Effect of morphine on cholecystokinin and μ-opioid receptor-like immunoreactivities in rat spinal dorsal horn neurons after peripheral axotomy and inflammation

Neuroscience

Volumn 95, Issue 1, 1999, Pages 197-207

  Zhang, X ^a,b   De Araujo Lucas, G ^a   Elde, R ^c   Wiesenfeld Hallin, Z ^a   Hokfelt T ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^c UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Analgesia; Co existence; Nerve injury; Pain; Spinal cord

Indexed keywords

CHOLECYSTOKININ; CHOLECYSTOKININ RECEPTOR; MORPHINE; MU OPIATE RECEPTOR; NALOXONE;

ANALGESIC ACTIVITY; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOSE RESPONSE; DRUG EFFECT; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; INFLAMMATION; INTRAVENOUS DRUG ADMINISTRATION; MALE; NERVE CELL; NERVE FIBER TRANSECTION; NONHUMAN; PRIORITY JOURNAL; RAT; SPINAL CORD DORSAL HORN;

ANALGESICS, OPIOID; ANIMALS; AXOTOMY; CHOLECYSTOKININ; GANGLIA, SPINAL; IMMUNOHISTOCHEMISTRY; INFLAMMATION; MALE; MORPHINE; POSTERIOR HORN CELLS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, OPIOID, MU; SPINAL CORD; TISSUE DISTRIBUTION;

EID: 0032703857     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(99)00419-4     Document Type: Article

References (78)

