Expression of μ-, δ-, and κ-opioid receptor-like immunoreactivities in rat dorsal root ganglia after carrageenan-induced inflammation

Journal of Neuroscience

Volumn 15, Issue 12, 1995, Pages 8156-8166

  Ji, Ru Rong ^a   Zhang, Qin ^a   Law, P Y ^b   Low, H H ^b   Elde, R ^b   Hokfelt T ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b UNIVERSITY OF MINNESOTA   (United States)

Author keywords

axonal transport; coexistence; multiple opioid receptors; pain; primary sensory neurons; spinal cord

Indexed keywords

CARRAGEENAN; EPITOPE; KAPPA OPIATE RECEPTOR; MU OPIATE RECEPTOR; SIGMA OPIATE RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; CYTOPLASM; GENE EXPRESSION; IMMUNOREACTIVITY; INFLAMMATION; MALE; NERVE FIBER TRANSPORT; NONHUMAN; PAIN; PRIORITY JOURNAL; RAT; SCIATIC NERVE; SENSORY NERVE CELL; SPINAL CORD; SPINAL CORD DORSAL HORN; SPINAL GANGLION;

EID: 0029416910     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.15-12-08156.1995     Document Type: Article

References (93)

1. Arvidsson U, Dado RJ, Riedl M, Lee JH, Law PY, Loh HH, Elde R, Wessendorf MW (1995a) δ-opioid receptor immunoreactivity: distribution in brainstem and spinal cord, and relationship to biogenic amines and enkephalin. J Neurosci 15:1215-1235.
2. Arvidsson U, Riedl M, Chakrabarti S, Lee JH, Nakano AH, Dado RJ, Loh HH, Law PY, Wessendorf MW, Eide R (1995b) Distribution and targeting of a μ-opioid receptor (MOR1) in brain and spinal cord. J Neurosci 15:3328-3341.
3. Arvidsson U, Riedl M, Chakrabarti S, Vulchanova L, Lee J-H, Nakano AH, Lin XQ, Loh HH, Law P-Y, Wessendorf MW, Elde R (1995c) The κ-opioid receptor is primarily postsynaptic: combined immunohistochemical localization of the receptor and endogenous opioids. Proc Natl Acad Sci USA 92:5062-5066.
4. Atweh SF, Kuhar MJ (1977) Autoradiographic localization of opiate receptors in rat brain. I. Spinal cord and lower medulla. Brain Res 124:53-67.
5. Basbaum AI, Fields HL (1984) Endogenous pain control systems: brainstem spinal pathways and endorphin circuitry. Annu Rev Neurosci 7:309-338.
6. Besse D, Lombard MC, Zajac JM, Roques BP, Besson JM (1990) Preand 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 521:15-22.
7. Besse D, Lombard MC, Perrot S, Besson JM (1992a) 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: 921-933.
8. Besse D, Weil-Fugazza J, Lombard MC, Butler SH, Besson JM (1992b) Monoarthritis induces complex changes in μ-, δ-, and κ-opioid binding sites in the superficial dorsal horn of the rat spinal cord. Eur J Pharmacol 223:123-131.
9. Besson JM, Chaouch A (1987) Peripheral and spinal mechanisms of nociception. Physiol Rev 67:67-186.
10. Bourgoin S, Le Bars D, Clot AM, Hamon M, Cesselin F (1988) Spontaneous and evoked release of met-enkephalin-like material from the spinal cord of arthritic rats in vivo. Pain 32:107-114.
11. Bzdega T, Chin H, Kim H, Jung HH, Kozak CA, Klee WA (1993) Regional expression and chromosomal localization of the δ opiate receptor gene. Proc Natl Acad Sci USA 90:9305-9309.
12. Cesselin F, Bourgoin S, Artaud F, Hamon M (1984) Basic and regulatory mechanisms of in vitro release of met-enkephalin from the dorsal zone of the rat spinal cord. J Neurochem 43:763-773.
13. Chang K-J, Cuatrecasas P (1979) Multiple opiate receptors. Enkephalins and morphine bind to receptors of different specificity. J Biol Chem 254:2610-2618.
14. Chen Y, Mestek A, Liu J, Hurley JA, Yu L (1993a) Molecular cloning and functional expression of a mu-opioid receptor from rat brain. Mol Pharmacol 44:8-12.
