Antinociceptive effects of RB101, a complete inhibitor of enkephalin- catabolizing enzymes, are enhanced by a cholecystokinin type B receptor antagonist, as revealed by noxiously evoked spinal c-Fos expression in rats

Journal of Pharmacology and Experimental Therapeutics

Volumn 281, Issue 1, 1997, Pages 208-217

  Honoré, Prisca ^a,c   Buritova, Jaroslava ^a   Fournié Zaluski, Marie Claude ^b   Roques, Bernard P ^b   Besson, Jean Marie ^a  

^a PSL RESEARCH UNIVERSITY   (France)

^b Laboratoire de Pharmacochimie   (France)

^c INSERM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

4 [[2 [2 [[(2 ADAMANTYLOXY)CARBONYL]AMINO] 3 (1H INDOL 3 YL) 2 METHYLPROPIONAMIDO] 1 PHENYLETHYL]AMINO] 4 OXOBUTYRIC ACID MEGLUMINE; CHOLECYSTOKININ RECEPTOR BLOCKING AGENT; DEVAZEPIDE; N [3 [(2 AMINO 4 METHYLTHIO)BUTYLDITHIO] 2 BENZYLPROPIONYL]PHENYLALANINE BENZYL ESTER;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTINOCICEPTION; ARTICLE; CONTROLLED STUDY; DRUG EFFECT; DRUG POTENTIATION; MALE; NONHUMAN; ONCOGENE C FOS; PAIN; PRIORITY JOURNAL; RAT; SUBCUTANEOUS DRUG ADMINISTRATION;

EID: 0030973073     PISSN: 00223565     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (81)

1. ABBADIE, C. AND BESSON, J.-M.: Effects of morphine and naloxone on basal and evoked Fos-like immunoreactivity in lumbar spinal cord neurons of arthritic rats. Pain 52: 29-39, 1993.
2. ABBADIE, C., HONORÉ, P. AND BESSON, J.-M.: Postsynaptic changes during sustained primary afferent fiber stimulation as revealed by c-Fos immunohistochemistry in the rat spinal cord. In The Cellular Mechanisms of Sensory Processing, ed. by L. Urban, A. Dray, S. Jeftinija, P. Reeh and C. J. Woolf, pp. 449-471, Laszlo Urban, Berlin, 1994a.
3. ABBADIE, C., HONORÉ, P. AND BESSON, J.-M.: Intense cold noxious stimulation of the rat hindpaw induces C-fos expression in lumbar spinal cord neurons. Neuroscience 59: 457-468, 1994b.
4. ABBADIE, C., HONORÉ, P., FOURNIÉ-ZALUSKI, M. C., ROQUES, B. P. AND BESSON, J.-M.: Effects of opioids and non-opioids on c-Fos immunoreactivity induced in rat lumbar spinal cord neurons by noxious heat stimulation. Eur. J. Pharmacol. 258: 215-227, 1994c.
5. BABER, N. S., DOURISH, C. T. AND HILL, D. R.: The role of CCK, caerulein, and CCK antagonists in nociception. Pain 39: 307-328, 1989.
6. BASBAUM, A. I. AND BESSON, J.-M.: Towards a New Pharmacotherapy of Pain, John Wiley & Sons, Chichester, UK, 1991.
7. BESSE, D., LOMBARD, M.-C., ZAJAC, J. M., ROQUES, B. P. AND BESSON, J.-M.: Autoradiographic distribution of μ, δ and κ opioid binding sites in the superficial dorsal horn, over the rostrocaudal axis of the rat spinal cord. Brain Res. 548: 287-291, 1991.
8. BESSON, J.-M. AND CHAOUCH, A.: Peripheral and spinal mechanisms of nociception. Physiol. Rev. 67: 67-186, 1987.
9. CHAPMAN, V., HONORÉ, P., BURITOVA, J. AND BESSON, J.-M.: Cholecystokinin B receptor antagonism enhances the ability of a low dose of morphine to reduce c-Fos expression in the spinal cord of the rat. Neuroscience 67: 731-739, 1995.
