Disruption of the κ-opioid receptor gene in mice enhances sensitivity to chemical visceral pain, impairs pharmacological actions of the selective κ-agonist U-50,488H and attenuates morphine withdrawal

EMBO Journal

Volumn 17, Issue 4, 1998, Pages 886-897

  Simonin, Frédéric ^a   Valverde, Olga ^b   Smadja, Claire ^b   Slowe, Susan ^c   Kitchen, Lan ^c   Dierich, Andrée ^d   Le Meur, Marianne ^d   Roques, Bernard P ^b   Maldonado, Rafael ^b   Kieffer, Brigitte L ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b INSERM   (France)

^c UNIVERSITY OF SURREY   (United Kingdom)

^d Institut de Génétique   (France)

Author keywords

opioid receptor knock out; Nociception; Opioid pharmacology; Spontaneous behaviour

Indexed keywords

3,4 DICHLORO N METHYL N [2 (1 PYRROLIDINYL)CYCLOHEXYL]BENZENEACETAMIDE METHANESULFONATE; ANALGESIC AGENT; GENE PRODUCT; HOT WATER; KAPPA OPIATE RECEPTOR; MORPHINE; OPIATE; OPIATE RECEPTOR;

ABDOMINAL PAIN; ANALGESIC ACTIVITY; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DRUG WITHDRAWAL; GENE DISRUPTION; GENE EXPRESSION; GENE TARGETING; HOT PLATE TEST; INTRAPERITONEAL DRUG ADMINISTRATION; LOCOMOTION; MOOD; MOUSE; NOCICEPTION; NONHUMAN; OPEN FIELD BEHAVIOR; PRIORITY JOURNAL; RECEPTOR BINDING; RECEPTOR GENE; SALIVATION; VISCERAL PAIN; WATER IMMERSION;

3,4-DICHLORO-N-METHYL-N-(2-(1-PYRROLIDINYL)-CYCLOHEXYL)-BENZENEACETAMIDE, (TRANS)-ISOMER; ANIMALS; BEHAVIOR, ANIMAL; ENKEPHALINS; FEMALE; GENE EXPRESSION REGULATION; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MORPHINE; PAIN; PRO-OPIOMELANOCORTIN; PROTEIN PRECURSORS; RECEPTORS, OPIOID, KAPPA; SUBSTANCE WITHDRAWAL SYNDROME; VISCERA;

ANIMALIA;

EID: 0032481350     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/17.4.886     Document Type: Article

References (69)

