes. Neurochem. Res. 17, 741-747.
10. George S. R., Zastawny R. L., Briones-Urbina R., Cheng R., Nguyen T., Heiber M., Kouvelas A., Chan A. S., and O'Dowd B. F. (1994) Distinct distributions of mu, delta, and kappa opioid receptor mRNA in rat brain. Biochem. Biophys. Res. Commun. 205, 1438-1444.
11. 3H] glutamic acid in rat neostriatum. Cell. Mol. Neurobiol. 4, 117-124.
12. Gray A. M., Rawls S. M., Shippenberg T. S., and McGinty J. F. (1999) The κ opioid agonist, U-69593, decreases acute amphetamine-evoked behaviors and calcium-dependent dialysate levels of dopamine and glutamate in the ventral striatum. J. Neurochem. 73, 1066-1074.
13. Griffiths R., Dunlop J., Gorman A., Senior J., and Grieve A. (1994) L-trans-Pyrrolidine-2,4-dicarboxylate and cis-1-aminocyclobutane-1,3-dicarboxylate behave as transportable, competitive inhibitors of the high-affinity glutamate transporters. Biochem. Pharmacol. 47, 267-274.
14. Grudt T. J. and Williams J. T. (1993) Kappa-opioid receptors also increase potassium conductance. Proc. Natl. Acad. Sci. USA 90, 11429-11432.
15. Grudt T. J. and Williams J. T. (1995) Opioid receptors and the regulation of ion conductances. Annu. Rev. Neurosci. 6, 279-286.
16. Heijna M. H., Padt M., Hogenboom H., Portoghese P. S., Mulder A. H., and Schoffelmeer A. N. M. (1990) Opioid receptor-mediated inhibition of dopamine and acetylcholine release from slices of rat nucleus accumbens, olfactory tubercle and frontal cortex. Eur. J. Pharmacol. 18, 267-278.
17. Hernandez-Echeagaray E., Galarraga E., and Bargas J. (1998) 3-α-Chloro-imperialine, a potent blocker of cholinergic presynaptic modulation of glutamatergic afferents in the rat neostriatum. Neuropharmacology 37, 1493-1502.
18. Hersch S. M. and Levey A. I. (1995) Diverse pre- and post-synaptic expression of m1-m4 muscarinic receptor proteins in neurons and afferents in the rat neostriatum. Life Sci. 56, 931-938.
19. Hill M. and Brotchie J. (1995) Modulation of glutamate release by a kappa-opioid agonist in rodent and primate striatum. Eur. J. Pharmacol. 281, R1-R2.
20. Howe A. R. and Surmeier D. J. (1995) Muscarinic receptors modulate N-, P-, and L-type calcium currents in rat striatal neurones through parallel pathways. J. Neurosci. 15, 458-469.
21. Hulme E. C., Birdsall N. J. M., and Buckley N. J. (1990) Muscarinic receptor subtypes. Annu. Rev. Pharmacol. Toxicol. 30, 633-673.
22. Jiang Z. G. and Dun N. J. (1986) Presynaptic suppression of excitatory postsynaptic potentials in rat ventral horn neurons by muscarinic agonists. Brain Res. 381, 182-186.
23. Jiang Z. G. and North R. A. (1992) Pre- and postsynaptic inhibition by opioids in rat striatum. J. Neurosci. 12, 356-361.
24. Kaneko S., Fukuda K., Yada N., Akaike A., Mori Y., and Satoh M. (1994) Calcium channel inhibition by kappa opioid receptors expressed in Xenopus oocytes. Neuroreport 5, 2506-2508.
25. Kanemasa T., Asakura K., and Ninomiya M. (1995) Kappa-opioid agonist U50,488 inhibits P-type calcium channels by two mechanisms. Brain Res. 702, 207-212.
26. Le Moine C., Kieffer B., Gaveriaux-Ruff C., Befort K., and Bloch B. (1994) Delta-opioid receptor gene expression in the mouse fore-brain: localization in cholinergic neurons of the striatum. Neuroscience 62, 635-640.
