The effects of RB101, a mixed inhibitor of enkephalin-catabolizing enzymes, on carrageenin-induced spinal c-Fos expression are completely blocked by β-funaltrexamine, a selective μ-opioid receptor antagonist

Brain Research

Volumn 834, Issue 1-2, 1999, Pages 200-206

  Le Guen, Stéphanie ^a   Honoré, Prisca ^a   Catheline, Gwénaëlle ^a   Fournié Zaluski, Marie Claude ^a   Roques, Bernard Pierre ^a   Besson, Jean Marie ^a  

^a INSERM   (France)

Author keywords

Funaltrexamine; Opioid receptor; c Fos; Carrageenin; RB101; Spinal cord

Indexed keywords

BETA FUNALTREXAMINE; CARRAGEENAN; ENKEPHALIN; MU OPIATE RECEPTOR; MU OPIATE RECEPTOR ANTAGONIST; N [3 [(2 AMINO 4 METHYLTHIO)BUTYLDITHIO] 2 BENZYLPROPIONYL]PHENYLALANINE BENZYL ESTER; PROTEIN C FOS;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINOCICEPTION; ARTICLE; CONTROLLED STUDY; DRUG MECHANISM; EDEMA; MALE; NOCICEPTION; NOCICEPTIVE STIMULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RECEPTOR BINDING;

ANIMALS; CARRAGEENAN; DISULFIDES; ENZYME INHIBITORS; MALE; NALTREXONE; NARCOTIC ANTAGONISTS; NEPRILYSIN; PHENYLALANINE; PROTO-ONCOGENE PROTEINS C-FOS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, OPIOID, MU; SPINAL CORD;

EID: 0033542772     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-8993(99)01569-3     Document Type: Article

References (50)