15. Chen Y, Mestek A, Yu L (1993b) Molecular cloning of a rat kappa opioid receptor reveals sequence similarities to the mu and delta opioid receptors. Biochem J 295:625-628.
16. Collin E, Mauborgne A, Bourgoin S, Mantelet S, Ferhat L, Hamon M, Cesselin F (1992) Kappa-/mu-receptor interactions in the opioid control of the in vivo release of substance P-like material from rat spinal cord. Neuroscience 51:347-355.
17. Coons AH (1958) Fluorescent antibody methods. In: General cytochemical methods (Danielli JF, eds), pp 399-422. New York: Academic.
18. Corbett AD, Paterson SJ, Kosterlitz HW (1993) Selectivity of ligands for opioid receptors. In: Handbook of experimental pharmacology, Opioids I (Herz A, ed), pp 645-679. Berlin: Springer.
19. Dado RJ, Law PY, Loh HH, Elde R (1993) Immunofluorescent identification of a delta (δ)-opioid receptor on primary afferent nerve terminals. Neuroreport 5:341-344.
20. Dickenson AH, Sullivan AF, Knox R, Zajac JM, Roques BP (1987) Opioid receptor subtypes in the rat spinal cord: electrophysiological studies with μ- and δ-opioid receptor agonists in the control of nociception. Brain Res 413:36-44.
21. Dubner R, Ruda MA (1992) Activity-dependent neuronal plasticity following tissue injury and inflammation. Trends Neurosci 15:96-103.
22. Eipper BA, Mains RE (1980) Structure and biosynthesis of pro-adrenocorticotropin/endorphin and related peptides. Endocrine Rev 1:1-27.
23. Evans CJ, Keith DE, Morrison H, Magendzo K, Edwards RH (1992) Cloning of a delta opioid receptor by functional expression. Science 258:1952-1955.
24. Fields HL, Emson PC, Leigh BK, Gilbert RF, Iversen LL (1980) Multiple opiate receptors on primary afferent fibers. Nature 284:351-353.
25. Gamse R, Holzer P, Lembeck F (1979) Indirect evidence for presynaptic location of opiate receptor on chemosensitive primary sensory neurons. Naunyn-Schmiedeberg's Arch Pharmacol 308:281-285.
26. Hartman BK, Zide D, Udenfriend S (1972) The use of dopamine β-hydroxylase as a marker for the noradrenergic pathways of the central nervous system in the rat. Proc Natl Acad Sci USA 69:2722-2726.
27. Hassan AH, Ableitner A, Stein C, Herz A (1993) Inflammation of the rat paw enhances axonal transport of opioid receptors in the sciatic nerve and increases their density in the inflamed tissue. Neuroscience 55:185-195.
28. Herz A (eds) (1993) Handbook of experimental pharmacology. Opioids II. Berlin, Heidelberg: Springer.
29. Hiller JM, Zhang Y, Bing G, Gioannini TL, Stone EA, Simon EJ (1995) 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, in press.
30. Hökfelt T, Ljungdahl A, Terenius L, Eide R, Nilsson G (1977) Immunohistochemical analysis of peptide pathway possibly related to pain and analgesia. Enkephalin and Substance P. Proc Natl Acad Sci USA 74:3081-3085.
31. Holaday JW, Long JB, Tortella FC (1985) Evidence for κ, μ and δ opioid-binding site interactions in vivo. Fed Proc 44:2860-2862.
32. Hsu S-M, Raind L, Fanger H (1981) Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase technique. A comparison between ABC and unlabeled antibody (PAP) procedures. J Histochem Cytochem 29:577-580.
33. Hylden JLK, Thomas DA, Iadarola MJ, Nahin RL, Dubner R (1991) Spinal opioid analgesic effects are enhanced in a model of unilateral inflammationn/hyperalgesia: possible involvement of noradrenergic mechanisms. Eur J Pharmacol 194:135-143.
34. Iadarola MJ, Brady LS, Draisci G, Dubner R (1988) Enhancement of dynorphin gene expression in spinal cord following experimental inflammation: stimulus specificity, behavioral parameters and opioid receptor binding. Pain 35:313-326.