10. DICKENSON, A. H., SULLIVAN, A. F., FOURNIÉ-ZALUSKI, M. C. AND ROQUES, B. P.: Prevention of degradation of endogenous enkephalins produces inhibition of nociceptive neurons in rat spinal cord. Brain Res. 408: 185-191, 1987.
11. DOURISH, C. T., HAWLEY, D. AND IVERSEN, S. D.: Enhancement of morphine and prevention of morphine tolerance in the rat by cholecystokinin antagonist L-364,718. Eur. J. Pharmacol. 147: 469-472, 1988.
12. DOURISH, C. T., O'NEILL, M. F., COUGHLAN, J., KITCHENER, S. J., HAWLEY, D. AND IVERSEN, S. D.: The selective CCK-B receptor antagonist L-365.260 enhances morphine analgesia and prevents morphine tolerance in the rat. Eur. J. Pharmacol. 176: 35-44, 1990.
13. DRAISCI, G. AND IADAROLA, M. J.: Temporal analysis of increases in c-fos, preprodynorphin and preprotnkephalin mRNAs in rat spinal cord. Mol. Brain Res. 6: 31-37, 1989.
14. FARIS, P. L., KOMISARUK, B. R., WATKINS, L. R. AND MAYER, D. J.: Evidence for the neuropeptide cholecystokinin as an antagonist of opiate analgesia. Science (Wash. DC) 219: 310-312, 1983.
15. FOURNIÉ-ZALUSKI, M. C., CHAILLET, P., BOUBOUTOU, R., COULAUD, A., CHEROT, P., WAKSMAN, G., COSTENTIN, J. AND ROQUES, B. P.: Analgesic effects of kelatorphan, a new highly potent inhibitor of multiple enkephalin degrading enzymes. Eur. J. Pharmacol. 102: 525-528, 1984.
16. FOURNIÉ-ZALUSKI, M. O., CORIC, P., TURCAUD, S., LUCAS, E., NOBLE, F., MALDONADO, R. AND ROQUES, B. P.: Mixed-inhibitor-prodrug as a new approach towards systemically active inhibitors of enkephalin degrading enzymes. J. Med. Chem. 35: 2473-2481, 1992.
17. FOURNIÉ-ZALUSKI, M. C., COULAUD, A., BOUBOUTOU, R., CHAILLET, P., DEVIN, J., WAKSMAN, G., COSTENTIN, J. AND ROQUES, B. P.: New bidentates as full inhibitors of enkephalin-degrading enzymes: Synthesis and analgesic properties. J. Med. Chem. 28: 1158-1169, 1985.
18. GALL, C., LAUTERBORN, J., BURKS, D. AND SEROGY, K.: Co-localization of enkephalins and cholecystokinin in discrete areas of rat brain. Brain Res. 403: 403-408, 1987.
19. GHILARDI, J. R., ALLEN, C. J., VIGNA, S. R., MCVEY, D. C. AND MANTHY, P. W.: Trigeminal and dorsal root ganglion neurons express CCK receptor binding sites in the rat, rabbit and monkey: Possible site of opiate-CCK analgesia interactions. J. Neurosci. 12: 4854-4866, 1992.
20. GOGAS, K. R., PRESLEY, R. W., LEVINE, J. D. AND BASBAUM, A. I.: The antinociceptive action of supraspinal opioids results from an increase in descending inhibitory control: Correlation of nociceptive behavior and c-fos expression. Neuroscience 42: 617-628, 1991.
21. HAMMOND, D. L., PRESLEY, R. W., GOGAS, K. R. AND BASBAUM, A. I.: Morphine or U-50,488 suppresses Fos protein-like immunoreactivity in the spinal cord and nucleus tractus solitarii evokvd by a noxious visceral stimulus in the rat. J. Comp. Neurol. 315: 244-253, 1992.
22. HARGREAVES, K., DUBNER, R., BROWN, P., FLORES, C. AND JORIS, J.: A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain 32: 77-88, 1988.