1. Akil, H., Watson, S.J., Young, E., Lewis, M.E., Khachaturian, H. and Walker, J.J. (1984) Endogenous opioids: biology and function. Annu. Rev. Neurosci., 7, 223-255.
2. Anisman, H. and Kokkinidis, L. (1975) Effects of scopolamine, Damphetamine and other drugs affecting catecholamines on spontaneous alternation and locomotor activity in mice. Psychopharmacology, 45, 55-63.
3. Ashton, N., Balment, R.J. and Blackbum, T.P. (1989) K-Opioid induced changes in renal water and electrolyte management and endocrine secretion. Br. J. Pharmacol., 97, 769-776.
4. Bhargava, H. (1994) Diversity of agents that modify opioid tolerance, physical dependence, abstinence syndrome and self-administrative behaviour. Pharmacol Rev., 46. 293-324.
5. 3H]-CI-977: a highly selective ligand for the K-opioid receptor in both guinea pig and rat forebrain. Mol Neuropharmacol., 1, 23-29.
6. Browstein, M. (1993) A brief history of opiates, opioid peptides and opioid receptors. Proc. Natl Acad. Sci. USA, 90, 5391-5393.
7. Capeccbi, M.R. (1989) Altering the genome by homologous recombination. Science, 244, 1288-1293.
8. Cowan, A., Zhu, X.Z., Mosberg, H.I., Omnaas, J.R. and Porreca, F. (1988) Direct dependence studies in rats with agents selective for different types of opioid receptors. J. Pharmacol. Exp. Then, 246, 950-955.
9. Décimo, D., Labouesse, G. and Dollé, P. (1995) In situ hybridization of nucleic acid probes to cellular RNA. In Hames, B.D. and Higgins, S. (eds). Gene Probes 2: A Practical Approach. Oxford University Press, Oxford, UK, pp. 183-210.
10. Dhawan, B.N., Cesselin, F., Raghubir, R., Reisine, T., Bradley, P.B., Portoghese, P.S. and Hamon, M. (1996) International union of pharmacology. XII. Classification of opioid receptors. Pharmacol. Rev., 48, 567-592.
11. Di Chiara, G. and Imperato, A. (1988) Opposite effects of mu and kappa opiate agonists on dopamine release in the nucleus accumbens and in the dorsal caudate of freely moving rats. J. Pharmacol, Exp. Ther., 244, 1061080.
12. Di Chiara, G. and North, A. (1992) Neurobiology of opiate abuse. Trends Pharmacol. Sci., 13, 185-193.
13. Dickenson, A.H. (1991) Mechanisms of the analgesic action of opiates and opioids. Br. Med. Bull., 47, 690-702.
14. Eddy, N.B. and Leimbach, D. (1953) Synthetic analgesic (II): dithienylbutenyl and dithienylbutylamines. J. Pharmacol. Exp. Ther., 107, 385-396.
15. Funada, M., Suzuki, T., Narita, M., Misiwa, M. and Nagase, H. (1993) Blockade of morphine reward through the activation of K-opioid receptors in mice. Neuropharmacology, 32, 1315-1323.
16. Goldstein, A. and Naidu, A. (1989) Multiple opioid receptors: ligand selectivity profiles and binding site signatures. Mol. Pharmacol., 36, 265-272.
17. Hunskaar, S., Fasmer, O.B. and Hole, K. (1985) Formalin test in mice, a useful technique for evaluating mild analgesics. J. Neurosci. Methods, 14, 69-75.
18. Hunter, J.C., Leighton, G.E., Meecham, K.G., Boyle, S.J., Horwell, D.C., Rees, D.C. and Hughes, J. (1990) CI-977, a novel selective agonist for the kappa opioid receptor. Br. J. Pharmacol., 101, 183-189.
19. Ilien, B., Galzi, J.-L., Mejean, A., Goeldner, M. and Hirth, C. (1988) A μopioid receptor-filter assay. Rapid estimation of binding affinity of ligands and reversibility of long-lasting ligand-receptor complexes. Biochem. Pharmacol., 37, 3843-3851.
20. Khachaturian, H., Lewis, M.E., Schafer, M.K.-H. and Watson, S.J. (1985) Anatomy of the CNS opioid system. Trends Neurosci., 8, 111-119.
21. Kieffer, B.L., Befort, K., Gaveriaux-Ruff, C. and Hirth, C.G. (1992) The δ-opioid receptor: isolation of a cDNA by expression cloning and pharmacological characterization. Proc. Natl Acad. Sci. USA, 89, 12048-12052.
22. Kieffe, B.L. (1995) Recent advances in molecular recognition and signal transduction of active peptides: receptors for opioid peptides. Cell. Mol. Neurobiol., 15, 615-635.
23. Kitchen, I., Leslie, F.M., Borsodi, A., Toth, G., Melchiorri, P. and Negri, L. (1995) Development of δ-opioid receptor subtypes and the regulatory role of weaning: radioligand binding autoradiography and in situ hybridisation studies. J. Pharmacol. Exp. Ther., 275, 1597-1607.