27. Linial M., Ilouz N., and Parnas H. (1997) Voltage-dependent interaction between the muscarinic acetylcholine receptor and proteins of the exocytotic machinery. J. Physiol. 504, 251-258.
28. Maneuf Y. P., Mitchell I. J., Crossman A., Woodruff G., and Brotchie J. (1995) Functional implications of kappa opioid receptor-mediated modulation of glutamate transmission in the output regions of the basal ganglia in rodent and primate models of Parkinson's disease. Brain Res. 683, 102-108.
29. Mansour A., Khachaturian M. E., Lewis M. E., Akil H., and Watson S. J. (1987) Autoradiographic differentiation of mu, delta, and kappa opioid receptors in the rat forebrain and midbrain. J. Neurosci. 7, 2445-2464.
30. Mansour A., Thompson R. C., Akil H., and Watson S. J. (1993) Delta opioid receptor mRNA distribution in the brain: comparison to delta receptor binding and proenkephalin mRNA. J. Chem. Neuroanat. 6, 351-362.
31. Mansour A., Fox C., Burke S., Meng F., Thompson R., Akil H., and Watson S. J. (1994) Mu, delta, and kappa opioid receptor mRNA expression in the rat CNS: an in situ hybridization study. J. Comp. Neurol. 350, 412-438.
32. Marchi M. and Raiteri M. (1988) Interaction of acetylcholine-glutamate in rat hippocampus: involvement of two subtypes of M-2 muscarinic receptors. J. Pharmacol. Exp. Ther. 248, 1255-1260.
33. McMahon H. T. and Nicholls D. G. (1991) The bioenergetics of neurotransmitter release. Biochim. Biophys. Acta 1059, 243-264.
34. Meshul C. K. and McGinty J. F. (1999) Kappa opioid receptor immunoreactivity in nucleus accumbens shell and caudate-putamen is primarily associated with synaptic vesicles in axons. Neuroscience (in press).
35. Mulder A. H., Wardeh G., Hogenboom F., and Frankhuyzen A. L. (1984) Kappa- and delta-opioid agonists differentially inhibit striatal dopamine and acetylcholine release. Nature 308, 278-280.
36. Nicholls D. G. and Sihra T. S. (1986) Synaptosomes possess an exocytotic pool of glutamate. Nature 321, 772-773.
37. 3H-U-69,593 binding sites in rat brain: evidence for kappa opioid receptor subtypes. Eur. J. Pharmacol. 154, 27-34.
38. Parent A. and Hazrati L.-N. (1995) Functional anatomy of the basal ganglia. I. The cortico-basal ganglia-thalamo-cortical loop. Brain Res. Rev. 20, 91-127.
39. Rawls S. M. and McGinty J. F. (1997) L-trans-Pyrrolidine-2,4-dicarboxylic acid-evoked glutamate levels are attenuated by calcium reduction, tetrodotoxin, and glutamate receptor blockade. J. Neurochem. 68, 1553-1563.
40. Rawls S. M. and McGinty J. F. (1998a) K receptor activation attenuates L-trans-pyrrolidine-2,4-dicarboxylic acid-evoked glutamate levels in the striatum. J. Neurochem. 70, 626-634.
41. Rawls S. M. and McGinty J. F. (1998b) Muscarinic receptors regulate extracellular glutamate levels in the rat striatum: an in vivo microdialysis study. J. Pharmacol. Exp. Ther. 286, 91-98.
42. Sandberg M., Butcher S. P., and Hagberg H. (1986) Extracellular overflow of neuroactive amino acids during severe insulin-induced hypoglycemia: in vivo dialysis of the rat hippocampus. J. Neurochem. 47, 178-184.
43. Sandor N. T., Lendvai B., and Vizi E. S. (1992) Effect of selective opiate antagonists on striatal acetylcholine and dopamine release. Brain Res. Bull. 29, 369-373.
44. Schad C. A., Justice J. B. Jr., and Holtzman S. G. (1996) Differential effects of δ- and μ-opioid receptor antagonists on the amphetamine-induced increase in extracellular dopamine in striatum and nucleus accumbens. J. Neurochem. 67, 2292-2299.