35. Ji RR, Zhang X, Wiesenfeld-Hallin Z, Hökfelt T (1994) Expression of neuropeptide Y and neuropeptide Y (Y1) receptor mRNA in rat spinal cord and dorsal root ganglia following peripheral tissue inflammation. J Neurosci 14:6423-6434.
36. Johnson DG, de C Nogeira Araujo GM (1981) A simple method of reducing the fading of immunofluorescence during microscopy. J Immunol Methods 43:349-350.
37. Kar S, Rees RG, Quirion R (1994) 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 6:345-354.
38. Kieffer BL, Befort K, Gaveriaux-Ruff C, Hirth CG (1992) The δ-ο-pioid receptor: isolation of a cDNA by expression cloning and pharmacological characterization. Proc Natl Acad Sci USA 89:12048-12052.
39. Lawson SN, Waddell PJ (1991) Soma neurofilament immunoreactivity is related to cell size and fiber conduction velocity in rat primary sensory neurons. J Physiol (Lond) 435:41-63.
40. Lee NM, Leybin L, Chang JK, Loh HH (1980) Opiate and peptide interaction: effect of enkephalins on morphine analgesia. Eur J Pharmacol 68:181-185.
41. Levine JD, Taiwo YO (1989) Involvement of the mu-opiate receptor in peripheral analgesia. Neuroscience 32:571-575.
42. Levine JD, Fields HL, Basbaum AI (1993) Peptides and the primary afferent fibers. J Neurosci 13:2273-2286.
43. Lewis JW, Tordoff MG, Sherman JE, Liebeskind JC (1982) Adrenal medullary enkephalin-like peptides may mediate opioid stress analgesia. Science 217:557-559.
44. Lord J, Waterfield A, Hughes J, Kosterlitz H (1977) Endogenous opioid peptides: multiple agonists and receptors. Nature 267:495-499.
45. Mansour A, Khachaturian H, Lewis ME, Akil H, Watson SJ (1988) Anatomy of CNS opioid receptors. Trends Neurosci 11:308-314.
46. Mansour A, Thompson RC, Akil H, Watson SJ (1993) Delta opioid receptor mRNA distribution in the brain: comparison to delta receptor binding and proenkephalin mRNA. J Chem Neuroanat 6:351-362.
47. Mansour A, Fox CA, Burke S, Meng F, Thompson RC, Akil H, Watson SJ (1994a) Mu, delta, and kappa opioid receptor mRNA expression in the rat CNS: an in situ hybridization study. J Comp Neurol 350: 412-438.
48. Mansour A, Fox CA, Meng F, Akil H, Watson SJ (1994b) Kappal receptor mRNA distribution in the rat CNS: comparison to kappa receptor binding and prodynorphin mRNA. Cell Mol Neurosci 5: 124-144.
49. Mansour A, Fox CA, Thompson RC, Akil H, Watson SJ (1994c) Muopioid receptor mRNA expression in the rat CNS: comparison to mureceptor binding. Brain Res 643:245-265.
50. Martin WR, Eades CG, Thompson JA, Huppler RE, Gilbert PE (1976) The effects of morphine- and nalorphine-like drugs in the nondependent and morphine-dependent chronic spinal dog. J Pharmacol Exp Ther 197:196-203.
51. Meng F, Xie GX, Thompson RC, Mansour A, Goldstein A, Watson SJ, Akil H (1993) Cloning and pharmacological characterization of a rat kappa opioid receptor. Proc Natl Acad Sci USA 90:9954-9958.
52. Millan MJ (1986) Multiple opioid systems. Pain 27:303-347.
53. Millan MJ, Millan MH, Czlonkowski A, Höllt V, Pilcher CWT, Herz A, Colpaert FC (1986) A model of chronic pain in the rat:response of multiple opioid system to adjuvant-induced arthritis. J Neurosci 6:899-906.
54. Millan MJ, Czlonkowski A, Morris B, Stein C, Arendt R, Huber A, Höllt V, Herz A (1988) 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 35:299-312.
55. Minami M, Toya T, Katao Y, Maekawa K, Nakamura S, Onogi T, Kaneko S, Satoh M (1993) Cloning and expression of a cDNA for the rat kappa-opioid receptor. FEBS Lett 329:291-295.