1. Afifiy E.A., Law P.Y., Riedl M., Elde R., Loh H.H. Role of carboxyl terminus of μ- and δ-opioid receptor in agonist-induced down-regulation. Molec. Brain Res. 54:1998;24-34.
2. Alster P., Lucas G. A., Zhang X., Hökfelt T. and Wiesenfeld-Hallin Z. (1998) On the mechanism of cholecystokinin release in the spinal cord dorsal horn during peripheral inflammation. In Opioid Sensitivity of Chronic Non-Cancer Pain. Proc. First IASP Research Symposium, Helsinki, (Abstract).
3. Arden J.R., Segredo V., Waing Z., Lameh J., Sadée W. Phosphorylation and agonist-specific intracellular trafficking of an epitope-tagged μ-opioid receptor expressed in HEK 293 cells. J. Neurochem. 65:1995;1636-1645.
4. Arnér L.D., Meyerson B.A. Lack of analgesic effect of opioids on neuropathic and idiopathic forms of pain. Pain. 33:1988;11-23.
5. Arvidsson U., Riedl M., Chakrabarti S., Lee J.H., Nakano A.H., Dado R.J., Loh H.H., Law P.Y., Wessendorf M.W., Elde R. Distribution and targeting of a μ-opioid receptor (MOR1) in brain and spinal cord. J. Neurosci. 15:1995;1215-1235.
6. Barber N.S., Dourish C.T., Hill D.R. The role of CCK, caerulein, and CCK antagonists in nociception. Pain. 39:1989;307-328.
7. Besse D., Lombard M.C., Perrot S., Besson J.M. Regulation of opioid binding sites in the superficial dorsal horn of the rat spinal cord following loose ligation of the sciatic nerve: comparison with sciatic nerve section and lumbar dorsal rhizotomy. Neuroscience. 50:1992;921-933.
8. Bourgoin S., Benoliel J.J., Collin E., Mauborgne A., Pohl M., Hamon M., Cesselin F. Opioidergic control of the spinal release of neuropeptides. Possible significance for the analgesic effects of opioids. Fundam. clin. Pharmac. 8:1994;307-321.
9. Bras J.M.A., Laporte A.-M., Benoliel J.J., Bourgoin S., Mauborgne A., Hamon M., Cesselin F., Pohl M. Effect of peripheral axotomy on cholecystokinin neurotransmission in the rat spinal cord. J. Neurochem. 72:1999;858-867.
10. Burford N.T., Tolbert L.M., Sadee W. Specific G protein activation and μ-opioid receptor internalization caused by morphine, DAMGO and endomorphin I. Eur. J. Pharmac. 342:1998;123-126.
11. Cesselin F. Opioid and anti-opioid petides. Fundam. clin. Pharmac. 9:1995;409-433.
12. Chen Y., Mestek A., Yu L. Molecular cloning of a rat kappa opioid receptor reveals sequence similarities to the mu and delta opioid receptors. Biochem. J. 295:1993;625-628.
13. Cheng P.Y., Liu-Chen L.-Y., Pickel V.M. Dual ultrastructural immunocytochemical labeling of μ and δ opioid receptors in the superficial layers of the rat cervical spinal cord. Brain Res. 778:1997;367-380.
14. 5-enkephalin. Brain Res. 731:1996;141-154.
15. Cortés R., Arvidsson U., Schalling M., Ceccatelli S., Hökfelt T. In situ hybridization studies on mRNAs for cholecystokinin, calcitonin gene-related peptide and choline acetyltransferase in the lower brain stem, spinal cord and dorsal root ganglia of rat and guinea pig with special reference to motoneurons. J. chem. Neuroanat. 3:1990;467-485.
16. deGroot J.F., Coggeshall R.E., Carlton S.M. The reorganization of μ opioid receptors in the rat dorsal horn following peripheral axotomy. Neurosci. Lett. 233:1997;113-116.
17. Dickenson A.H. Mechanisms of the analgesic actions of opiates and opioids. Br. med. Bull. 47:1991;690-702.
18. Ding Y.-Q., Kaneko T., Nomura S., Mizuno N. Immunohistochemical localization of μ-opioid receptors in the central nervous system of the rat. J. comp. Neurol. 367:1996;375-402.
19. Ding Y.Q., Nomura S., Kaneko T., Mizuno N. Presynaptic localization of mu-opioid receptor-like immunoreactivity in retinal axon terminals within the terminal nuclei of the accessory optic tract: a light and electron microscope study in the rat. Neurosci. Lett. 199:1995;142-149.
20. Duggan A.W., North R.A. Electrophysiology of opioids. Pharmac. Rev. 35:1984;219-281.
21. Faris P.L., Komisaruk B.R., Watkins L.R., Mayer D.J. Evidence for the neuropeptide cholecystokinin as an antagonist of opiate analgesia. Science. 219:1983;310-312.
