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PMID: 10559388 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Dopamine receptors and groups I and II mGluRs cooperate for long-term depression induction in rat prefrontal cortex through converging postsynaptic activation of MAP kinases.

Otani S, Auclair N, Desce JM, Roisin MP, Crépel F

Abstract

Tetanic stimuli to layer I-II afferents in rat prefrontal cortex induced long-term depression (LTD) of layer I-II to layer V pyramidal neuron glutamatergic synapses when tetani were coupled to bath application of dopamine. This LTD was blocked by the following metabotropic glutamate receptor (mGluR) antagonists coapplied with dopamine: (S)-alpha-methyl-4-carboxyphenylglycine (MCPG; group I and II antagonist), (RS)-1-aminoindan-1,5-dicarboxylic acid (AIDA; group I antagonist), or (RS)-alpha-methylserine-O-phosphate monophenyl ester (MSOPPE; group II antagonist). This suggests that the dopamine-facilitated LTD requires synaptic activation of groups I and II mGluRs during tetanus. LTD could also be induced by coupling tetani to bath application of groups I and II mGluR agonist (1S, 3R)-1-aminocyclopentane-1,3-dicarboxylic acid (1S,3R-ACPD). In the next series of experiments, coapplication of dopamine and 1S,3R-ACPD, but not application of either drug alone, consistently induced LTD without tetani or even single test stimuli during drug application, suggesting that coactivation of dopamine receptors and the mGluRs is sufficient for LTD induction. Immunoblot analyses with anti-active mitogen-activated protein kinases (MAP-Ks) revealed that D1 receptors, D2 receptors, group I mGluRs, and group II mGluRs all contribute to MAP-K activation in prefrontal cortex, and that combined activation of dopamine receptors and mGluRs synergistically or additively activate MAP-Ks. Consistently, LTD by dopamine + 1S, 3R-ACPD coapplication, as well as the two other forms of LTD (LTD by dopamine + tetani and LTD by 1S,3R-ACPD + tetani), was blocked by bath application of MAP-K kinase inhibitor PD98059. LTD by dopamine + 1S,3R-ACPD coapplication was also blocked by postsynaptic injection of synthetic MAP-K substrate peptide. Our results suggest that dopamine receptors and groups I and II mGluRs cooperate to induce LTD through converging postsynaptic activation of MAP-Ks.

MeSH Terms
Animals Benzoates/pharmacology Cycloleucine/analogs & derivatives,pharmacology Dopamine/pharmacology Electric Stimulation Enzyme Activation Excitatory Amino Acid Agonists/pharmacology Excitatory Amino Acid Antagonists/pharmacology Glycine/analogs & derivatives,pharmacology In Vitro Techniques Indans/pharmacology Kinetics Male Mitogen-Activated Protein Kinases/metabolism Models, Neurological Neuronal Plasticity/drug effects,physiology Phosphoserine/analogs & derivatives,pharmacology Prefrontal Cortex/drug effects,physiology Rats Rats, Sprague-Dawley Receptors, Dopamine/physiology Receptors, Metabotropic Glutamate/agonists,antagonists & inhibitors,physiology
Chemicals
1-aminoindan-1,5-dicarboxylic acid Benzoates Excitatory Amino Acid Agonists Excitatory Amino Acid Antagonists Indans Receptors, Dopamine Receptors, Metabotropic Glutamate methylserine phosphate Cycloleucine 1-amino-1,3-dicarboxycyclopentane alpha-methyl-4-carboxyphenylglycine Phosphoserine Mitogen-Activated Protein Kinases Glycine Dopamine
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Otani S
Laboratoire de Neurobiologie et Neuropharmacologie du Développement, Institut des Neurosciences, Université de Paris VI, 75005 Paris, France. satoru.otani@snv.jusseiu.fr
Auclair N
Desce J M
Roisin M P
Crépel F
References (66)
66 references, click to expand
  1. Regional, cellular, and subcellular variations in the distribution of D1 and D5 dopamine receptors in primate brain.
    J Neurosci. 1995 Dec;15(12):7821-36 PMID: 8613722
  2. Differential localization of phosphoinositide-linked metabotropic glutamate receptor (mGluR1) and the inositol 1,4,5-trisphosphate receptor in rat brain.