23. HERDBGEN, T., KOVARY, K., LEAH, J. AND BRAVO, R.: Specific temporal and spatial distribution of JUN, FOS and KROX-24 proteins in spinal neurons following noxious transsynaptic stimulation. J. Comp. Neurol. 313: 178-191, 1991.
24. HILL, D. R. AND WOODRUFF, G. N.: Differentiation of central cholecystokinin receptor binding sites using the non peptide antagonists MK-329 and L-365,260. Brain Res. 526: 276-283, 1990.
25. HONORÉ, P., BURITOVA, J. AND BESSON, J.-M.: Carrageenin-evoked c-Fos expression in rat lumbar spinal cord: The effects of indomethacin. Eur. J. Pharmacol. 272: 249-259, 1995a.
26. HONORÉ P., BURITOVA, J., FOURNIÉ-ZALUSKI, M. C., ROQUES, B. P. AND BESSON, J.-M.: The effects of RB101, a full inhibitor of enkephalin-catabolizing enzymes, on carrageenin induced spinal c-Fos expression are enhanced by a CCK-B receptor antagonist (CI988). In Proceedings of the International Association for the Study of Pain, 8th World Congress on Pain, Vancouver, Canada, 1996.
27. HONORÉ, P., CHAPMAN, V., BURITOVA, J. AND BESSON, J.-M.: When is the maximal effect of pre-administered systemic morphine on carrageenin evoked spinal c-Fos expression in the rat? Brain Res. 705: 91-96, 1995b.
28. HSU, S., RAINE, L. AND FANGER, H.: Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: A comparison between ABC and unlabelled antibody (PAP) procedures. J. Histochem. Cytochem. 29: 577-580, 1981.
29. HUGHES, J., BODEN, P., COSTALL, B., DOMENEY, A., KELLY, E., HORWELL, D. C., HUNTER, J. C., PINNOCK, R. D. AND WOODRUFF, G. N.: Development of a class of selective cholecystokinin type B receptor antagonists having potent anxiolytic activity. Proc. Natl. Acad. Sci. U.S.A. 87: 6728-6732, 1990.
30. IADAROLA, M. J., BRADY, L. S., DRAISCI, G. AND DUBNER, R.: Enhancement of dynorphin gene expression in spinal cord following experimental inflammation: Stimulus specificity, behavioral parameters and opioid receptor binding. Pain 35: 313-326, 1988.
31. JASMIN, L., WANG, H., TARCY-HORNOCH, K., LEVINE, J. D. AND BASBAUM, A. I.: Differential effects of morphine on noxious stimulus-evoked Fos-like immunoreactivity in subpopulation of spinoparabrachial neurons. J. Neurosci. 14: 7252-7260, 1994.
32. JORIS, J., COSTELLO, A., DUBNER, R. AND HARGREAVES, K.: Opiates suppress carrageenan-induced edema and hyperthermia at doses that inhibit hyperalgesia. Pain 43: 95-103, 1990.
33. KAYSER, V., FOURNIÉ-ZALUSKI, M. C., GUILBAUD, G. AND ROQUES, B. P.: Potent antinociceptive effects of kelaturphan (a highly efficient inhibitor of multiple enkephalin-degrading enzymes) systemically administered in normal and arthritic rats. Brain Res. 497: 94-101, 1989.
34. KAYSER, V. AND GUILBAUD, G.: Local and remote modifications of nociceptive sensitivity during carrageenin-induced inflammation in the rat. Pain 28: 99-107, 1987.
35. KELLSTEIN, D. E. AND MAYER, D. J.: Chronic administration of cholecystokinin antagonists reverses the enhancement of spinal morphine analgesia induced by acute pretreatment. Brain Res. 516: 263-270, 1990.
36. KOPIN, A. S., LEE, Y.-M., MCBRIDE, E. W., MILLER, L. J., LU, M., LIN, H. Y., KOLAKOWSKI, L. F., JR. AND BEINBORN, M.: Expression cloning and characterization of the canine parietal cell gastrin receptor. Proc. Natl. Acad. Sci. U.S.A. 89: 3605-3609, 1992.
