Down-regulation of μ-opioid receptors in rat and monkey dorsal root ganglion neurons and spinal cord after peripheral axotomy

Neuroscience

Volumn 82, Issue 1, 1997, Pages 223-240

  Zhang, X ^a,b   Bao, L ^a,b   Shi, T J ^a   Ju, G ^b   Elde, R ^c   Hokfelt T ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^c UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Endorphins; Morphine; Nerve injury; Pain; Sensory neurons

Indexed keywords

CALCITONIN GENE RELATED PEPTIDE; MU OPIATE RECEPTOR; OPIATE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; INTERNEURON; MALE; MONKEY; NERVE CELL; NERVE FIBER TRANSECTION; NONHUMAN; PERIPHERAL NERVE INJURY; PRIORITY JOURNAL; RAT; RECEPTOR DOWN REGULATION; SPINAL CORD DORSAL HORN; SPINAL GANGLION;

ANIMALS; AXOTOMY; DOWN-REGULATION; GANGLIA, SPINAL; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MACACA MULATTA; MALE; MICROSCOPY, ELECTRON; NEURONS; OLIGONUCLEOTIDE PROBES; PERIPHERAL NERVES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, OPIOID, MU; RNA, MESSENGER; SPECIES SPECIFICITY; SPINAL CORD;

EID: 0030921750     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(97)00240-6     Document Type: Article

References (95)