    J Neurosci. 1993 May;13(5):2001-12 PMID: 8386753
  3. Direct dopamine D2-receptor-mediated modulation of arachidonic acid release in transfected CHO cells without the concomitant administration of a Ca2+-mobilizing agent.
    Br J Pharmacol. 1998 Aug;124(8):1651-8 PMID: 9756380
  4. A synthetic inhibitor of the mitogen-activated protein kinase cascade.
    Proc Natl Acad Sci U S A. 1995 Aug 15;92(17):7686-9 PMID: 7644477
  5. Long-term depression in hippocampus.
    Annu Rev Neurosci. 1996;19:437-62 PMID: 8833450
  6. Supranormal stimulation of D1 dopamine receptors in the rodent prefrontal cortex impairs spatial working memory performance.
    J Neurosci. 1997 Nov 1;17(21):8528-35 PMID: 9334425
  7. The convergence of axon terminals from the mediodorsal thalamic nucleus and ventral tegmental area on pyramidal cells in layer V of the rat prelimbic cortex.
    Eur J Neurosci. 1996 Jul;8(7):1340-9 PMID: 8758941
  8. Phenylglycine derivatives discriminate between mGluR1- and mGluR5-mediated responses.
    Neuropharmacology. 1995 Aug;34(8):895-903 PMID: 8532171
  9. A novel metabotropic glutamate receptor agonist: marked depression of monosynaptic excitation in the newborn rat isolated spinal cord.
    Br J Pharmacol. 1993 Aug;109(4):1169-77 PMID: 8401927
  10. Pharmacology and functions of metabotropic glutamate receptors.
    Annu Rev Pharmacol Toxicol. 1997;37:205-37 PMID: 9131252
  11. Dual phosphorylation and autophosphorylation in mitogen-activated protein (MAP) kinase activation.
    Biochem J. 1993 Nov 15;296 ( Pt 1):25-31 PMID: 7504457
  12. The group III metabotropic glutamate receptor agonist, l-AP4, reduces EPSPs in some layers of rat visual cortex.
    Brain Res. 1998 Jun 29;797(2):218-24 PMID: 9666134
  13. Quisqualate Metabotropic Receptors Modulate NMDA Currents and Facilitate Induction of Long-Term Potentiation Through Protein Kinase C.
    Eur J Neurosci. 1992;4(6):500-505 PMID: 12106336
  14. Requirement of rapid Ca2+ entry and synaptic activation of metabotropic glutamate receptors for the induction of long-term depression in adult rat hippocampus.
    J Physiol. 1998 Sep 15;511 ( Pt 3):761-70 PMID: 9714858
  15. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.
    Anal Biochem. 1976 May 7;72:248-54 PMID: 942051
  16. Functions of the frontal cortex of the rat: a comparative review.
    Brain Res. 1984 Nov;320(1):65-98 PMID: 6440660
  17. Dopamine activation of the arachidonic acid cascade as a basis for D1/D2 receptor synergism.
    Nature. 1991 Sep 12;353(6340):164-7 PMID: 1909771
  18. A synaptic model of memory: long-term potentiation in the hippocampus.
    Nature. 1993 Jan 7;361(6407):31-9 PMID: 8421494
  19. PD 098059 is a specific inhibitor of the activation of mitogen-activated protein kinase kinase in vitro and in vivo.
    J Biol Chem. 1995 Nov 17;270(46):27489-94 PMID: 7499206
  20. How MAP kinases are regulated.
    J Biol Chem. 1995 Jun 23;270(25):14843-6 PMID: 7797459
  21. Immunocytochemical localization of group III metabotropic glutamate receptors in the hippocampus with subtype-specific antibodies.
    J Neurosci. 1996 Mar 15;16(6):2044-56 PMID: 8604049
  22. Signal transduction, pharmacological properties, and expression patterns of two rat metabotropic glutamate receptors, mGluR3 and mGluR4.
    J Neurosci. 1993 Apr;13(4):1372-8 PMID: 8463825
  23. Interactions between excitatory amino acids and dopamine systems in the forebrain: implications for schizophrenia and Parkinson's disease.
