Reduction of stress-induced analgesia but not of exogenous opioid effects in mice lacking CB1 receptors

European Journal of Neuroscience

Volumn 12, Issue 2, 2000, Pages 533-539

  Valverde, Olga ^a,c   Ledent, Catherine ^b   Beslot, Francoise ^a   Parmentier, Marc ^b   Roques, Bernard P ^a  

^a CNRS   (France)

^b UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^c UNIVERSITAT POMPEU FABRA   (Spain)

Author keywords

Cannabinoids; CB1 receptors; Conditioned suppression of motility; Opioid analgesia; Stress

Indexed keywords

3,4 DICHLORO N METHYL N [2 (1 PYRROLIDINYL)CYCLOHEXYL]BENZENEACETAMIDE METHANESULFONATE; CANNABINOID; CANNABINOID RECEPTOR; DELTA OPIATE RECEPTOR AGONIST; DELTORPHIN; ENKEPHALIN DERIVATIVE; KAPPA OPIATE RECEPTOR AGONIST; MORPHINE; MU OPIATE RECEPTOR AGONIST; OPIATE; OPIATE RECEPTOR;

ANALGESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINOCICEPTION; ARTICLE; CONTROLLED STUDY; ELECTRIC SHOCK; FORCED SWIMMING TEST; HOT PLATE TEST; MECHANICAL STIMULATION; MOUSE; MUTANT; NONHUMAN; PAIN; PRIORITY JOURNAL; STRESS; THERMAL STIMULATION; VISCERA; WATER TEMPERATURE;

3,4-DICHLORO-N-METHYL-N-(2-(1-PYRROLIDINYL)-CYCLOHEXYL)-BENZENEACETAMIDE, (TRANS)-ISOMER; ANALGESICS, OPIOID; ANIMALS; DOPAMINE; ELECTROSHOCK; ENKEPHALIN, D-PENICILLAMINE (2,5)-; ENKEPHALINS; EXPLORATORY BEHAVIOR; FOOT; HABITUATION, PSYCHOPHYSIOLOGIC; HEAT; MICE; MICE, KNOCKOUT; MODELS, NEUROLOGICAL; MORPHINE; MOTOR ACTIVITY; NOCICEPTORS; OLIGOPEPTIDES; PAIN; PAIN THRESHOLD; RECEPTORS, CANNABINOID; RECEPTORS, DRUG; RECEPTORS, OPIOID; RECEPTORS, OPIOID, DELTA; RECEPTORS, OPIOID, KAPPA; RECEPTORS, OPIOID, MU; STRESS; STRESS, MECHANICAL; SWIMMING; TAIL; VISCERA;

EID: 0034095022     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1460-9568.2000.00929.x     Document Type: Article

References (45)