1. Abbadie C., Besson J.-M. c-Fos expression in rat lumbar spinal cord during the development of adjuvant-induced arthritis. Neuroscience. 48:1992;985-993.
2. Abbadie C., Honoré P., Fournié-Zaluski M.-C., Roques B.P., 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. 258:1994;215-227.
3. Barber A., Gottschlich R. Opioid agonists and antagonists: an evaluation of their peripheral actions in inflammation. Med. Res. Rev. 12:1992;525-562.
4. Basbaum A.I., Fields H.L. Endogenous pain control systems: brainstem spinal pathways and endorphin circuitry. Annu. Rev. Neurosci. 7:1984;309-388.
5. V. Chapman, J.-M. Besson, Pharmacological studies of nociceptive systems using the c-Fos immunohistochemical technique: an indicator of noxiously activated spinal neurones, in: A.H. Dickenson, J.-M. Besson (Eds.), Handbook of Experimental Pharmacology: The Pharmacology of Pain, Springer-Verlag, Berlin, 1997, pp. 235-279.
6. Dickenson A.H., Sullivan A.F., Fournié-Zaluski M.-C., Roques B.P. Prevention of degradation of endogenous enkephalins produce inhibition of nociceptive neurons in rat spinal cord. Brain Res. 408:1987;185-191.
7. Draisci G., Iadarola M.J. Temporal analysis of increases in c-fos, preprodynorphin and preproenkephalin mRNAs in rat spinal cord. Mol. Brain Res. 6:1989;31-37.
8. Fournié-Zaluski M.-C., Chaillet P., Bouboutou R., Coulaud A., Chérot P., Waksman G., Costentin J., Roques B.P. Analgesic effects of kelatorphan, a new highly potent inhibitor of multiple enkephalin degrading enzymes. Eur. J. Pharmacol. 102:1984;525-528.
9. Fournié-Zaluski M.-C., Coric P., Turcaud S., Lucas E., Noble F., Maldonado R., Roques B.P. Mixed-inhibitor prodrug as a new approach towards systemically active inhibitors of enkephalin-degrading enzymes. J. Med. Chem. 35:1992;2473-2481.
10. Fournié-Zaluski M.-C., Coulaud A., Bouboutou R., Chaillet P., Devin J., Waksman G., Costentin J., Roques B.P. New bidentates as full inhibitors of enkephalin-degrading enzymes: synthesis and analgesic properties. J. Med. Chem. 28:1985;1158-1169.
11. Gogas K.R., Cho H.J., Botchkina G.I., Levine J.D., Basbaum A.I. Inhibition of noxious stimulus-evoked pain behaviors and neuronal fos-like immunoreactivity in the spinal cord of the rat by supraspinal morphine. Pain. 65:1996;9-15.
12. Gogas K.R., Presley R.W., Levine J.D., 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(3):1991;617-628.
13. Heyman J.S., Jiang Q., Rothman R.B., Mosberg H.I., Porreca F. Modulation of μ-mediated antinociception by ∂-agonists: characterization with antagonists. Eur. J. Pharmacol. 169:1989;43-52.
14. P. Honoré, J. Buritova, J.-M. Besson, Aspirin and acetaminophen reduced both Fos expression in rat lumbar spinal cord and inflammatory signs produced by carrageenin inflammation, Pain (1995).
15. Honoré P., Buritova J., Besson J.-M. Carrageenin-evoked c-Fos expression in rat lumbar spinal cord: the effects of indomethacin. Eur. J. Pharmacol. 272:1995;249-259.
16. Honoré P., Buritova J., Besson J.-M. The effects of morphine on carrageenin-induced spinal c-Fos expression are completely blocked by β-funaltrexamine, a selective mu-opioid receptor antagonist. Brain Res. 732:1996;242-246.
17. B receptor antagonist as revealed by noxiously evoked spinal c-Fos expression in the rat. J. Pharmacol. Exp. Ther. 281(1):1997;208-217.
18. Honoré P., Catheline G., Le Guen S., Besson J.-M. Chronic treatment with systemic morphine-induced tolerance to the systemic and peripheral antinociceptive effects of morphine on both carrageenin-induced mechanical hyperalgesia and spinal c-Fos expression in awake rats. Pain. 71:1997;99-108.
19. Honoré P., Chapman V., Buritova J., Besson J.-M. Reduction of carrageenin oedema and the associated c-Fos expression in the rat lumbar spinal cord by nitric oxide synthase inhibitor. Br. J. Pharmacol. 114:1995;77-84.
20. Honoré P., Chapman V., Buritova J., 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. 705:1995;91-96.
21. Hsu S., Raine L., Fanger H. Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabelled antibody (PAP) procedures. J. Histochem. Cytochem. 29:1981;577-580.
22. Kayser V., Fournié-Zaluski M.-C., Guilbaud G., Roques B.P. Potent antinociceptive effects of kelatorphan (a highly efficient inhibitor of multiple enkephalin-degrading enzymes) systemically administered in normal and arthritic rats. Brain Res. 497:1989;94-101.
23. Lord J.A.H., Waterfield A.A., Hughes J., Kosterlitz H.W. Endogenous opioid peptides: multiple agonists and receptors. Nature. 267:1979;495.
24. Maldonado R., Derrien M., Noble F., Roques B.P. Association of the peptidase inhibitor RB101 and a CCK-B antagonist strongly enhances antinociceptive responses. NeuroReport. 4:1993;947-950.