22. Fields H.L., Emson P.C., Leigh B.K., Gilbert R.F., Iversen L.L. Multiple opiate receptors on primary afferent fibers. Nature. 284:1980;351-353.
23. Fuji K., Senba E., Fuji S., Nomura I., Wu J.-Y., Ueda U., Tohyama M. Distribution, ontogeny and projections of cholecystokinin-8, vasoactive intestinal polypeptide and γ-aminobutyrate-containing neuron systems in the rat spinal cord: an immunohistochemical analysis. Neuroscience. 14:1985;881-894.
24. Ghilardi J.R., Allen C.J., Steven R.V., McVey D.C., Mantyh P.W. Trigeminal and dorsal root ganglion neurons express CCK receptor binding sites in the rat, rabbit, and monkey: possible site of opiate-CCK analgesic interactions. J. Neurosci. 12:1992;4854-4866.
25. Han J.S., Ding X.Z., Fan S.G. Is cholecystokinin octapeptide (CCK-8) a candidate for endogenous anti-opioid substrate? Neuropeptides. 5:1985;399-402.
26. Hökfelt T., Herrera-Marschitz M., Seroogy K., Gong J., Staines W.A., Holets V., Schalling M., Ungerstedt U., Post C., Rehfeld J.F., Frey P., Fischer J., Dockray G., Hamaoka T., Walsh H.H., Goldstein M. Immunohistochemical studies on cholecystokinin (CCK)-immunoreactive neurons in the rat using sequence specific antisera and with special reference to the caudate nucleus and primary sensory neurons. J. chem. Neuroanat. 1:1988;11-52.
27. Hökfelt T., Skirboll L., Everitt B.J., Meister B., Brownstein M., Jacobs T., Faden A., Kuga S., Goldstein M., Markstein R., Dockray G., Rehfeld J. Distribution of cholecystokinin-like immunoreactivity in the nervous system with special reference to coexistence with classical neurotransmitters and other neuropeptides. Ann. N.Y. Acad. Sci. 448:1985;255-274.
28. Hökfelt T., Zhang X., Wiesenfeld-Hallin Z. Messenger plasticity in primary sensory neurons following axotomy and its functional implications. Trends Neurosci. 17:1994;22-30.
29. Itoh S., Katsuura G., Maeda Y. Cauerulein and cholecystokinin suppress β-endorphin-induced analgesia in the rat. Eur. J. Pharmac. 80:1982;421-425.
30. Jessell T.M., Iversen L.L. Opiate analgesics inhibit substance P release from rat trigeminal nucleus. Nature. 268:1977;549-551.
31. Ji R.-R., Zhang Q., Law P.-Y., Low H.H., Elde R., Hökfelt T. Expression of μ-, δ-, and κ-opioid receptor-like immunoreactivities in rat dorsal root ganglia after carrageenan-induced inflammation. J. Neurosci. 15:1995;8156-8166.
32. Johnson G.D., Nogueira Araujo G.M. A simple method of reducing the fading of immunofluorescence during microscopy. J. immun. Meth. 43:1981;349-350.
33. Kar S., Quirion R. Neuropeptide receptors in developing and adult rat spinal cord: an in vitro quantitative autoradiography study of calcitonin gene-related peptide, neurokinins, μ-opioid, galanin, somatostatin, neurotensin and vasoactive intestinal polypeptide receptors. J. comp. Neurol. 354:1995;253-281.
34. Keith D.E., Anton B., Murray S.R., Zaki P.A., Chu P.C., Lissin D.V., Monteillet-Agius G., Stewart P.L., Evans C.J., von Zastrow M. μ-Opioid receptor internalization: opiate drugs have differential effects on a conserved endocytic mechanism in vitro and in the mammalian brain. Molec. Pharmac. 53:1998;377-384.
35. Kemp T., Spike R.C., Watt C., Todd A. The u-opioid receptor (MOR1) is mainly restricted to neurons that do not contain GABA or glycine in the superficial dorsal horn of the rat spinal cord. Neuroscience. 75:1996;1231-1238.
36. Koch T., Schulz S., Schröder H., Wolf R., Raulf E., Höllt V. Carboxyl-terminal splicing of the rat μ opioid receptor modulates agonist-mediated internalization and receptor resensitization. J. biol. Chem. 273:1998;13,652-13,657.
37. Leah J., Menetrey D., de Pommery J. Neuropeptides in long ascending spinal tract cells in the rat: evidence for parallel processing of ascending information. Neuroscience. 24:1988;195-207.