1. Aceto, M.D., Scates, S.M., Lowe, J. & Martin, B.R. (1996) Dependence on A9-tetrahydrocannabinol: studies on precipitated and abrupt withdrawal. J. Pharmacol. Exp. Ther., 278, 1290-1295.
2. Adams, I.B. & Martin, B.R. (1996) Cannabis: pharmacology and toxicology in animals and humans. Addiction, 91, 1585-1614.
3. Akil, H. & Mayer, D.J. (1972) Antagonism of stimulation produced analgesia by p-CPA, a serotonin synthesis inhibitor. Brain Res., 44, 692-697.
4. Anderson, P.F., Jackson, D.M., Chesher, G.B. & Malor, R. (1975) Tolerance to the effects of Δ9-tetrahydrocannabinol in mice on intestinal motility, temperature and locomotor activity. Psychopharmacology., 48, 31-36.
5. 1 receptor stimulation. Eur. J. Pharmacol., 216, 157-166.
6. Burstein, S., Budrow, J., Debatis, M., Hunter, S.A. & Subramanian, A. (1994) Phospholipase participation in cannabinoid-induced release of free arachidonic acid. Biochem. Pharmacol., 48, 1253-1264.
7. Calignano, A., La Rana, G., Giuffrida, A. & Piomelli, D. (1998) Control of pain initiation by endogenous cannabinoids. Nature, 394, 277-281.
8. Chen, J., Paredes, W., Li, J., Smith, D., Lowinson, J. & Gardner, E.L. (1991) Δ9-tetrahydrocannabinol produces naloxone-blockable enhancement of presynaptic basal dopamine efflux in nucleus accumbens of conscious, freely-moving rats as measured by intracerebral microdialysis. Psycopharmacology., 102, 156-162.
9. Childers, S.R., Pacheco, M.A., Bennet, M.A., Edwards, T.A., Hampson, R.E., Mu, J. & Deadwyler, S.A. (1993) Cannabinoid receptors: G-protein-mediated signal transduction mechanisms. Biochem. Soc. Symp., 59, 27-50.
10. Corchero, J., Avila, M.A., Fuentes, J.A. & Manzanares, J. (1997a) Δ9-tetrahydrocannabinol increases prodynorphin and proenkephalin gene expression in the spinal cord of the rat. Life Sci., 61, 39-4-3.
11. Corchero, J., Fuentes, J.A. & Manzanares, J. (1997b) Δ9-Tetrahydrocannabinol increases proopiomelanocortin gene expression in the arcuate nucleus of the rat hypothalamus. Eur. J. Pharmacol., 323, 193-195.
12. De Felipe, C., Herrero, J.F., O'Brien, J.A., Palmer, J.A., Doyle, C.A., Smith, A.J.H., Laird, J.M.A., Belmonte, C., Cervero, F. & Hunt, S.P. (1998) Altered nociception, analgesia and aggression in mice lacking the receptor for substance P. Nature, 392, 394-397.
13. Devane, W.A., Dysarz, F.A., Johnson, M.R., Melvin, L.S. & Howlett, A.C. (1988) Determination and characterization of a cannabinoid receptor in rat brain. Mol. Pharmacol., 34, 605-613.
14. Dewey, W.L., Harris, L.S., Howes, J.F. & Nuite, J.A. (1970) The effect of various neurohumoral modulators on the activity of morphine and the narcotic antagonists in the tail-flick and phenylquinone test. J. Pharmacol. Exp. Ther., 175, 435-442.
15. Dewey, W.L. (1986) Cannabinoid pharmacology. Pharmacology, 38, 151-178.
16. French, E.D. (1997) Δ9-Tetrahydrocannabinol excites rat VTA dopamine neurons through activation of cannabinoid CBI but not opioid receptors. Neurosci. Lett., 226, 159-162.
17. Hutcheson, D.M., Tzavara, E.Th., Smadja, C., Valjent, E., Roques, B.P., Hanoune, J. & Maldonado, R. (1998) Behavioural and biochemical evidence for signs of abstinence in mice chronically treated with Δ9-tetrahydrocannabinol. Br. J. Pharmacol., 125, 1567-1577.
18. Kameyama, T. & Nagasaka, M. (1982) Effects of apomorphine and diazepan in a quickly conditioned suppression in rats. Pharmacol. Biochem. Behav., 17, 59-63.
19. König, M., Zimmer, A.M., Steiner, H., Holmes, P.V., Crawley, J.N., Browstein, M.J. & Zimmer, A. (1996) Pain responses, anxiety and aggression in deficient mice in pre-proenkephalin. Nature, 383, 535-538.
20. Koster, R., Anderson, M. & Deeber, E.J. (1959) Acetic acid for analgesia screening. Fed. Proc., 18, 412.
21. Kozel, N.J. & Adams, E.H. (1986) Epidemology of drug abuse: an overview. Science, 234, 970-974.
22. 1, receptor knockout mice. Science, 283, 401-404.
23. Lichtman, A.H. & Martin, B.R. (1991) Spinal and supraspinal components of cannabinoid-induced antinociception. J. Pharmacol. Exp. Ther., 258, 517-523.
24. Mailleux, P. & Vanderhaeghen, J.J. (1994) Δ9-Tetrahydrocannabinol regulates substance P and enkephalin mRNAs levels in the caudate-putamen. Eur. J. Pharmacol., 266, 193-196.