56. Morris BJ, Herz A (1987) Distinct distribution of opioid receptor types in rat lumbar spinal cord. Naunyn-Schmiedebergs Arch Pharmacol 336:240-243.
57. Ninkovic M, Hunt SP, Kelly JS (1981) Effect of dorsal rhizotomy on the autoradiographic distribution of opiate and neurotensin receptors and neurotensin-like immunoreactivity within the rat spinal cord. Brain Res 230:111-119.
58. Ninkovic M, Hunt SR Gleave JRW (1982) Localization of opiate and histamine H1-receptors in the primate sensory ganglia and spinal cord. Brain Res 241:197-206.
59. Noguchi K, Morita Y, Kiyama H, Sato M, Ono K, Tohyama M (1989) Preproenkephalin gene expression in the rat spinal cord after noxious stimuli. Mol Brain Res 5:227-234.
60. Noguchi K, Dubner R, De Leon M, Senba E, Ruda MA (1994) Axotomy induces preprotachykinin gene expression in a subpopulation of dorsal root ganglion neurons. J Neurosci Res 37:596-603.
61. Pasternak GW (1988) The opioid receptors, New Jersey: Humana.
62. Pease PC (1962) Buffered formaldehyde as a killing agent and primary fixative for electron microscopy. Anat Rec 142:342.
63. Platt JL, Michael AF (1983) Retardation of fading and enhancement of intensity of immunofluorescence by p-phenylenediamine. J Histochem Cytochem 31:840-842.
64. Presley RW Menetrey D, Levine JD, Basbaum AI (1990) Systemic morphine suppresses noxious-evoked Fos protein-like immunoreactivity in the rat spinal cord. J Neurosci 10:323-335.
65. Rothman RB, Holaday JW, Porreca F (1993) Allosteric coupling among opioid receptors: evidence for an opioid receptor complex. In: Handbook of experimental pharmacology, Opioids I (Herz A, ed), pp 217-237. Berlin: Springer.
66. Ruda MA, Iadarola MJ, Cohen LV, Young WSI (1988) In situ hybridization histochemistry and immunocytochemistry reveal an increase in spinal dynorphin biosynthesis in rat model of peripheral inflammation and hyperalgesia. Proc Natl Acad Sci USA 85:622-626.
67. Schultzberg M, Lundberg JM, Hökfelt T, Terenius L, Brandt J, Eide RP, Goldstein M (1978) Enkephalin-like immunoreactivity in gland cells and nerve terminals of the adrenal medulla. Neuroscience 3:1169-1186.
68. Schäfer M-H, Nohr D, Krause JE, Weihe E (1993) Localization of kappa-opioid receptor mRNA in neuronal subpopulations of rat sensory ganglia and spinal cord. Neurosci Lett 167:137-140.
69. Simon EJ, Gioannini TL (1993) Opioid receptor multiplicity: isolation, purification, and chemical characterization of binding sties. In: Handbook of experimental pharmacology, Opioids I (Herz A, eds), pp 3-26. Berlin: Springer.
70. Smith JR, Simon EJ (1980) Selective protection of sterospecific enkephalin and opiate binding against inactivation by N-ethylmaleimide: Evidence for two classes of opiate receptors. Proc Natl Acad Sci USA 77:281-284.
71. Standifier KM, Chien C-C, Wahlested C, Brown GP, Pasternak GW (1994) Selective loss of 8 opioid analgesia and binding by antisense oligodeoxynucleotides to a δ opioid receptor. Neuron 12:805-810.
72. Stanfa LC, Sullivan AF, Dickenson AH (1992) Alterations in neuronal excitability and the potency of spinal mu, delta and kappa opioids after carrageenan-induced inflammation. Pain 50:345-354.
73. Stein C, Gramsch C, Herz A (1990a) Intrinsic mechanisms of antinociception in inflammation: local opioid receptors and β-endorphin. J Neurosci 10:1292-1298.