1. Arnér L. D., Meyerson B. A. Lack of analgesic effect of opioids on neuropathic and idiopathic forms of pain. Pain. 33:1988;11-23.
2. Arnér S., Meyerson B. A. Opioids in neuropathic pain. Pain Digest. 3:1993;15-22.
3. Arvidsson U., Dado R. J., Riedl M., Lee J. H., Law P. Y., Loh H. H., Elde R., Wessendorf M. W. δ-Opioid receptor immunoreactivity: distribution in brainstem and spinal cord, and relationship to biogenic amines and enkephalin. J. Neurosci. 15:1995;3328-3341.
4. 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.
5. Arvidsson U., Riedl M., Chakrabarti S., Vulchanova L., Lee J.-H., Nakano A. H., Lin X. Q., Loh H. H., Law P.-Y., Wessendorf M. W., Elde R. The κ-opioid receptor (KOR1) is primarily postsynaptic: combined immunohistochemical localization of the receptor and endogenous opioids. Proc. natn. Acad. Sci. U.S.A. 92:1995;5062-5066.
6. Atweh S. F., Kuhar M. J. Autoradiographic localization of opiate receptors in rat brain. I. Spinal cord and lower medulla. Brain Res. 124:1977;53-67.
7. Baber N. S., Dourish C. T., Hill D. R. The role of CCK, Caerulein, and CCK antagonists in nociception. Pain. 39:1989;307-328.
8. Basbaum A. I., Fields H. L. Endogenous pain control systems: brainstem spinal pathways and endorphin circuitry. A. Rev. Neurosci. 7:1984;53-67.
9. Besse D., Lombard M. C., 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. 548:1991;287-291.
10. 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.
11. Besse D., Lombard M. C., Zajac J. M., Roques B. P., Besson J. M. Pre- and postsynaptic distribution of μ, δ and κ opioid receptors in the superficial layers of the cervical dorsal horn of the rat spinal cord. Brain Res. 521:1990;15-22.
12. Besse D., Weil-Fugazza J., Lombard M. C., Butler S. H., Besson J. M. Monoarthritis induces complex changes in μ-, δ-, and κ-opioid binding sites in the superficial dorsal horn of the rat spinal cord. Eur. J. Pharmac. 223:1992;123-131.
13. Besson J. M., Chaouch A. Peripheral and spinal mechanisms of nociception. Physiol. Rev. 67:1987;67-186.
14. Bzdega T., Chin H., Kim H., Jung H. H., Kozak C. A., Klee W. A. Regional expression and chromosomal localization of the δ opiate receptor gene. Proc. natn. Acad. Sci. U.S.A. 90:1993;9305-9309.
15. Chang K.-J., Cuatrecasas P. Multiple opiate receptors. Enkephalins and morphine bind to receptors of different specificity. J. biol. Chem. 254:1979;2610-2618.
16. Chen Y., Mestek A., Liu J., Hurley J. A., Yu L. Molecular cloning and functional expression of a mu-opioid receptor from rat brain. Molec. Pharmac. 44:1993;8-12.
17. 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.
18. Cheng P. Y., Svingos A. L., Wang H., Clarke C. L., Jebab S., Beczkowska I. W., Inturrisi C. E., Pickel V. M. Ultrastructural immunolabeling shows prominent presynaptic vesicular localization of δ-opioid receptor within both enkephalin- and nonenkephalin-containing axon terminals in the superficial layers of the rat cervical spinal cord. J. Neurosci. 15:1995;5976-5988.
19. Coons A. H. (1958) Fluorescent antibody methods. In General Cytochemical Methods (ed. Danielli J. F.), pp. 399-422. Academic, New York.
20. Corbett A. D., Paterson S. J. and Kosterlitz H. W. (1993) Selectivity of ligands for opioid receptors. In Handbook of Experimental Pharmacology, Opioids I (ed. Herz A.), pp. 645-679. Springer, Berlin.
21. Dado R. J., Law P. Y., Loh H. H., Elde R. Immunofluorescent identification of a delta (δ)-opioid receptor on primary afferent nerve terminals. NeuroReport. 5:1993;341-344.
22. Dagerlind Å., Friberg K., Bean A., Hökfelt T. Sensitive mRNA detection using unfixed tissue: combined radioactive and non-radioactive in situ hybridization histochemistry. Histochemistry. 98:1992;39-49.
23. Dourish C. T., O'Neill M. F., Coughlan J., Kitchener S. J., Hawley D., Iversen S. D. The selective CCK-B receptor antagonist L-365,260 enhances morphine analgesia and prevents morphine tolerance in the rat. Eur. J. Pharmac. 176:1990;35-44.
