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PMID: 11698615 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Repeated cocaine administration attenuates group I metabotropic glutamate receptor-mediated glutamate release and behavioral activation: a potential role for Homer.

The Journal of neuroscience : the official journal of the Society for Neuroscience ·Vol. 21 ·No. 22 ·2001-11-15 ·Pages 9043-52

Swanson CJ, Baker DA, Carson D, Worley PF, Kalivas PW

Abstract

The present study aimed to characterize a functional role for group I metabotropic glutamate receptors (mGluRs) in the nucleus accumbens and the capacity of repeated cocaine to elicit long-term changes in group I mGluR function. Reverse dialysis of the group I agonist (RS)-3,5-dihydroxyphenylglycine (DHPG) into the nucleus accumbens resulted in an increase in extracellular glutamate levels that was mediated by the mGluR1 subtype and depended on voltage-dependent Na(+) and Ca(2+) conductance. At 3 weeks after discontinuing 1 week of daily cocaine injections, the capacity of DHPG to induce glutamate release was markedly reduced. Similarly, DHPG induced an mGluR1-dependent increase in locomotor activity after microinjection into the nucleus accumbens that was significantly blunted 3 weeks after repeated cocaine administration. Signaling through group I mGluRs is regulated, in part, by Homer proteins, and it was found that the blunting of group I mGluR-induced glutamate release and motor activity after repeated cocaine was associated with a reduction in Homer1b/c protein that was selective for the medial nucleus accumbens. These data show that repeated cocaine produces an enduring inhibition of the neurochemical and behavioral consequences of stimulating mGluR1 that is accompanied by changes in the mGluR scaffolding apparatus.