45. Schlame M. and Hemmings H. C. (1995) Inhibition by volatile anesthetics of endogenous glutamate release from synaptosomes by presynaptic mechanism. Anesthesiology 82, 1406-1416.
46. Schoffelmeer A. N. M., Rice K. C., Jacobson A. E., Van Gelderen J. G., Hogenboom F., Heijna N. H., and Mulder A. H. (1988) Mu-, delta-, and kappa-opioid mediated inhibition of neurotransmitter release and adenylate cyclase activity in rat brain slices: studies with fentanyl isothiocyanate. Eur. J. Pharmacol. 154, 169-178.
47. Semba K., Fibiger H. C., and Vincent S. R. (1987) Neurotransmitters in the mammalian striatum: neuronal circuits and heterogeneity. Can. J. Neurol. Sci. 14, 386-394.
48. Sheng Z., Retting J., Cook T., and Catterall W. A. (1996) Calcium-dependent interaction of N-type calcium channels with the synaptic core complex. Nature 379, 451-454.
49. Simmons M. L. and Chavkin C. (1996) Kappa opioid receptor activation of a dendrotoxin-sensitive potassium channel mediates pre-synaptic inhibition of mossy fiber neurotransmitter release. Mol. Pharmacol. 50, 80-85.
50. Smolders I., Bogaert L., Ebinger G., and Michotte Y. (1997) Muscarinic modulation of striatal dopamine, glutamate, GABA release, as measured with in vivo microdialysis. J. Neurochem. 68, 1942-1948.
51. 2+ currents in rat sensorimotor pyramidal cells via two distinct pathways. J. Neurophysiol. 81, 72-84.
52. Svingos A. L., Clarke C. L., and Pickel V. M. (1998) Cellular sites for activation of delta-opioid receptors in the rat nucleus accumbens shell: relationship with met-enkephalin. J. Neurosci. 18, 1923-1933.
53. Tallent M., Dichter M. A., Bell G. I., and Reisine T. (1994) The cloned kappa opioid receptor couples to an N-type calcium current in undifferentiated PC-12 cell lines. Neuroscience 63, 1033-1040.
54. Terman G. W., Wagner J. J., and Chavkin C. (1994) Kappa opioids inhibit induction of long-term potentiation in the dentate gyrus of the guinea pig hippocampus. J. Neurosci. 14, 4740-4747.
55. Tibbs G. R., Barrie A. P., Van Mieghem F., McMahon H. T., and Nicholls D. G. (1989a) Repetitive action potentials in isolated nerve terminals in the presence of 4-aminopyridine: effects on cytosolic free calcium and glutamate release. J. Neurochem. 53, 1693-1699.
56. Tibbs G. R., Dolly J. O., and Nicholls D. G. (1989b) Dendrotoxin, 4-aminopyridine, and beta-bungarotoxin act at common loci but by two distinct mechanisms to induce calcium-dependent release of glutamate from guinea-pig cerebrocortical synaptosomes. J. Neurochem. 52, 201-206.
57. 2 opioid receptors in rat and guinea pig brain. Brain Res. 562, 57-65.
58. Wagner J. J., Caudle R. M., and Chavkin C. (1992) Kappa-opioids decrease excitatory transmission in the dentate gyrus of the guinea pig hippocampus. J. Neurosci. 12, 132-141.
59. Waldmeier P. C., Wicki P., and Feldtrauer J. (1993) Release of endogenous glutamate from rat cortical slices in the presence of the glutamate uptake inhibitor L-trans-pyrrolidine-2,4-dicarboxylic acid. Naunyn Schmiedbergs Arch. Pharmacol. 348, 478-485.
60. Weiner D. M., Levey A. I., and Brann M. R. (1990) Expression of muscarinic acetylcholine and dopamine receptor mRNAs in rat basal ganglia. Proc. Natl. Acad. Sci. USA 87, 7050-7054.
61. ++ currents in rat neostriatal cholinergic inter-neurons through a fast, membrane-delimited, G-protein pathway. J. Neurosci. 16, 2592-2604.