24. Dray A., Urban L., Dickenson A. Pharmacology of chronic pain. Trends pharmac. Sci. 15:1994;190-197.
25. Evans C. J., Keith D. E., Morrison H., Magendzo K., Edwards R. H. Cloning of a delta opioid receptor by functional expression. Science. 258:1992;1952-1955.
26. 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.
27. 3H]dipronorphine binding sites with the laminar pattern of substance P, myelin and Nissl staining. Neuroscience. 20:1987;395-407.
28. 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.
29. Gamse R., Holzer P., Lembeck F. Indirect evidence for presynaptic location of opiate receptor on chemosensitive primary sensory neurons. Naunyn-Schmiedeberg's Arch. Pharmac. 308:1979;281-285.
30. 125I]FK-33-824-labelled mu opioid receptors in the spinal cord of normal and deafferented rats. Neuroscience. 43:1991;197-209.
31. Gouarderes C., Cros J., Quirion R. Autoradiographic localization of mu, delta and kappa receptor binding sites in rat and guinea pig spinal cord. Neuropeptides. 6:1985;331-342.
32. Govrin-Lippmann R., Devor M. Ongoing activity in severed nerves: source and variation with time. Brain Res. 159:1978;406-410.
33. Gundersen H. J. G., Bagger P., Bendtsen T. F., Evans S. M., Korbo L., Marcussen N., Møller A., Nielsen K., Nyengaard J. R., Pakkenberg B., Sorensen F. B., Vesterby A., West M. The new stereological tools: disector, fractionator, nucleator and point sampled intercepts and their use in pathological research and diagnosis. APMIS. 96:1988;857-881.
34. Herz A. (ed.) (1993) Handbook of Experimental Pharmacology, Opioids I and II. Springer, Berlin.
35. Hiller J. M., Zhang Y., Bing G., Gioannini T. L., Stone E. A., Simon E. J. Immunohistochemical localization of mu-opioid receptors in rat brain using antibodies generated against a peptide sequence present in a purified mu-opioid binding protein. Neuroscience. 62:1994;829-841.
36. 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.
37. Honda C. N., Arvidsson U. Immunohistochemical localization of delta- and mu-opioid receptors in primate spinal cord. NeuroReport. 6:1995;1025-1028.
38. Iadarola M. J., Brady L. S., Draisci G., Dubner R. Enhancement of dynorphin gene expression in spinal cord following experimental inflammation: stimulus specificity, behavioral parameters and opioid receptor binding. Pain. 35:1988;313-326.
39. Itoh S., Katsuura G., Maeda Y. Caerulein and cholecystokinin suppress β-endorphin-induced analgesia in the rat. Eur. J. Pharmac. 80:1982;421-425.
40. Jessell T., Tsunoo A., Kanazawa I., Otsuka M. Substance P: depletion in the dorsal horn of the rat spinal cord after section of the peripheral processes of primary sensory neurons. Brain Res. 168:1979;247-259.
41. 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.
42. Johnson D. G., de C. Nogueira Araujo G. M. A simple method of reducing the fading of immunofluorescence during microscopy. J. immun. Meth. 43:1981;349-350.
43. Kar S., Rees R. G., Quirion R. Altered calcitonin gene-related peptide, substance P and enkephalin immunoreactivities and receptor binding sites in the dorsal spinal cord of the polyarthritic rat. Eur. J. Neurosci. 6:1994;345-354.
44. Kieffer B. L., Befort K., Gaveriaux-Ruff C., Hirth C. G. The δ-opioid receptor: isolation of a cDNA by expression cloning and pharmacological characterization. Proc. natn. Acad. Sci. U.S.A. 89:1992;12048-12052.
45. Kupers R. C., Konings H., Adriensen H., Gybels J. M. Morphine differentially affects the sensory and affective pain ratings in neurogenic and idiopathic forms of pain. Pain. 47:1991;5-12.
46. Lamotte C., Pert C. B., Snyder S. H. Opiate receptor binding in primate spinal cord: distribution and changes after dorsal root section. Brain Res. 112:1976;407-412.
47. Lawson S. N., Waddell P. J. Soma neurofilament immunoreactivity is related to cell size and fiber conduction velocity in rat primary sensory neurons. J. Physiol. 435:1991;41-63.