37. LOMBARD, M.-C., BESSE, D. AND BESSON, J.-M.: Opioid receptors in the superficial layers of the rat spinal cord: Functional implications in pain processing. In Neuropeptides in the Spinal Cord, ed. by F. Nyberg, H. S. Sharma and Z. Wiesonfeld-Hallin, pp. 77-92, Elsevier Science, New York, 1995.
38. 2 with μ and δ opioid antinociception in the rat spinal cord. Neuropeptides 16: 213-218, 1990.
39. MALDONADO, R., DERRIEN, M., NOBLE, F. AND ROQUES, B. P.: Association of the peptidase inhibitor RB101 and a CCK-B antagonist strongly enhances antinociceptive responses. Neuroreport 4: 947-950, 1993.
40. MALDONADO, R., VALVERDE, O., TURCAUD, S., FOURNIÉ-ZALUSKI, M. C. AND ROQUES, B. P.: Antinociceptive response induced by mixed inhibitors of enkephalin catabolism in peripheral inflammation. Pain 58: 77-83, 1994.
41. MOLANDER, C., XU, Q. AND GRANT, G.: The cytoarchitectonic organization of the spinal cord in the rat. I. The lower thoracic and lumbosacral cord. J. Comp. Neurol. 230: 133-141, 1984.
42. MORAN, T. H., ROBINSON, P. H., GOLDRICH, M. S. AND MCHUGH, P. R.: Two brain cholecystokinin receptors: Implication for behavioral actions. Brain Res. 362: 175-179, 1986.
43. MORGAN, J. I.: Discussions in Neuroscience: Proto-oncogene Expression in the Nervous System, Elsevier, Amsterdam, 1991.
44. MORGAN, J. I. AND CURRAN, T.: Immediate-early genes: Ten years on. Trends Neurosci. 18: 66-67, 1995.
45. 5)enkephalin in the substantia gelatinosa of the cat spinal cord. Eur. J. Pharmacol. 140: 195-201, 1987.
46. B receptor antagonist potentiates μ-, but not δ-opioid receptor-mediated antinociception in the formalin test. Eur. J. Pharmacol. 273: 145-151, 1995.
47. NOBLE, F., DERRIEN, M. AND ROQUES, B. P.: Modulation of opioid antinociception by CCK at the supraspinal level: Evidence of regulatory mechanisms between CCK and enkephalin systems in the control of pain. Br. J. Pharmacol. 109: 1064-1070, 1993.
48. NOBLE, F. AND ROQUES, B. P.: Assessment of endogenous enkephalin efficacy in the hot plate in mice: Comparative study with morphine. Neurosci. Lett. 185: 75-78, 1995.
49. NOBLE, F., SOLEIHAC, J. M., SOROCAS-LUCAS, E., TURCAUD, S., FOURNIÉ-ZALUSKI, M. C. AND ROQUES, B. P.: Inhibition of the enkephalin-metabolizing enzymes by the first systemically active mixed inhibitor prodrug RB 101 induces potent analgesic responses in mice and rats. J. Pharmacol. Exp. Ther. 261: 181-190, 1992.
50. NOGUCHI, K., DUBNER, R. AND RUDA, M. A.: Preproenkephalin mRNA in spinal dorsal horn neurons is induced by peripheral inflammation and is co-localised with Fos and Fos-related proteins. Neuroscience 46: 561-570, 1992.
51. NOGUCHI, K., KOWALSKI, K., TRAUB, B. R., SOLODKIN, A., IADAROLA, M. J. AND RUDA, M. A.: Dynorphin expression and Fos-like immunoreactivity following inflammation induced hyperalgeaia are colocalized in spinal cord neurons. Mol. Brain Res. 10: 227-233, 1991.
52. NOZAKI, K., MOSKOWITZ, A. AND BOCCALINI, P.: CP-93,129, sumatriptan, and dihydroergotamine block c-fos expression within rat trigeminal nucleus caudalis caused by chemical stimulation of the meninges. Br. J. Pharmacol. 106: 409-415, 1992.
