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PMID: 9412521 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Hypoactivity of the spinal cannabinoid system results in NMDA-dependent hyperalgesia.

Richardson JD, Aanonsen L, Hargreaves KM

Abstract

Cannabinoids, such as Delta9-THC, are capable of inhibiting nociception, i.e., pain transmission, at least in part, by interacting with spinal Gi/Go-coupled cannabinoid receptors. What is not known, however, is the antinociceptive role of endogenous spinal cannabinoids. If endogenous cannabinoids modulate basal nociceptive thresholds, then alterations in this system could be involved in the etiology of certain pain states. In this report we provide evidence for tonic modulation of basal thermal nociceptive thresholds by the spinal cannabinoid system. Administration of oligonucleotides directed against CB1 cannabinoid receptor mRNA significantly reduced spinal cannabinoid binding sites and produced significant hyperalgesia when compared with a randomer oligonucleotide control. A second method used to reduce activity of the spinal cannabinoid receptor was intrathecal administration of the cannabinoid receptor antagonist SR 141716A. SR 141716A evoked thermal hyperalgesia with an ED50 of 0.0012 fmol. The SR 141716A-induced hyperalgesia was dose-dependently blocked by the administration of D-AP-5 or MK-801, two antagonists to the NMDA receptor. These results indicate that there is tonic activation of the spinal cannabinoid system under normal conditions. Furthermore, hypoactivity of the spinal cannabinoid system results in an NMDA-dependent hyperalgesia and thus may participate in the etiology of certain chronic pain states.