48. Levine J. D., Fields H. L., Basbaum A. I. Peptides and the primary afferent nociceptor. J. Neurosci. 13:1993;2273-2286.
49. 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.
50. Lord J., Waterfield A., Hughes J., Kosterlitz H. Endogenous opioid peptides: multiple agonists and receptors. Nature. 267:1977;495-499.
51. Maekawa K., Minami M., Masuda T., Satoh M. Expression of μ- and κ-, but not δ-, opioid receptor mRNAs is enhanced in the spinal dorsal horn of the arthritic rats. Pain. 64:1995;365-371.
52. 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.
53. 1 receptor in the rat CNS and pituitary. Neuroscience. 71:1996;671-690.
54. 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.
55. Mansour A., Fox C. A., Burke S., Akil H., Watson S. J. Immunohistochemical localization of the cloned μ opioid receptor in the rat CNS. J. comp. Neurol. 350:1995;412-438.
56. Mansour A., Fox C. A., Burke S., Meng F., Thompson R. C., Akil H., Watson S. J. Mu, delta, and kappa opioid receptor mRNA expression in the rat CNS: an in situ hybridization study. J. comp. Neurol. 350:1994;412-438.
57. Mansour A., Fox C. A., Meng F., Akil H., Watson S. J. Kappa1 receptor mRNA distribution in the rat CNS: comparison to kappa receptor binding and prodynorphin mRNA. Cell. molec. Neurosci. 5:1994;124-144.
58. Mansour A., Fox C. A., Thompson R. C., Akil H., Watson S. J. Mu-opioid receptor mRNA expression in the rat CNS: comparison to mu-receptor binding. Brain Res. 643:1994;245-265.
59. Mansour A., Thompson R. C., Akil H., Watson S. J. Delta opioid receptor mRNA distribution in the brain: comparison to delta receptor binding and proenkephalin mRNA. J. chem. Neuroanat. 6:1993;351-362.
60. Martin W. R., Eades C. G., Thompson J. A., Huppler R. E., Gilbert P. E. The effects of morphine- and nalorphine-like drugs in the nondependent and morphine-dependent chronic spinal dog. J. Pharmac. exp. Ther. 197:1976;196-203.
61. Maxwell D. J., Réthelyi M. Ultrastructure and synaptic connections of cutaneous afferent fibres in the spinal cord. Trends Neurosci. 10:1987;117-123.
62. Meng F., Xie G. X., Thompson R. C., Mansour A., Goldstein A., Watson S. J., Akil H. Cloning and pharmacological characterization of a rat kappa opioid receptor. Proc. natn. Acad. Sci. U.S.A. 90:1993;9954-9958.
63. Millan M. J., Czlonkowski A., Morris B., Stein C., Arendt R., Huber A., Höllt V., Herz A. Inflammation of the hind limb as a model of unilateral localized pain: influence on multiple opioid systems in the spinal cord of the rat. Pain. 35:1988;299-312.
64. Millan M. J., Millan M. H., Czlonkowski A., Höllt V., Pilcher C. W. T., Herz A., Colpaert F. C. A model of chronic pain in the rat: response of multiple opioid system to adjuvant-induced arthritis. J. Neurosci. 6:1986;899-906.
65. 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.
66. Minami M., Onogi T., Toya T., Katao Y., Hosoi Y., Maekawa K., Katsumata S., Yabuuchi K., Satoh M. Molecular cloning and in situ hybridization histochemistry for rat μ-opioid receptor. Neurosci. Res. 18:1994;315-322.
67. Minami M., Satoh M. Molecular biology of the opioid receptors: structures, functions and distributions. Neurosci. Res. 23:1995;121-145.
68. Minami M., Toya T., Katao Y., Maekawa K., Nakamura S., Onogi T., Kaneko S., Satoh M. Cloning and expression of a cDNA for the rat kappa-opioid receptor. Fedn Eur. biochem. Socs Lett. 329:1993;291-295.
69. Ninkovic M., Hunt S. P., Gleave J. R. W. Localization of opiate and histamine H1-receptors in the primate sensory ganglia and spinal cord. Brain Res. 241:1982;197-206.
70. Ninkovic M., Hunt S. P., Kelly J. S. Effect of dorsal rhizotomy on the autoradiographic distribution of opiate and neurotensin receptors and neurotensin-like immunoreactivity within the rat spinal cord. Brain Res. 230:1981;111-119.
71. Pasternak G. W. (ed.) (1988) The Opioid Receptors. Humana, New Jersey.
72. 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.
73. Scadding J. W. (1984) Peripheral neuropathies. In Textbook of Pain (eds Wall P. D. and Melzack R.), pp. 413-425. Churchill Livingstone, Edinburgh.