24. Kitchen, I., Slowe, S.J., Matthes, H.W.D. and Kieffer, B.L. (1997) Quantitative autoradio graphic mapping of mu, delta and kappa opioid receptors in knockout mice lacking the mu-opioid receptor gene. Brain Res., 778, 73-78.
25. Konig, M., Zimmer, A.M., Steiner, H., Holmes, P.V., Crawley, J.N., Brownstein, M.J. and Zimmer, A. (1996) Pain responses, anxiety and aggression in mice deficient in pre-proenkephalin. Nature, 383, 535- 538.
26. Koob, G.F. (1992) Drug of abuse: anatomy, pharmacology and function of reward pathways. Trends Pharmacol. Sci., 13, 177-184.
27. Koster, R., Anderson, M. and Debeer, E.J. (1959) Acetic acid for analgesia screening. Fed. Proc., 18, 412.
28. Lahti, R.A., VonVoigtlander, P.F. and Barsuhn, C. (1982) Properties of a selective kappa agonist, U-50,488H. Life Sci., 31, 2257-2260.
29. Locke, K.W. and Holtzman, S.G. (1986) Behavioural effects of opioid peptides selective for mu or delta receptors. II. Locomotor activity in nondependent and morphine dependent rats. J. Pharmacol. Exp. Ther., 238, 997-1003.
30. Lufkin, T., Dierich, A., LeMeur, M., Mark, M. and Chambon, P. (1991) Disruption of the Hox-1.6 homeobox gene results in defects in a region corresponding to its rostral domain of expression. Cell, 88, 1105-1119.
31. Maldonado, R., Negus, S. and Koob, G.F. (1992) Precipitation of morphine withdrawal syndrome in rats by administration of mu-, delta- and kappa-selective opioid antagonists. Neuropharmacology, 31, 1231-1241.
32. Maldonado, R. Blendy, J.A. Tzavara, E., Gass, P., Roques, B.P., Hanoune, J. and Schiütz,G. (1996) Reduction of morphine abstinence in mice with a mutation in the gene encoding CREB. Science, 273, 657-659.
33. Mansour,A. and Watson, S.J. (1993) Anatomical distribution of opioid receptors in mammalian: an overview. In Herz, A. (ed.), Handbook of Experimental Pharmacology, Opioids I. Springer-Verlag, Berlin, Vol. 104/I, pp. 79-105.
34. Mansour, A., Fox, C.A., Akil, H. and Watson, S.J. (1995) Opioid-receptor mRNA expression in the rat CNS: anatomical and functional implications. Trends Neurosci., 18, 22-29.
35. Matthes, H.W.D. et al. (1996) Loss of morphine-induced analgesia, reward effect and withdrawal symptoms in mice lacking the fi-opioid- receptor gene. Nature, 383, 819-823.
36. Millan, M. J. (1990) K-Opioid receptors and analgesia. Trends Pharmacol. Sci., 11, 70-76.
37. Mucha, R.F. and Herz, A. (1985) Motivational properties of kappa and mu opioid receptor agonists studied with place and taste preference conditioning. Psychopharmacology, 86, 274-280.
38. Murray, C.W. and Cowan, A. (1990) [D-Pen2, D-Pen 5]enkephalin, the standard δ-opioid agonist, induces morphine-like behaviour in mice. Psychopharmacology, 102, 425-426.
39. Olson, G.A., Olson, R.D. and Kastin, A.J. (1996). Endogenous opiates: 1995. Peptides, 17, 1421-1466.
40. Pasternak, G.W. (1993) Pharmacological mechanisms of opioid analgesics. Clin. Neuropharmacol., 16, 1-18.
41. Pintar, J.E. and Scott, R.E.M. (1993) Ontogeny of mammalian opioid systems. In Herz, A. (ed.), Handbook of Experimental Pharmacology, Opioids I. Springer-Verlag, Berlin, Vol. 104/I, pp. 711-727.
42. Pfeiffer, A., Brantl, V., Herz, A. and Emrich, M. (1986) Psychomimesis mediated by K opiate receptors. Science, 233, 774-775.
43. Randall, L.O. and Selitto, J.J. (1957) A method for measurement of analgesic activity on inflamed tissue. Arch. Int. Pharmacodyn. Ther., 111, 409-19.
44. Richardson, A., Demoliou-Mason, C. and Barnard, E. (1992) Guanine nucleotide-binding protein-coupled and -uncoupled states of opioid receptors and their relevance to the determination of subtypes. Proc. Natl Acad. Sci. USA, 89, 10198-10202.
45. Robson, L.E., Gillan, M.G.C. and Kosterlitz, H.W. (1985) Species differences in the concentrations and distributions of opioid binding sites. Eur. J. Pharmacol., 112, 65-71.
46. Roques, B.R, Noble, F., Dauge, V., Fournie-Zaluski, M.C. and Beaumont, A. (1993) Neutral endopeptidase 24.11. Structure, inhibition, and experimental and clinical pharmacology. Pharmacol. Rev., 45, 87-146.