    Behav Pharmacol. 1995 Aug;6(5 And 6):478-491 PMID: 11224356
  24. Decreased prefrontal dopamine D1 receptors in schizophrenia revealed by PET.
    Nature. 1997 Feb 13;385(6617):634-6 PMID: 9024661
  25. Mitogen-activated protein kinase pathways.
    Curr Opin Cell Biol. 1997 Apr;9(2):180-6 PMID: 9069255
  26. Structure-activity relationships of new agonists and antagonists of different metabotropic glutamate receptor subtypes.
    Br J Pharmacol. 1996 Apr;117(7):1493-503 PMID: 8730745
  27. Modulation of memory fields by dopamine D1 receptors in prefrontal cortex.
    Nature. 1995 Aug 17;376(6541):572-5 PMID: 7637804
  28. Dopamine modulation of synaptic transmission in rat prefrontal cortex: an in vitro electrophysiological study.
    Neurosci Res. 1994 Dec;21(2):151-60 PMID: 7724066
  29. Dopamine facilitates long-term depression of glutamatergic transmission in rat prefrontal cortex.
    Neuroscience. 1998 Aug;85(3):669-76 PMID: 9639264
  30. The protein kinase C family for neuronal signaling.
    Annu Rev Neurosci. 1994;17:551-67 PMID: 8210187
  31. The role of D1-dopamine receptor in working memory: local injections of dopamine antagonists into the prefrontal cortex of rhesus monkeys performing an oculomotor delayed-response task.
    J Neurophysiol. 1994 Feb;71(2):515-28 PMID: 7909839
  32. Activation of p42 mitogen-activated protein kinase in hippocampal long term potentiation.
    J Biol Chem. 1996 Oct 4;271(40):24329-32 PMID: 8798683
  33. Distribution of metabotropic glutamate receptor mGluR5 immunoreactivity in rat brain.
    J Comp Neurol. 1995 May 8;355(3):455-69 PMID: 7636025
  34. A family of metabotropic glutamate receptors.
    Neuron. 1992 Jan;8(1):169-79 PMID: 1309649
  35. Potassium chloride pulse enhances mitogen-activated protein kinase activity in rat hippocampal slices.
    J Neurochem. 1996 Mar;66(3):1005-10 PMID: 8769860
  36. Metabotropic glutamate receptors are involved in long-term potentiation in isolated slices of rat medial frontal cortex.
    J Neurophysiol. 1997 Dec;78(6):3039-46 PMID: 9405523
  37. Activation of glutamatergic neurotransmission by ketamine: a novel step in the pathway from NMDA receptor blockade to dopaminergic and cognitive disruptions associated with the prefrontal cortex.
    J Neurosci. 1997 Apr 15;17(8):2921-7 PMID: 9092613
  38. Use-dependent changes in synaptic efficacy in rat prefrontal neurons in vitro.
    J Physiol. 1990 Aug;427:31-49 PMID: 2213602
  39. The mitogen-activated protein kinase cascade couples PKA and PKC to cAMP response element binding protein phosphorylation in area CA1 of hippocampus.
    J Neurosci. 1999 Jun 1;19(11):4337-48 PMID: 10341237
  40. Ontogenetic and pharmacological studies on metabotropic glutamate receptors coupled to phospholipase D activation.
    Neuropharmacology. 1997 Mar;36(3):305-11 PMID: 9175608
  41. Reversal of phencyclidine effects by a group II metabotropic glutamate receptor agonist in rats.
    Science. 1998 Aug 28;281(5381):1349-52 PMID: 9721099
  42. Multiple presynaptic metabotropic glutamate receptors modulate excitatory and inhibitory synaptic transmission in hippocampal area CA1.
    J Neurosci. 1995 Oct;15(10):6879-89 PMID: 7472445
  43. Cellular basis of working memory.
    Neuron. 1995 Mar;14(3):477-85 PMID: 7695894
  44. Molecular characterization of a novel metabotropic glutamate receptor mGluR5 coupled to inositol phosphate/Ca2+ signal transduction.
    J Biol Chem. 1992 Jul 5;267(19):13361-8 PMID: 1320017
  45. Preferential stimulation of extracellular release of dopamine in rat frontal cortex to striatum following competitive inhibition of the N-methyl-D-aspartate receptor.