74. Schäfer M.-H., Nohr D., Krause J. E., Weihe E. Localization of kappa-opioid receptor mRNA in neuronal subpopulations of rat sensory ganglia and spinal cord. Neurosci. Lett. 167:1993;137-140.
75. Simon E. J. and Gioannini T. L. (1993) Opioid receptor multiplicity: isolation, purification, and chemical characterization of binding sites. In Handbook of Experimental Pharmacology, Opioids I (ed. Herz A.), pp. 3-26. Springer, Berlin.
76. Smith J. R., Simon E. J. Selective protection of sterospecific enkephalin and opiate binding against inactivation by N-ethylmaleimide: evidence for two classes of opiate receptors. Proc. natn. Acad. Sci. U.S.A. 77:1980;281-284.
77. 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.
78. Stevens C. W., Lacey C. B., Miller K. E., Elde R. P., Seybold V. S. Biochemical characterization and regional quantification of μ, δ and κ opioid binding sites in rat spinal cord. Brain Res. 550:1991;77-85.
79. Tasker R. R., Tsuda T. and Hawrylyshyn P. (1983) Clinical neurophysiological investigation of deafferentation pain. In Advances in Pain Research and Therapy (eds Bonica J. J., Lindblom U. and Iggo A.), Vol. 5, pp. 713-738. Raven, New York.
80. Thompson R. C., Mansour A., Akil H., Watson S. J. Cloning and phamacological characterization of a rat μ opioid receptor. Neuron. 11:1993;903-913.
81. Verge V. M. K., Wiesenfeld-Hallin Z., Hökfelt T. Cholecystokinin in mammalian primary sensory neurons and spinal cord: in situ hybridization studies in rat and monkey. Eur. J. Neurosci. 5:1993;240-250.
82. Wall P. D., Gutnick M. Ongoing activity in peripheral nerves: the physiology and pharmacology of impulses originating from a neuroma. Expl Neurol. 43:1974;580-593.
83. Wang J. B., Imai Y., Eppler C. M., Gregor P., Spivak C. E., Uhl G. R. μ opiate receptor: cDNA cloning and expression. Proc. natn. Acad. Sci. U.S.A. 90:1993;10230-10234.
84. Watkins L. R., Kinscheck I. B., Mayer D. J. Potentiation of opiate analgesia and apparent reversal of morphine tolerance by proglumide. Science. 224:1983;395-396.
85. Wiesenfeld-Hallin Z., Duranti R. Intrathecal cholecystokinin interacts with morphine but not substance P in modulating the nociceptive flexion reflex in the rat. Peptides. 8:1987;153-158.
86. Wiesenfeld-Hallin Z., Xu X. J., Hughes J., Horwell D. C., Hökfelt 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. natn. Acad. Sci. U.S.A. 87:1990;7105-7109.
87. Willis W. D. Jr and Coggeshall R. E. (1991) Sensory Mechanisms of the Spinal Cord. Plenum, New York.
88. 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;129-132.
89. Yasuda K., Raynor K., Kong H., Breder C. D., Takeda J., Reisine T., Bell G. I. Cloning and functional comparison of κ and δ opioid receptors from mouse brain. Proc. natn. Acad. Sci. U.S.A. 90:1993;6736-6740.
90. Young W. S. I., Wamsley J. K., Zarbin M. A., Kuhar M. J. Opioid receptors undergo axonal flow. Science. 210:1980;76-78.
91. Zamboni I., De Martino C. Buffered picric acid formaldehyde. A new rapid fixative for electron microscopy. J. Cell Biol. 35:1967;148A.
92. Zarbin M. A., Wamsley J. K., Kuhar M. J. Anterograde transport of opioid receptors in rat vagus nerves and dorsal roots of spinal nerves: pharmacology and sensitivity to sodium and guanine nucleotides. Expl Brain Res. 81:1990;267-278.
93. Zerari F., Zouaoui D., Gastard M., Apartis E., Fischer J., Herbrecht F., Cupo A., Cucumel K., Conrath M. Ultrastructural study of δ-opioid receptors in the dorsal horn of the rat spinal cord using monoclonal anti-idiotypic antibodies. J. chem. Neuroanat. 7:1994;159-170.
94. Zhang X., Bao L., Xu Z.-Q., Kopp J., Arvidsson U., Elde R., Hökfelt T. Localization of neuropeptide Y Y1 receptors in the rat nervous system with special reference to somatic receptors on small dorsal root ganglion neurons. Proc. natn. Acad. Sci. U.S.A. 91:1994;12540-12543.
95. 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.