47. Rossier, J. (1982). Opioid peptides have found their roots. Nature, 298, 221.
48. Rothman, R.B., Holaday, J.W. and Porreca, F. (1993) Allosteric coupling among opioid receptors: evidence for an opioid receptor complex. In Herz, A. (ed.), Handbook of Experimental Pharmacology, Opioids I. Springer-Verlag, Berlin, Vol. 104/I, pp. 217-237.
49. Rubinstein, M., Mogil, J.S., Japón, M., Chan, E.C., Allen, R.G. and 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, 3995-1000.
50. Schmauss, C., Yaksh, T.L., Shimohigashi, Y., Harty, G., Jensen, T. and Rodbard, D. (1983) Differential association of spinal mu, delta and kappa opioid receptors with subcutaneous, thermal and visceral chemical nociceptive stimuli in the rat. Life Sci., 33 Supp 1, 653-656.
51. Schug, S.A., Zech, D. and Grond, S. (1992) Adverse effects of systemic opioid analgesics. Drug Safety, 7, 200-213.
52. Shippenberg, T.S., Bals-Kubik, R. and Herz, A. (1987) Motivational properties of opioids: evidence that an activation of δ-receptors mediates reinforcement processes. Brain Res., 436, 234-239.
53. 3H]U-69,593. Adv. Biosci., 75, 49-52.
54. Sora, I., Takahashi, N., Funada, M., Ujike, H., Revay, R.S., Donovan, D.M., Miner, L.L. and Uhl, G.R. (1997) Opiate receptor knockout mice define μ receptor roles in endogenous nociceptive responses and morphineinduced analgesia. Proc. Natl Acad. Sci. USA, 94, 1544-1549.
55. Spanagel, R., Herz, A. and Shippenberg, T.S. (1992) Opposing tonically active endogenous opioid systems modulate the mesolimbic dopaminergic pathway. Proc. Natl Acad. Sci. USA, 89, 2046-2050.
56. Takemori, A.E. and Portoghese, P.S. (1987) Evidence for the interaction of morphine with K- and δ-opioid receptors to induce analgesia in βfunaltrexamine-treated mice. J. Phannacol. Exp. Ther., 243, 91-94.
57. Tao, P.L., Hwang, C.L. and Chen, C.Y. (1994) U-50,488H blocks the development of morphine tolerance and dependence at very low doses in guinea pigs. Eur. J. Pharmacol, 256, 281-286.
58. Tian, M. et al. (1997) Altered hematopoiesis, behaviour, and sexual function in μ opioid receptor-deficient mice. J. Exp. Med., 185, 1517-1522.
59. Tortella, F.C., Echevarria, E., Lipkowski, A.W., Takemori, A.E., Ponoghese, P.S. and Holaday, J.W. (1989) Selective kappa antagonist properties of nor-binaltorphimine in the rat MES seizure model. Life Sci., 44, 661-665
60. Traynor, J. (1989) Subtypes of the K-opioid receptor: fact or fiction? Trends Pharmacol. Sci., 10, 52-53.
61. Tyers,M.B. (1980) A classification of opiate receptors that mediate antinociception in animals. Br. J. Pharmacol., 69, 503-512
62. 2 opioid receptors in rat and guinea pig brain. Brain Res., 562, 52-65.
63. Valverde, O., Fournier-Zaluski, M.-C., Roques, B.P. and Maldonado, R. (1996) The CCK-B antagonist PD-134,308 facilitates rewarding effects of endogenous enkephalins but does not induce place preference in rats. Psychopharmacology, 123, 119-126.
64. Valverde, O., Maldonado, R. and Kieffer, B.L. (1997) Recent findings on the mechanism of action of morphine. CNS Drug, in press.
65. Vonvoigtlander, P.F., Lahti, R.A. and Ludens, J.H. (1983) U-50, 488: a selective and structurally novel non-mu (kappa) opioid agonist. J. Pharmacol. Exp. Ther., 224, 7-12.
66. Waksman, G., Hamel, E., Fournie-Zaluski, M.C. and Roques, B.P. (1986) Comparative distribution of the neutral endopeptidase 'enkephalinase' and mu and delta opioid receptors in rat brain by autoradiography. Proc. Natl Acad. Sci. USA, 83, 1523-1527.
67. Wards, S.J. and Takemori, A.E. (1983) Relative involvement of mu, kappa and delta receptor mechanisms in opiate-mediated antinociception in mice. J. Pharmacol. Exp. Ther., 224, 525-530.
68. Zadina, J.E., Hackler, L., Ge, L.-J. and Kastin, A.J. (1997) A potent and selective endogenous agonist for the fi-opiate receptor. Nature, 386, 499-502.
69. Zhu, Y., King, M., Schuller, A., Unterwald, E., Pasternak, G. and Pintar, J.E. (1997) Genetic disruption of the mouse delta opioid gene. In Soc. Neurosci. Abstr. Society for Neuroscience, Washington D.C. 20036, vol. 23, part 1, pp. 584.