MeSH Terms
2-Amino-5-phosphonovalerate/pharmacology Analgesics/pharmacology Animals Cannabinoids/antagonists & inhibitors,metabolism Cyclohexanols/pharmacology Dizocilpine Maleate/pharmacology Excitatory Amino Acid Antagonists/pharmacology Hot Temperature Hyperalgesia/drug therapy,physiopathology Male Mice Nociceptors/drug effects,physiology Pain Measurement Piperidines/pharmacology Pyrazoles/pharmacology Receptors, N-Methyl-D-Aspartate/physiology Rimonabant Spinal Cord/chemistry,drug effects,physiology Tritium
Chemicals
Analgesics Cannabinoids Cyclohexanols Excitatory Amino Acid Antagonists Piperidines Pyrazoles Receptors, N-Methyl-D-Aspartate Tritium Dizocilpine Maleate 2-Amino-5-phosphonovalerate 3-(2-hydroxy-4-(1,1-dimethylheptyl)phenyl)-4-(3-hydroxypropyl)cyclohexanol Rimonabant
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Richardson J D
Department of Pharmacology, University of Minnesota, Minneapolis, Minnesota 55455, USA.
Aanonsen L
Hargreaves K M
References (30)
30 references, click to expand
  1. Suppression of noxious stimulus-evoked expression of Fos protein-like immunoreactivity in rat spinal cord by a selective cannabinoid agonist.
    Neuroscience. 1996 Feb;70(3):791-8 PMID: 10627219
  2. Electrically evoked acetylcholine release from hippocampal slices is inhibited by the cannabinoid receptor agonist, WIN 55212-2, and is potentiated by the cannabinoid antagonist, SR 141716A.
    J Pharmacol Exp Ther. 1996 Jun;277(3):1431-6 PMID: 8667207
  3. Drug efficacy at guanine nucleotide-binding regulatory protein-linked receptors: thermodynamic interpretation of negative antagonism and of receptor activity in the absence of ligand.
    Mol Pharmacol. 1992 Mar;41(3):549-60 PMID: 1312216
  4. Opiate receptor knockout mice define mu receptor roles in endogenous nociceptive responses and morphine-induced analgesia.
    Proc Natl Acad Sci U S A. 1997 Feb 18;94(4):1544-9 PMID: 9037090
  5. Characterization and distribution of binding sites for [3H]-SR 141716A, a selective brain (CB1) cannabinoid receptor antagonist, in rodent brain.
    Life Sci. 1996;58(15):1239-47 PMID: 8614277
  6. Cannabinoid receptor agonists inhibit Ca current in NG108-15 neuroblastoma cells via a pertussis toxin-sensitive mechanism.
    Br J Pharmacol. 1992 Jun;106(2):231-2 PMID: 1327374
  7. Inhibition of neuroblastoma adenylate cyclase by cannabinoid and nantradol compounds.
    Life Sci. 1984 Oct 22;35(17):1803-10 PMID: 6090851
  8. Determination and characterization of a cannabinoid receptor in rat brain.
    Mol Pharmacol. 1988 Nov;34(5):605-13 PMID: 2848184
  9. Improvement of memory in rodents by the selective CB1 cannabinoid receptor antagonist, SR 141716.
    Psychopharmacology (Berl). 1996 Jul;126(2):165-72 PMID: 8856836
  10. Increased transmitter release at excitatory synapses produced by direct activation of adenylate cyclase in rat hippocampal slices.
    J Neurosci. 1994 Jan;14(1):310-7 PMID: 7506766
  11. SR141716A, a potent and selective antagonist of the brain cannabinoid receptor.
    FEBS Lett. 1994 Aug 22;350(2-3):240-4 PMID: 8070571
  12. Antisense oligodeoxynucleotide treatment to the brain cannabinoid receptor inhibits antinociception.
    Neuroreport. 1996 Jan 31;7(2):593-6 PMID: 8730837
  13. Inhibition of exocytotic noradrenaline release by presynaptic cannabinoid CB1 receptors on peripheral sympathetic nerves.
    Br J Pharmacol. 1996 Aug;118(8):2023-8 PMID: 8864538
  14. Comparison of the pharmacology and signal transduction of the human cannabinoid CB1 and CB2 receptors.
    Mol Pharmacol. 1995 Sep;48(3):443-50 PMID: 7565624
  15. The antinociceptive effects of intrathecally administered levonantradol and desacetyllevonantradol in the rat.
    J Clin Pharmacol. 1981 Aug-Sep;21(S1):334S-340S PMID: 6895380
  16. Intrathecal pertussis toxin produces hyperalgesia and allodynia in mice.
    Pain. 1997 Apr;70(2-3):223-8 PMID: 9150297
  17. In vivo characterization of a specific cannabinoid receptor antagonist (SR141716A): inhibition of delta 9-tetrahydrocannabinol-induced responses and apparent agonist activity.
    J Pharmacol Exp Ther. 1996 May;277(2):586-94 PMID: 8627535
  18. Peripheral and spinal mechanisms of nociception.
    Physiol Rev. 1987 Jan;67(1):67-186 PMID: 3543978
  19. Nociceptive action of excitatory amino acids in the mouse: effects of spinally administered opioids, phencyclidine and sigma agonists.
    J Pharmacol Exp Ther. 1987 Oct;243(1):9-19 PMID: 2822907
  20. Cannabinoids inhibit N-type calcium channels in neuroblastoma-glioma cells.
    Proc Natl Acad Sci U S A. 1992 May 1;89(9):3825-9 PMID: 1315042
  21. Glutamate and substance P coexist in primary afferent terminals in the superficial laminae of spinal cord.
    Proc Natl Acad Sci U S A. 1988 Oct;85(20):7820-4 PMID: 2459717
  22. Characterization and localization of cannabinoid receptors in rat brain: a quantitative in vitro autoradiographic study.
    J Neurosci. 1991 Feb;11(2):563-83 PMID: 1992016
  23. Intrathecal morphine in mice: a new technique.
    Eur J Pharmacol. 1980 Oct 17;67(2-3):313-6 PMID: 6893963
  24. The analgesic effects of R(+)-WIN 55,212-2 mesylate, a high affinity cannabinoid agonist, in a rat model of neuropathic pain.
    Neurosci Lett. 1997 Jan 17;221(2-3):157-60 PMID: 9121688
  25. Cannabinoid receptor agonists inhibit glutamatergic synaptic transmission in rat hippocampal cultures.
    J Neurosci. 1996 Jul 15;16(14):4322-34 PMID: 8699243
  26. Activation of inwardly rectifying potassium channels (GIRK1) by co-expressed rat brain cannabinoid receptors in Xenopus oocytes.
    Neurosci Lett. 1995 Feb 17;186(2-3):91-4 PMID: 7777206
  27. Spinal and supraspinal components of cannabinoid-induced antinociception.
    J Pharmacol Exp Ther. 1991 Aug;258(2):517-23 PMID: 1650831
  28. Cannabinoids modulate potassium current in cultured hippocampal neurons.
    Receptors Channels. 1993;1(2):121-34 PMID: 8081716
  29. Characterisation of the rat cerebella CB1 receptor using SR141716A, a central cannabinoid receptor antagonist.
    Neurosci Lett. 1996 Dec 13;220(2):101-4 PMID: 8981483
  30. Inhibition of noxious stimulus-evoked activity of spinal cord dorsal horn neurons by the cannabinoid WIN 55,212-2.
    Life Sci. 1995;56(23-24):2111-8 PMID: 7776839
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
0270-6474
Published
1998-01-01
Pages
451-7
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6793401
Subset
IM
Grants
NIDCR NIH HHS · DE9860 · United States
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