    J Neurochem. 1994 Jul;63(1):375-8 PMID: 8207441
  46. Induction of LTP in the hippocampus needs synaptic activation of glutamate metabotropic receptors.
    Nature. 1993 May 27;363(6427):347-50 PMID: 8388549
  47. Molecular, functional, and pharmacological characterization of the metabotropic glutamate receptor type 5 splice variants: comparison with mGluR1.
    J Neurosci. 1995 May;15(5 Pt 2):3970-81 PMID: 7751958
  48. Metabotropic glutamate receptor agonist DCG-IV as NMDA receptor agonist in immature rat hippocampal neurons.
    Eur J Pharmacol. 1994 Sep 12;262(3):287-91 PMID: 7813594
  49. Subtype-specific involvement of metabotropic glutamate receptors in two forms of long-term potentiation in the dentate gyrus of freely moving rats.
    Neuroscience. 1998 Oct;86(3):709-21 PMID: 9692711
  50. Dopamine D2 receptors potentiate arachidonate release via activation of cytosolic, arachidonate-specific phospholipase A2.
    J Neurochem. 1995 Jun;64(6):2765-72 PMID: 7760057
  51. Two distinct forms of long-term depression coexist in CA1 hippocampal pyramidal cells.
    Neuron. 1997 Jun;18(6):969-82 PMID: 9208864
  52. The search for physiological substrates of MAP and SAP kinases in mammalian cells.
    Trends Cell Biol. 1997 Sep;7(9):353-61 PMID: 17708980
  53. alpha-Methyl derivatives of serine-O-phosphate as novel, selective competitive metabotropic glutamate receptor antagonists.
    Neuropharmacology. 1996 Jun;35(6):637-42 PMID: 8887973
  54. Dopamine receptors and brain function.
    Neuropharmacology. 1996;35(11):1503-19 PMID: 9025098
  55. Metabotropic glutamate receptors: a new target for the therapy of neurodegenerative disorders?
    Trends Neurosci. 1996 Jul;19(7):267-71 PMID: 8799968
  56. Corticolimbic dopamine neurotransmission is temporally dissociated from the cognitive and locomotor effects of phencyclidine.
    J Neurosci. 1998 Jul 15;18(14):5545-54 PMID: 9651235
  57. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications.
    Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350-4 PMID: 388439
  58. Dopaminergic A10 neurones are involved in cognitive functions.
    Nature. 1980 Jul 10;286(5769):150-1 PMID: 7402306
  59. Biochemical correlates of long-term potentiation in hippocampal synapses.
    Int Rev Neurobiol. 1993;35:1-41 PMID: 8463060
  60. D1 dopamine receptor immunoreactivity in human and monkey cerebral cortex: predominant and extrasynaptic localization in dendritic spines.
    Proc Natl Acad Sci U S A. 1994 Jun 7;91(12):5720-4 PMID: 7911245
  61. P42/44 MAP kinase inhibitor PD98059 attenuates multiple forms of synaptic plasticity in rat dentate gyrus in vitro.
    J Neurophysiol. 1999 Jan;81(1):103-10 PMID: 9914271
  62. Dependence of long-term depression on postsynaptic metabotropic glutamate receptors in visual cortex.
    Proc Natl Acad Sci U S A. 1993 Apr 15;90(8):3650-4 PMID: 8097320
  63. The metabotropic glutamate receptors, mGluR2 and mGluR3, show unique postsynaptic, presynaptic and glial localizations.
    Neuroscience. 1996 Apr;71(4):949-76 PMID: 8684625
  64. mGluR II agonist inhibition of LTP induction, and mGluR II antagonist inhibition of LTD induction, in the dentate gyrus in vitro.
    Neuroreport. 1997 Feb 10;8(3):687-93 PMID: 9106748
  65. Pharmacological characterization of 1-aminoindan-1,5-dicarboxylic acid, a potent mGluR1 antagonist.
    J Pharmacol Exp Ther. 1997 May;281(2):721-9 PMID: 9152378
  66. Dopamine favours the emergence of long-term depression versus long-term potentiation in slices of rat prefrontal cortex.
    Neurosci Lett. 1995 Mar 24;188(2):125-8 PMID: 7792056
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
1529-2401
Published
1999-11-15
Pages
9788-802
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6782965
Subset
IM
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