53. B antagonist in the rat. Neurosci. Lett. 181: 9-12, 1994.
54. PELAPRAT, D., PESCHANSKI, M., BROER, Y., BESSON, J.-M. AND ROQUES, B. P.: Postsynaptic receptors for cholecystokinin in the thalamic reticular nucleus: A possible modulatory system for sensory transmission. Neurosci. Lett. 80: 16-20, 1987.
55. PERROT, S., KAYSER, V., FOURNIÉ-ZALUSKI, M. C., ROQUES, B. P. AND GUILBAUD, G. Antinociceptive properties of PC 12, a systemically active mixed inhibitor of enkephalin degrading enzymes in normal and arthritic rats. Eur. J. Pharmacol. 241: 129-133, 1993.
56. PRESLEY, R. W., MENETREY, D., LEVINE, J. D. AND BASBAUM, A. I.: Systemic morphine suppresses noxious stimulus-evoked Fos protein-like immunoreactivity in the rat spinal cord. J. Neurosci. 10: 323-335, 1990.
57. PU, S.-F., ZHUANG, H.-X. AND HAN, J.-S.: Cholecystokinin octapeptido (CCK-8) antagonizes morphine analgesia in nucleus accumbens of the rat via the CCK-B receptor. Brain Res. 657: 159-164, 1994.
58. ROQUES, B. P., NOBLE, F., DAUGER, V., FOURNIÉ-ZALUSKI, M. C. AND BEAUMONT, A.: Neutral endopeptidase 24.11: Structure, inhibition, and experimental and clinical pharmacology. Pharmacol. Rev. 45: 87-146, 1993.
59. SCHMIDT, C., PEYROUX, J., FOURNIÉ-ZALUSKI, M. C. AND ROQUES, B. P.: Analgesic responses elicited by endogenous enkephalins (protected by mixed peptidases inhibitors) on a variety of morphine-sensitive noxious tests. Eur. J. Pharmacol. 192: 253-262, 1991.
60. STANFA, L. C. AND DICKENHON, A. H.: Cholecystokinin as a factor in the enhanced potency of spinal morphine following carrageenin inflammation. Br. J. Pharmacol. 108: 967-973, 1993.
61. STANFA, L. C. AND DICKENSON, A. H.: Electrophysiological studies on the spinal role of endogenous opioids in carrageenan inflammation. Pain 56: 185-191, 1994.
62. STANFA, L. C., DICKENSON, A. H., XU, X.-J. AND WIESENFELD-HALLIN, Z.: Cholecystokinin and morphine analgesia: Variations on a theme. Trends Pharmacol. Sci. 15: 65-66, 1994.
63. SULLIVAN, A. F., DICKKNSON, A. H. AND ROQUES, B. P.: β opioid mediated inhibitions of acute and prolonged noxious-evoked responses in rat dorsal horn neurones. Br. J. Pharmacol. 98: 1039-1049, 1989.
64. TÖLLE, T. R., CASTRO-LOPES, J. M., COIMBRA, A. AND ZIEGLGÄNSBERGER, W.: Opiates modify induction of c-foss proto-oncogene in the spinal cord of the rat following noxious stimulation. Neurosci. Lett. 111: 46-51, 1990.
65. TÖLLE, T. R., CASTRO-LOPES, J. M. AND ZIEGLGÄNSBERGER, W.: c-fos induction in the spinal cord following noxious stimulation: Prevention by opiates but not by NMDA antagonists. In Proceedings of the VIth World Congress on Pain, ed. by M. R. Bond, J. E. Charlton and C. J. Woolf, pp. 299-1305, Elsevier, Amsterdam, 1991.
66. TÖLLE, T. R., HERDEGEN, T., SCHADRACK, J., BRAVO, R., ZIMMERMANN, M. AND ZIEGLGÄNSBERGER, W.: Application of morphine prior to noxious stimulation differentially modulates expression of Fos, Jun and Krox-24 proteins in rat spinal cord neurons, Neuroscience 58: 300-321, 1994a.