25. Marek, P., Mogil, J.S., Sternberg, W.F., Panocka, I. & Lieberskind, J.C. (1992) N-methyl D-aspartic acid (NMDA) receptor antagonist MK-801 blocks non-opioid stress-induced analgesia. II Comparison across three swim-stress paradigms in selectively bred mice. Brain Res., 578, 197-202.
26. Matsuda, L.A., Lolait, S.J., Brownstein, M.J., Young, A.C. & Bonner, T.I. (1990) Structure of a cannabinoid receptor and functional expression of the cloned cDNA. Nature, 346, 561-564.
27. Matthes, H.W.D., Smadja, C., Valverde, O., Vonesch, J.L., Foutz, A.S., Boudinot, E., Denavit-Saubié, M., Severini, C., Negri, L., Roques, B.P., Maldonado, R. & Kieffer, B.L. (1998) Activity of the delta-opioid receptor is partially reduced, whereas activity of the kappa receptor is maintained in mice lacking the mu receptor. J. Neurosci., 18, 7285-7295.
28. 1 receptors in Δ9-tetrahydrocannabinol-induced expression of Fos protein in the rat brain. Brain Res., 710, 234-240.
29. Munro, S., Thomas, K.L. & Abu-Shaar, M. (1993) Molecular characterization of a peripheral receptor for cannabinoids. Nature, 365, 61-65.
30. Navarro, M., Chowen, J., Carrera, R.A., del Arco, I., Villanua, M.A., Martin, Y., Roberts, A.J., Koob, G.F. & Rodríguez de Fonseca, F.R. (1998) CB1 cannabinoid receptor antagonist-induced opiate withdrawal in morphine-dependent rats. Neuroreport, 9, 3397-3402.
31. Randall, L.O. & Selitto, J.J. (1957) A method for measurement of analgesic activity on inflamed tissue. Arch. Int. Pharmacodyn. Ther., 111, 409-419.
32. 9-tetrahydrocannabinol-induced analgesia in mice. Eur. J. Pharmacol., 301, 75-81.
33. Rodríguez de Fonseca, F., Carrera, M.R.A., Navarro, M., Koob, G.F. & Weiss, F. (1997) Activation of corticotropin-releasing factor in the limbic system during cannabinoid withdrawal. Science, 276, 2050-2054.
34. Rodríguez de Fonseca, F., Del Arco, I., Martín-Calderón, J.L., Gorriti, M.A. & Navarro, M. (1998) Role of the endogenous cannabinoid system in the regulation of motor activity. Neurobiol. Dis., 5, 483-501.
35. Roques, B.P., Noble, F., Daugé, V., Fournié-Zaluski, M.-C. & Beaumont, A. (1993) Neutral endopeptidase 24.11: structure, inhibition and experimental and clinical pharmacology. Pharmacol. Rev., 45, 87-146.
36. Rubinstein, M., Mogil, J.S., Japón, M., Chan, E.C., Allen, R.G. & Low, M.J. (1996) Absence of opioid stress-induced analgesia in mice lacking β-endorphin by site-directed mutagenesis. Proc. Natl Acad. Sci. USA, 93, 3995-4000.
37. 3H]diprenorphine binding. Brain Res., 571, 306-312.
38. Shippenberg, T.S., Bals-Kubik, R., Spanagel, R. & Herz, A. (1989) Reinforced and aversive effects of opioid agonist: involvement of the mesolimbic dopamine system. Behav. Pharmacol., 1, 18-27.
39. Simonin, F., Valverde, O., Smadja, C., Slowe, S., Kitchen, I., Dierich, A., LeMeur, M., Roques, B.P., Maldonado, R. & Kieffer, B.L. (1998) Disruption of the kappa-opioid receptor in gene in mice enhances sensitivity to chemical visceral pain, impairs pharmacological actions of the selective kappa-agonist U-50,488H and attenuates morphine withdrawal. EMBO J., 17, 886-897.
40. Stinus, L., Koob, G.F., Ling, N., Bloom, F.E. & Le Moal, M. (1980) Locomotor activation induced by infusion of endorphins into the ventral tegmental area: evidence for opiate-dopamine interactions. Proc. Natl Acad. Sci. USA, 77, 2323-2328.
41. Tanda, G., Pontieri, F.E. & Di Chiara, G. (1997) Cannabinoid and heroin activation of mesolimbic dopamine transmission by a common mu 1 opioid receptor mechanism. Science, 276, 2048-2050.
42. Thorat, S.N. & Bargava, H.N. (1994) Evidence for a bidirectional cross-tolerance between morphine and Δ9-tetrahydrocannabinol in mice. Eur. J. Pharmacol., 260, 5-13.
43. Welch, S.P. & Stevens, D.L. (1992) Antinociceptive activity of intrathecally administered cannabinoids alone, and in combination with morphine, in mice. J. Pharmacol Exp. Ther., 262, 10-18.
44. Welch, S.P. (1993) Blockade of cannabinoid-induced antinociception by norbinaltorphimine, but not N,N-diallyl-tyrosine-aib-phenylalanine-leucine, ICI 174,864 in mice. J. Pharmacol. Exp. Ther., 256, 633-640.
45. Zimmer, A., Zimmer, A.M., Hohmann, A.C., Herkenham, M. & Bonner, T.I. (1999) Increased mortality, and hypoalgesia in cannabinoid CB1 receptor knockout mice. Proc. Natl Acad. Sci. USA, 96, 5780-5785.