74. Stein C, Hassan AH, Przewxocki R, Gramsch C, Peter K, Herz A (1990b) Opioids from immunocytes interact with receptors on sensory nerves to inhibit nociception in inflammation. Proc Natl Acad Sci USA 87:5935-5939.
75. Stein C, Millan MJ, Shippenberg TS, Peter K, Herz A (1989) Peripheral opioid receptors mediating antinociception in inflammation. Evidence for involvement of mu, delta and kappa receptors. J Pharmacol Exp Ther 248:1269-1275.
76. Stevens CW, Kajander KC, Bennett GJ, Seybold VS (1991a) Bilateral and differential changes in spinal mu, delta, and kappa opioid binding in rats with a painful, unilateral neuropathy. Pain 46:315-326.
77. Stevens CW, Lacey CB, Miller KE, Eide RP, Seybold VS (1991b) Biochemical characterization and regional quantification of μ, δ and κ opioid binding sites in rat spinal cord. Brain Res 550:77-85.
78. Terenius L (1984) Approaches to neuropeptide and, in particular, endorphin measurements. In: Frontiers in biochemical and pharmacological research in depression (Usdin E, eds), pp 35-43. New York: Raven.
79. Thompson RC, Mansour A, Akil H, Watson SJ (1993) Cloning and phamacological characterization of a rat μ opioid receptor. Neuron 11:903-913.
80. Vaught JL, Takemori AE (1979) Differential effects of leucine enkephalin and methionine enkephalin on morphine-induced analgesia, acute tolerance and dependence. J Pharmacol Exp Ther 208:86-90.
81. Viveros OH, Diliberto JEJ, Hazem E, Chang K-J (1979) Opiate-like materials in the adrenal medulla: evidence for storage and secretion with catecholamines. Mol Pharmacol 16:1101-1108.
82. Wall PD, Devor M (1981) The effect of peripheral nerve injury on dorsal root potentials and on transmission of afferent signals into the spinal cord. Brain Res 209:95-111.
83. Wall PD, Devor R, Inbal JW, Scadding D, Schonfeld Z, Seltzer Z, Tomkiewitz MM (1979) Autotomy following peripheral nerve lesions: experimental anaesthesia dolorosa. Pain 7:103-113.
84. Wang JB, Imai Y, Eppler CM, Gregor P, Spivak CE, UhI GR (1993) μ Opiate receptor: cDNA cloning and expression. Proc Natl Acad Sci USA 90:10230-10234.
85. Weihe E, Nohr D, Millan MJ, Stein C, Muller S, Gramsch C, Herz A (1988) Peptide neuroanatomy of adjuvant-induced arthritic inflammation in rat. Agents Actions 25:255-259.
86. Willis WD Jr, Coggeshall RE (1991) Sensory mechanisms of the spinal cord. New York: Plenum.
87. Yasuda K, Raynor K, Kong H, Breder CD, Takeda J, Reisine T, Bell GI (1993) Cloning and functional comparison of κ and δ opioid receptors from mouse brain. Proc Natl Acad Sci USA 90:6736-6740.
88. Young WSI, Wamsley JK, Zarbin MA, Kuhar MJ (1980) Opioid receptors undergo axonal flow. Science 210:76-78.
89. Zamboni L, De Martino C (1967) Buffered picric acid formaldehyde: a new rapid fixative for electron microscopy. J Cell Biol 148A:35.
90. Zarbin MA, Wamsley JK, Kuhar MJ (1990) Anterograde transport of opioid receptors in rat vagus nerves and dorsal roots of spinal nerves: pharmacology and sensitivity to sodium and guanine nucleotides. Exp Brain Res 81:267-278.
91. Zhang X, Bao L, Xu ZQ, Jutta K, Arvidsson U, Eide R, Hökfelt T (1994a) Differential transport of Y1 receptors: a specific distribution of Y1 receptors on somatic plasmalemma of small neurons in rat lumbar DRGs. Proc Natl Acad Sci USA 91:11738-11442.
92. Zhang X, Wiesenfeld-Hallin Z, Hökfelt T (1994b) Effect of peripheral axotomy on expression of neuropeptide Y (Y1) receptor mRNA in rat lumbar dorsal root ganglia. Eur J Neurosci 6:43-57.
93. Zimmermann M (1983) Ethical guidelines for investigations of experimental pain in conscious animals. Pain 16:109-110.