MeSH Terms
Animals Brain Chemistry/drug effects Calcium Channel Blockers/pharmacology Carrier Proteins/metabolism Cocaine/administration & dosage Drug Administration Schedule Drug Tolerance Excitatory Amino Acid Agonists/pharmacology Excitatory Amino Acid Antagonists/pharmacology Extracellular Space/chemistry,metabolism Glutamic Acid/metabolism Glycine/analogs & derivatives,pharmacology Homer Scaffolding Proteins Male Microdialysis Motor Activity/drug effects Neuropeptides/metabolism Nucleus Accumbens/drug effects,metabolism Rats Rats, Inbred Strains Rats, Sprague-Dawley Receptor, Metabotropic Glutamate 5 Receptors, AMPA/metabolism Receptors, Metabotropic Glutamate/agonists,antagonists & inhibitors,metabolism Resorcinols/pharmacology Tetrodotoxin/administration & dosage
Chemicals
Calcium Channel Blockers Carrier Proteins Excitatory Amino Acid Agonists Excitatory Amino Acid Antagonists Homer Scaffolding Proteins Neuropeptides Receptor, Metabotropic Glutamate 5 Receptors, AMPA Receptors, Metabotropic Glutamate Resorcinols metabotropic glutamate receptor type 1 Glutamic Acid Tetrodotoxin 3,5-dihydroxyphenylglycine Cocaine Glycine
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Swanson C J
Department of Physiology and Neuroscience, Medical University of South Carolina, Charleston, South Carolina 29425, USA.
Baker D A
Carson D
Worley P F
Kalivas P W
References (51)
51 references, click to expand
  1. SNARE protein-dependent glutamate release from astrocytes.
    J Neurosci. 2000 Jan 15;20(2):666-73 PMID: 10632596
  2. Role of extracellular dopamine in the initiation and long-term expression of behavioral sensitization to cocaine.
    J Pharmacol Exp Ther. 1996 Aug;278(2):490-502 PMID: 8768696
  3. Addiction, dopamine, and the molecular mechanisms of memory.
    Neuron. 2000 Mar;25(3):515-32 PMID: 10774721
  4. New perspectives for the development of selective metabotropic glutamate receptor ligands.
    Eur J Pharmacol. 1999 Jun 30;375(1-3):277-94 PMID: 10443583
  5. 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
  6. Reciprocal changes in dopamine responsiveness in the nucleus accumbens shell and core and in the dorsal caudate-putamen in rats sensitized to morphine.
    Neuroscience. 1999 May;90(2):447-55 PMID: 10215150
  7. Positive feedback of glutamate exocytosis by metabotropic presynaptic receptor stimulation.
    Nature. 1992 Nov 12;360(6400):163-6 PMID: 1359425
  8. Regulation of locomotor activity by metabotropic glutamate receptors in the nucleus accumbens and ventral tegmental area.
    J Pharmacol Exp Ther. 2000 Jan;292(1):406-14 PMID: 10604977
  9. Pharmacology and functions of metabotropic glutamate receptors.
    Annu Rev Pharmacol Toxicol. 1997;37:205-37 PMID: 9131252
  10. Role of L- and N-type calcium channels in the pathophysiology of traumatic spinal cord white matter injury.
    Neuroscience. 2000;99(1):179-88 PMID: 10924962
  11. Homer: a protein that selectively binds metabotropic glutamate receptors.
    Nature. 1997 Mar 20;386(6622):284-8 PMID: 9069287
  12. Amphetamine-induced time-dependent sensitization of dopamine neurotransmission in the dorsal and ventral striatum: a microdialysis study in behaving rats.
    Synapse. 1995 Jan;19(1):56-65 PMID: 7709344
  13. The effect of previous exposure to amphetamine on drug-induced locomotion and self-administration of a low dose of the drug.
    Psychopharmacology (Berl). 1999 Nov;147(2):125-34 PMID: 10591879
  14. Modulation of calcium channels by group I and group II metabotropic glutamate receptors in dentate gyrus neurons from patients with temporal lobe epilepsy.
    Epilepsia. 2000 Oct;41(10):1249-58 PMID: 11051119
  15. Potentiation of synaptic transmission in the rat dentate gyrus in vitro by (S)-3,5-dihydroxyphenylglycine ((S)-DHPG).
    Neurosci Lett. 1997 Jun 20;229(1):29-32 PMID: 9224794
  16. Repeated cocaine modifies the mechanism by which amphetamine releases dopamine.
    J Neurosci. 1997 May 1;17(9):3254-61 PMID: 9096158
  17. Persistent phosphorylation parallels long-term desensitization of cerebellar purkinje cell AMPA-type glutamate receptors.
    Learn Mem. 1997 Mar-Apr;3(6):578-91 PMID: 10456118
  18. Behavioral and neurochemical effects of acute and daily cocaine administration in rats.
    J Pharmacol Exp Ther. 1988 May;245(2):485-92 PMID: 3130474
  19. Metabotropic glutamate receptor-mediated control of neurotransmitter release.
    Neuron. 1998 May;20(5):1007-16 PMID: 9620704
  20. Catecholamine innervation of the basal forebrain. IV. Topography of the dopamine projection to the basal forebrain and neostriatum.
    J Comp Neurol. 1978 Aug 1;180(3):545-80 PMID: 659674
  21. Activation of metabotropic glutamate receptor 5 has direct excitatory effects and potentiates NMDA receptor currents in neurons of the subthalamic nucleus.
    J Neurosci. 2000 Nov 1;20(21):7871-9 PMID: 11050106
  22. Pharmacological characterisation of metabotropic glutamatergic and purinergic receptors linked to Ca2+ signalling in hippocampal astrocytes.
    Neuropharmacology. 1998;37(2):169-78 PMID: 9680241