25. Maldonado R., Valverde O., Turcaud S., Fournié-Zaluski M.-C., Roques B.P. Antinociceptive response induced by mixed inhibitors of enkephalin catabolism in peripheral inflammation. Pain. 58:1994;77-83.
26. Martin J.L., Magistretti P.J. Regulation of gene expression by neurotransmitters in the central nervous system. Eur. Neurol. 39(1):1998;129-134.
27. Meucci E., Delay-Goyet P., Roques B.P., Zajac J.-M. Binding in vivo of selective μ- and δ-opioid receptor agonists. Eur. J. Pharmacol. 171:1989;167-178.
28. 6-enkephalin in the substancia gelatinosa of the cat spinal cord. Eur. J. Pharmacol. 140:1987;195-201.
29. B receptor antagonist potentiates μ-, but not δ-opioid receptor-mediated antinociception in the formalin test. Eur. J. Pharmacol. 273:1995;145-151.
30. Noble F., Roques B.P. Assessment of endogenous enkephalins efficacy in the hot plate test in mice: comparative study with morphine. Neurosci. Lett. 185:1995;75-78.
31. Noble F., Soleihac J.M., Sorocas-Lucas E., Turcaud S., Fournié-Zaluski M.-C., 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. 261:1992;181-190.
32. Parsons C.G., Czlonkowski A., Stein C., Herz A. Peripheral opioid receptors mediating antinociception in inflammation. Activation by endogenous opioids and role of the pituitary-adrenal axis. Pain. 41:1990;81-93.
33. Perrot S., Kayser V., Fournié-Zaluski M.-C., Roques B.P., Guilbaud G. Antinociceptive effect of systemic PC12, a prodrug mixed inhibitor of enkephalin-degrading enzymes, in normal and arthritic rats. Eur. J. Pharmacol. 241:1993;129-133.
34. Portoghese P.S., Larson D.L., Sayre L.M., Fries D.S. A novel opioid receptor site directed alkylating agent with irreversible narcotic antagonistic and reversible agonistic activities. J. Med. Chem. 23:1980;233-234.
35. Roques B.P., Noble F., Dauger V., Fournié-Zaluski M.-C., Beaumont A. Neutral endopeptidase 24.11: structure, inhibition, and experimental and clinical pharmacology. Pharmacol. Rev. 45(1):1993;87-146.
36. Rothman R.B., Long J.B., Bykov V., Jacobson A.E., Rice K.C., Holaday J.W. β-FNA binds irreversibly to the opiate receptor complex: in vivo and in vitro evidence. J. Pharmacol. Exp. Ther. 247:1989;405.
37. Rothman R.B., Schumacher U.K., Pert C.B. Effect of beta-FNA on opiate delta receptor binding. J. Neurochem. 43:1984;1197-1200.
38. 3H ]diprenorphine binding Brain Res. 571:1992;306-312.
39. Sawynok J., Pinsky C., Labella F.S. Minireview on the specificity of naloxone as an opiate antagonist. Life Sci. 25:1979;1621-1632.
40. Schmidt C., Peyroux J., Fournié-Zaluski M.-C., 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. 192:1991;253-262.
41. Stanfa L.C., Dickenson A.H. Electrophysiological studies on the spinal role of endogenous opioids in carrageenin inflammation. Pain. 56:1994;185-191.
42. Stein C., Hassan A.H.S., Przewlocki R., Gramsch C., Peter K., Herz A. Opioids from immunocytes interact with receptors on sensory nerves to inhibit nociception in inflammation. Proc. Natl. Acad. Sci. U.S.A. 87:1990;5935-5939.
43. C. Stein, M. Schäfer, P.J. Cabot, Q. Zhang, L. Zhou, L. Carter, Opioids and inflammation, in: D. Borsook (Ed.), Molecular Neurobiology of Pain, Progress in Pain Research and Management, IASP Press, Seattle, 1997, pp. 25-43.
44. Sullivan A.F., Dickenson A.H., Roques B.P. δ-Opioid-mediated inhibitions of acute and prolonged noxious-evoked responses in rat dorsal horn neurones. Br. J. Pharmacol. 98:1989;1039-1049.
45. Takemori A.E., Larson D.L., Portoghese P.S. The irreversible narcotic antagonistic and reversible agonistic properties of the fumaramate methyl ester derivative of naltrexone. Eur. J. Pharmacol. 70:1981;445-451.
46. Tölle T.R., Schadrack J., Castro-Lopes J.M., Evan G.I., Roques B.P., Zieglgänsberger W. Effects of kelatorphan and morphine before and after noxious stimulation on immediate-early gene expression in rat spinal cord neurons. Pain. 56:1994;103-112.
47. Valverde O., Maldonado R., Fournié-Zaluski M.-C., Roques B.P. Cholecystokinin B antagonists strongly potentiate antinociception mediated by endogenous enkephalins. J. Pharmacol. Exp. Ther. 270(1):1994;77-88.
48. Ward S.J., Portoghese P.S., Takemori A.E. Pharmacological characterization in vivo of the novel opiate, β-funaltrexamine. J. Pharmacol. Exp. Ther. 220(3):1982;494-498.
49. Zimmerman D.M., Leander J.D., Reel J.K., Hynes M.D. Use of β-funaltrexamine to determine mu opioid receptor involvement in the analgesic activity of various opioid ligands. J. Pharmacol. Exp. Ther. 241(2):1987;374-378.
50. Zimmermann M. Ethical guidelines for investigations of experimental pain in conscious animals. Pain. 16:1983;109-110.