38. Li J.-L., Ding Y.-D., Li Y.-Q., Li J.-S., Nomura S., Kaneko T., Mizuno N. Immunocytochemical localization of μ-opioid receptor in primary afferent neurons containing substance P or calcitonin gene-related peptide. A light and electron microscope study in the rat. Brain Res. 794:1998;347-352.
39. Lombard M.C., Besse D., Chen Y.L., Besson J.M. Mu-opioid receptors in the superficial spinal dorsal horn in an experimental model of peripheral mononeuropathy in the rat. Eur. J. Pharmac. 181:1990;2308.
40. Lucas G.A., Alster P., Brodin E., Wiesenfeld-Hallin Z. Differential release of cholecystokinin by morphine in rat spinal cord. Neurosci. Lett. 245:1998;13-16.
41. Maciewicz R., Phipps B.S., Grenier J., Poletti C.E. Edinger-Westphal nucleus: cholecystokinin immunocytochemistry and projections to spinal cord and trigeminal nucleus in the cat. Brain Res. 299:1984;139-145.
42. Maekawa K., Minami M., Yabuuchi K., Toya T., Katao Y., Hosoi Y., Onogi T., Satoh M. In situ hybridization of μ- and κ-opioid receptor mRNAs in the rat spinal cord and dorsal root ganglia. Neurosci. Lett. 168:1994;97-100.
43. Magnuson D.S., Dickenson A.H. Lamina-specific effects of morphine and naloxone in dorsal horn of rat spinal cord in vitro. J. Neurophysiol. 66:1991;1941-1950.
44. Mansour A., Fox C.A., Akil H., Watson S.J. Opioid-receptor mRNA expression in the rat CNS: anatomical and functional implications. Trends Neurosci. 18:1995;22-29.
45. Min B.H., Augustin L.B., Felsheim R.F., Fuchs J.A., Loh H.H. Genomic structure and analysis of promoter sequence of a mouse μ opioid receptor gene. Proc. natn. Acad. Sci. U.S.A. 91:1994;9081-9085.
46. Minami M., Maekawa K., Yabuuchi K., Satoh M. Double in situ hybridization study on coexistence of μ-, δ-, and κ-opioid receptor mRNAs with preprotachykinin A mRNA in the rat dorsal root ganglia. Molec. Brain Res. 30:1995;203-210.
47. Minami M., Satoh M. Molecular biology of the opioid receptors: structures, functions and distributions. Neurosci. Res. 23:1995;121-145.
48. North R.A. Twelfth Gaddum memorial lecture. Drug receptors and the inhibition of nerve cells. Br. J. Pharmac. 98:1989;13-28.
49. Pan Z.Z., William J.T., Osborne P.B. Opioid actions on single nucleus raphe magnus neurons from rat and guinea-pig in vitro. J. Physiol. 427:1990;519-532.
50. Pease P.C. Buffered formaldehyde as a killing agent and primary fixative for electron microscopy. Anat. Rec. 142:1962;342.
51. Platt J.L., Michael A.F. Retardation of fading and enhancement of intensity of immunofluorescence by p-phenylenediamine. J. Histochem. Cytochem. 31:1983;840-842.
52. Porreca F., Tang Q., Bian D., Riedl M., Elde R., Lai J. Spinal opioid mu receptor expression in lumbar spinal cord of rats following nerve injury. Brain Res. 795:1998;197-203.
53. Sarne Y., Fields A., Keren O., Gafni M. Stimulatory effects of opioids on transmitter release and possible cellular mechanisms: overview and original results. Neurochem. Res. 21:1996;1353-1361.
54. Segredo V., Burford N.T., Lameh J., Sadée W. A constitutively internalizing and recycling mutant of the μ-opioid receptor. J. Neurochem. 68:1997;2395-2404.
55. Stanfa L., Dickenson A., Xu X.-J., Wiesenfeld-Hallin Z. Cholecystokinin and morphine analgesia: variations on a theme. Trends pharmac. Sci. 15:1994;65-66.
56. Stanfa L.C., Sullivan A.F., Dickenson A.H. Alterations in neuronal excitability and the potency of spinal mu, delta and kappa opioids after carrageenan-induced inflammation. Pain. 50:1992;345-354.
57. Stein C., Hassan 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. natn. Acad. Sci. U.S.A. 87:1990;5935-5939.
58. Stein C., Millan M.J., Shippenberg T.S., Peter K., Herz A. Peripheral opioid receptors mediating antinociception in inflammation: evidence for involvement of mu, delta and kappa receptors. J. Pharmac. exp. Ther. 248:1992;1269-1275.
59. Sternini C., Spann M., Anton B., Keith D.E., Bunnet N.W., von Zastrow M., Evans C., Brecha N.C. Agonist-selective endocytosis of μ opioid receptor by neurons in vivo. Proc. natn. Acad. Sci. U.S.A. 93:1996;9241-9246.