  23. Potentiation of NMDA and AMPA responses by the specific mGluR5 agonist CHPG in spinal cord motoneurons.
    Neuropharmacology. 1999 Oct;38(10):1569-76 PMID: 10530818
  24. Repeated cocaine augments excitatory amino acid transmission in the nucleus accumbens only in rats having developed behavioral sensitization.
    J Neurosci. 1996 Feb 15;16(4):1550-60 PMID: 8778304
  25. Context-specific cross-sensitization between systemic cocaine and intra-accumbens AMPA infusion in the rat.
    Psychopharmacology (Berl). 1996 Oct;127(4):377-83 PMID: 8923575
  26. The cellular framework for chemical signalling in the nucleus accumbens.
    Prog Brain Res. 1993;99:3-24 PMID: 7906426
  27. Distribution of metabotropic glutamate receptor mGluR5 immunoreactivity in rat brain.
    J Comp Neurol. 1995 May 8;355(3):455-69 PMID: 7636025
  28. Presynaptic mGlu1 type receptors potentiate transmitter output in the rat cortex.
    Eur J Pharmacol. 1998 Apr 24;347(2-3):189-95 PMID: 9653880
  29. Homer proteins regulate coupling of group I metabotropic glutamate receptors to N-type calcium and M-type potassium channels.
    J Neurosci. 2000 Oct 1;20(19):7238-45 PMID: 11007880
  30. Novel members of the Vesl/Homer family of PDZ proteins that bind metabotropic glutamate receptors.
    J Biol Chem. 1998 Sep 11;273(37):23969-75 PMID: 9727012
  31. Metabotropic glutamate receptors: electrophysiological properties and role in plasticity.
    Brain Res Brain Res Rev. 1999 Jan;29(1):83-120 PMID: 9974152
  32. Brain microdialysis of GABA and glutamate: what does it signify?
    Synapse. 1997 Nov;27(3):242-61 PMID: 9329159
  33. Homer binds a novel proline-rich motif and links group 1 metabotropic glutamate receptors with IP3 receptors.
    Neuron. 1998 Oct;21(4):717-26 PMID: 9808459
  34. Time course of extracellular dopamine and behavioral sensitization to cocaine. I. Dopamine axon terminals.
    J Neurosci. 1993 Jan;13(1):266-75 PMID: 8423473
  35. Specificity in the projection patterns of accumbal core and shell in the rat.
    Neuroscience. 1991;41(1):89-125 PMID: 2057066
  36. Homer regulates the association of group 1 metabotropic glutamate receptors with multivalent complexes of homer-related, synaptic proteins.
    Neuron. 1998 Oct;21(4):707-16 PMID: 9808458
  37. Coupling of mGluR/Homer and PSD-95 complexes by the Shank family of postsynaptic density proteins.
    Neuron. 1999 Jul;23(3):583-92 PMID: 10433269
  38. Molecular basis of long-term plasticity underlying addiction.
    Nat Rev Neurosci. 2001 Feb;2(2):119-28 PMID: 11252991
  39. Group I mGlu receptors potentiate synaptosomal [3H]glutamate release independently of exogenously applied arachidonic acid.
    Neuropharmacology. 1999 Apr;38(4):477-85 PMID: 10221751
  40. Shank, a novel family of postsynaptic density proteins that binds to the NMDA receptor/PSD-95/GKAP complex and cortactin.
    Neuron. 1999 Jul;23(3):569-82 PMID: 10433268
  41. Neuroadaptations involved in amphetamine and cocaine addiction.
    Drug Alcohol Depend. 1998 Jun-Jul;51(1-2):141-53 PMID: 9716936
  42. Glutamate transmission in the nucleus accumbens mediates relapse in cocaine addiction.
    J Neurosci. 2000 Aug 1;20(15):RC89 PMID: 10899176
  43. Potentiation of NMDA and AMPA responses by group I mGluR in spinal cord motoneurons.
    Neuropharmacology. 1997 Aug;36(8):1047-55 PMID: 9294969
  44. L-glutamate uptake inhibitors may stimulate phosphoinositide hydrolysis in baby hamster kidney cells expressing mGluR1a via heteroexchange with L-glutamate without direct activation of mGluR1a.
    J Neurochem. 1994 Dec;63(6):2038-47 PMID: 7964721
  45. Metabotropic glutamate receptors in the rat nucleus accumbens contribute to amphetamine-induced locomotion.
    J Pharmacol Exp Ther. 1998 Jan;284(1):317-22 PMID: 9435194
  46. The role of excitatory amino acids in behavioral sensitization to psychomotor stimulants.
    Prog Neurobiol. 1998 Apr;54(6):679-720 PMID: 9560846
  47. Organization of glutamate receptors at the synapse.
    Eur J Neurosci. 1997 Nov;9(11):2219-24 PMID: 9464917
  48. Characterization of multiple phosphorylation sites on the AMPA receptor GluR1 subunit.
    Neuron. 1996 Jun;16(6):1179-88 PMID: 8663994
  49. Intracellular calcium transients and potassium current oscillations evoked by glutamate in cultured rat astrocytes.
    J Neurosci. 1997 Oct 1;17(19):7278-87 PMID: 9295374
  50. Stress preferentially increases extraneuronal levels of excitatory amino acids in the prefrontal cortex: comparison to hippocampus and basal ganglia.
    J Neurochem. 1993 May;60(5):1650-7 PMID: 8097232
  51. Voltage-dependent ion channels in glial cells.
    Glia. 1994 Jun;11(2):156-72 PMID: 7523291
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
1529-2401
Published
2001-11-15
Pages
9043-52
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6762267
Subset
IM
Grants
NIDA NIH HHS · DA-03906 · United States
NIDA NIH HHS · DA-05963-01 · United States
NIDA NIH HHS · DA10309 · United States
NIMH NIH HHS · MH-40817 · United States
External Links
PubMed source PMC Full Text View journal details
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