67. TÖLLE, T. R., SCHADRACK, J., CASTRO-LOPES, J. M., EVAN, G., ROQUES, B. P. AND ZIEGLGÄNSBERGER W.: Effects of kelatorphan and morphine before and after noxious stimulation on immediate-early gene expression in rat spinal cord neurons. Pain 56: 103-112, 1994b.
68. B receptor antagonist. Eur. J. Pharmacol. 286: 79-93, 1995.
69. VALVERDE, O., MALDONADO, R., FOURNIÉ-ZALUSKI, M. C. AND ROQUES, B. P.: Cholecystokinin B antagonists strongly potentiate antinociception mediated by endogenous enkephalins. J. Pharmacol. Exp. Ther. 270: 77-88, 1994.
70. 5)enkephalin antiserum-sensitive enhancement of morphine antinociception. Neuroreport 5: 2601-2605, 1994.
71. VANDERHAEGEN, J. J., SIGNEAU, J. C. AND GEPTS, W.: New peptide in the vertebrate central nervous system reacting with gastrin antibodies. Nature (Lond.) 257: 604-605, 1975.
72. WANK, S. A., HARKINS, R., JENSEN, R. T., SHAPIRA, H., WEERTH, A. AND SLATTERY, T.: Purification, molecular cloning and functional expression of the cholecystokinin receptor from rat pancreas. Proc. Natl. Acad. Sci. U.S.A. 89: 3125-3129, 1992.
73. WATKINS, L. R., KINSCHECK, I. B. AND MAYER, D. L.: Potentiation of morphine analgesia by cholecystokinin antagonist proglumide. Brain Res. 327: 169-180, 1985.
74. WIESENFELD-HALLIN, Z. AND DURANTI, R.: Intrathecal cholecystokinin interacts with morphine but not substance P in modulating the nociceptive flexion reflex in the rat. Peptides 8: 153-158, 1987.
75. WIESENFELD-HALLIN, Z., Xu, X.-J., HUGHES, J., HORWELL, D. C. AND HOKFELT, T.: PD134308, a selective antagonist of cholecystokinin type B receptor, enhances the analgesic effect of morphine and synergistically interacts with intrathecal galanin to depress spinal nociceptive reflexes. Proc. Natl. Acad. Sci. U.S.A. 87: 7105-7109, 1990.
76. WINTER, C. A., RISLEY, E. A. AND NUSS, G. W.: Carrageenan-induced edema in hind paw of the rat as an assay for antiinflammatory drugs. Proc. Soc. Exp. Biol. Med. 111: 544-547, 1962.
77. XU, X.-J., HAO, J.-X., SEIGER, A., HUGHES, J., HOKFELT, T. AND WIESENFELD-HALLIN, Z.: Chronic pain-related behaviours in spinally injured rats: Evidence for functional alterations of the endogenous cholecystokinin and opioid systems. Pain 56: 271-277, 1994a.
78. XU, X.-J., HOKFELT, T., HUGHES, J. AND WIESENFELD-HALLIN, Z.: The CCK-B antagonist CI988 enhances the effect of the reflex-depressive effects of morphine in axotomized rats. Neuroreport 5: 718-720, 1994b.
79. ZHOU, Y., SUN, Y.-H., ZHANG, Z.-W. AND HAN, J.-S.: Increased release of immunoreactive cholecystokinin octapeptide by morphine and potentiation of μ-opioid analgesia by CCK-B receptor antagonist L-365,260 in the rat spinal cord. Eur. J. Pharmacol. 234: 147-154, 1993.
80. ZIEGLGÄNSBERGER, W. AND TÖLLE, T. R.: The pharmacology of pain signalling. Curr. Opin. Neurobiol. 3: 611-618, 1993.
81. ZIMMERMANN, M.: Ethical guidelines for investigations of experimental pain in conscious animals. Pain 16: 109-110, 1983.