60. Stevens C.W., Kajander K.C., Bennett G.J., Seybold V.S. Bilateral and differential changes in spinal mu, delta, and kappa opioid binding in rats with a painful, unilateral neuropathy. Pain. 46:1991;315-326.
61. Tong Y.-G., Wang H.F., Ju G., Grant G., Hökfelt T., Zhang X. Increased uptake and transport of cholera toxin B-subunit in dorsal root ganglion neurons after peripheral axotomy: possible implications for sensory sprouting. J. comp. Neurol. 404:1999;143-158.
62. Vanderhaeghen J.J., Deschepper C., Lotstra F., Vierendeels G., Schoenen J. Immunohistochemical evidence for cholecystokinin-like peptides in neuronal cell bodies of the rat spinal cord. Cell Tiss. Res. 223:1982;463-467.
63. Verge V.M.K., Wiesenfeld-Hallin Z., Hökfelt T. Cholecystokinin in mammalian primary sensory neurons and spinal cord: in situ hybridization studies on rat and monkey spinal ganglia. Eur. J. Neurosci. 5:1993;240-250.
64. Vizi E.S., Harsing L.G., Knoll J. Inhibitory effect of dopamine on acetylcholine release from caudate nucleus. Pol. J. Pharmac. Pharm. 29:1977;201-211.
65. Wang X.J., Wang X.H., Han J.S. Cholecystokinin octapeptide antagonized opioid analgesia mediated by μ- and κ- but not δ-receptors in the spinal cord of the rat. Brain Res. 523:1990;5-10.
66. Watkins L.R., Kinscheck I.B., Kaufman E.F.S., Miller J., Frenk H., Mayer D.J. Cholecystokinin antagonists selectively potentiate analgesia induced by endogenous opiates. Brain Res. 327:1985;181-190.
67. Watkins L.R., Kinscheck I.B., Mayer D.J. Potentiation of opiate analgesia and apparent reversal of morphine tolerance by proglumide. Science. 224:1984;395-396.
68. Xu X.-J., Puke M.J.C., Verge V.M.K., Wiesenfeld-Hallin Z., Hughes J., Hökfelt T. Up-regulation of cholecystokinin in primary sensory neurons is associated with morphine insensitivity in experimental neuropathic pain. Neurosci. Lett. 152:1993;132-139.
69. Xu Z.-Q.D., Zhang X., Grillner S., Hökfelt T. Electrophysiological studies on rat dorsal root ganglion neurons after peripheral axotomy: changes in responses to neuropeptides. Proc. natn. Acad. Sci. U.S.A. 94:1997;13,262-13,266.
70. Yabaluri N., Medzihradsky F. Down-regulation of μ-opioid receptor by full but not partial agonists is independent of G protein coupling. Molec. Pharmac. 52:1997;896-902.
71. Zajac J.-M., Lombard M.-C., Peschanski M., Besson J.-M., Roques B.P. Autoradiographic study of μ and δ opioid binding sites and neutral endopeptidase-24.11 in rat after dorsal root rhizotomy. Brain Res. 477:1989;400-403.
72. Zamboni I., De Martino C. Buffered picric acid formaldehyde. A new rapid fixative for electron microscopy. J. Cell Biol. 35:1967;148A.
73. Zhang J., Ferguson S.S.G., Barak L.S., Bodduluri S.R., Laporte S.A., Law P.-Y., Caron M.G. Role for G protein-coupled receptor kinase in agonist-specific regulation of μ-opioid receptor responsiveness. Proc. natn. Acad. Sci. U.S.A. 95:1998;7157-7162.
74. Zhang X., Bao L., Shi T.-J., Ju G., Elde R., Hökfelt T. Downregulation of u-opioid receptors in rat and monkey dorsal root ganglion neurons and spinal cord after peripheral axotomy. Neuroscience. 82:1998;223-240.
75. Zhang X., Dagerlind Å., Elde R.P., Castel M.-N., Broberger C., Wiesenfeld-Hallin Z., Hökfelt T. Marked increase in cholecystokinin B receptor messenger RNA levels in rat dorsal root ganglia after peripheral axotomy. Neuroscience. 57:1993;227-233.
76. Zhang X., Nicholas A.P., Hökfelt T. Ultrastructural studies on peptides in the dorsal horn of the spinal cord. I. Co-existence of galanin with other peptides in primary afferents in normal rats. Neuroscience. 57:1993;365-384.
77. Zieglgänsberger W., French E.D., Siggins G.R., Bloom F.E. Opioid peptides may excite hippocampal pyramidal neurons by inhibiting adjacent inhibitory interneurons. Science. 205:1979;415-417.
78. Zouaoui D., Benoliel J.J., Cesselin F., Conrath M. Cholecystokinin-like immunoreactivity in the rat spinal cord: effects of thoracic transection. Brain Res. Bull. 26:1991;543-547.