Endogenous opioid peptides acting at μ-opioid receptors in the dorsal horn contribute to midbrain modulation of spinal nociceptive neurons

Journal of Neurophysiology

Volumn 79, Issue 2, 1998, Pages 677-687

  Budai, Dénes ^a,b   Fields, Howard L ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

KAINIC ACID; MU OPIATE RECEPTOR; N METHYL DEXTRO ASPARTIC ACID;

ANALGESIA; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN STEM; INTERNEURON; IONTOPHORESIS; MALE; MESENCEPHALON; NOCICEPTION; NONHUMAN; PAIN THRESHOLD; PRIORITY JOURNAL; RAT; RECEPTOR BINDING; SPINAL CORD DORSAL HORN;

EID: 0031882905     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.1998.79.2.677     Document Type: Article

References (75)

1. AIMONE, L. D. AND GEBHART, G. F. Stimulation-produced spinal inhibition from the midbrain in the rat is mediated by an excitatory amino acid neurotransmitter in the medial medulla. J. Neurosci. 6: 1803-1813, 1986.
2. AIMONE, L. D., JONES, S. L., AND GEBHART, G. F. Stimulation-produced descending inhibition from the periaqueductal gray and nucleus raphe magnus in the rat: mediation by spinal monoamines but not opioids. Pain 31: 123-136, 1987.
3. ARVIDSSON, U., DADO, R. J., RIEDL, M., LEE, J. H., LAW, P. Y., LOH, H. H., ELDE, R., AND WESSENDORF, M. W. Delta-opioid receptor immunoreactivity: distribution in brainstem and spinal cord, and relationship to biogenic amines and enkephalin. J. Neurosci. 15: 1215-1235, 1995a.
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., AND ELDE, R. Distribution and targeting of a mu-opioid receptor (MOR1 ) in brain and spinal cord. J. Neurosci. 15: 3328-3341, 1995b.
5. BASBAUM, A. I., CLANTON, C. H., AND FIELDS, H. L. Three bulbospinal pathways from the rostral medulla of the cat: An autographic study of pain modulating systems. J. Comp. Neurol. 178: 209-224, 1978.
6. BASBAUM, A. I. AND FIELDS, H. L. Endogenous pain control systems: Brainstem spinal pathways and endorphin circuitry. Annu. Rev. Neurosci. 7: 309-338, 1984.
7. BESSE, D., LOMBARD, M. C., AND BESSON, J. M. Autoradiographic distribution of mu, delta and kappa opioid binding sites in the superficial dorsal horn, over the rostrocaudal axis of the rat spinal cord. Brain Res. 548: 287-291, 1991.
8. BESSE, D., LOMBARD, M. C., AND BESSON, J. M. Time-related decreases in mu and delta opioid receptors in the superficial dorsal horn of the rat spinal cord following a large unilateral dorsal rhizotomy. Brain Res. 578: 115-127, 1992a.
9. 3H]DTLET opioid binding sites in laminae I-II of the spinal cord in intact and deafferented morphine-tolerant rats. Neurosci Lett. 136: 209-212, 1992b.
10. BOURGOIN, S., LE BARS, D., CLOT, A. M., HAMON, M., AND CESSELIN, F. Spontaneous and evoked release of met-enkephalin-like material from the spinal cord of arthritic rats in-vivo. Pain 32: 107-114, 1988.
11. BUDAI, D. A computer-controlled system for post-stimulus time histogram and wind-up studies. J. Neurosci. Methods 51: 205-211, 1994.
12. CARSTENS, E., CULHANE, E. S., AND BANISADR, R. Partial involvement of monoamines and opiates in the inhibition of rat spinal nociceptive neurons evoked by stimulation in midbrain periaqueductal gray or lateral reticular formation. Brain Res. 522: 7-13, 1990.
13. CARSTENS, E., GUINAN, M. J., AND MACKINNON, J. D. Naloxone does not consistently affect inhibition of spinal nociceptive transmission produced by medial diencephalic stimulation in the cat. Neurosci Lett. 42: 71-76, 1983.
14. CARSTENS, E., KLUMPP, D., AND ZIMMERMANN, M. The opiate antagonist, naloxone, does not affect descending inhibition from midbrain of nociceptive spinal neuronal discharges in the cat. Neurosci. Lett. 11: 323-327, 1979.
15. CHENG, P. Y., MORIWAKI, A., WANG, J. B., UHL, G. R., AND PICKEL, V. M. Ultrastructural localization of μ-opioid receptors in the superficial layers of the rat cervical spinal cord: extrasynaptic localization and proximity to Leu5-enkephalin. Brain Res. 731: 141-154, 1996.
16. CHO, H. J. AND BASBAUM, A. I. Arborization of single axons of the spinal dorsolateral funiculus to the contralateral superficial dorsal horn. Brain Res. 477: 344-349, 1989a.
17. CHO, H. J. AND BASBAUM, A. I. Ultrastructural analysis of dynorphin B-immunoreactive cells and terminals in the superficial dorsal horn of the deafferented spinal cord of the rat. J. Comp. Neurol. 281: 193-205. 1989b.
18. COLLIN, E., BOURGOIN, S., MANTELET, S., HAMON, M., AND CESSELIN, F. Feedback inhibition of met-enkephalin release from the rat spinal cord in vivo. Synapse 11: 76-84, 1992.
19. DADO, R. J., LAW, P. Y., LOH, H. H., AND ELDE, R. Immunofluorescent identification of a delta (delta)-opioid receptor on primary afferent nerve terminals. Neuroreport 5: 341-344, 1993.
20. DINGLEDINE, R., IVERSEN, L. L., AND BREUKER, E. Naloxone as a GABA antagonist: evidence from iontophoretic, receptor binding and convulsant studies. Eur. J. Pharmacol. 47: 19-27, 1978.
21. DOSTROVSKY, J. O., SHAH, Y., AND GRAY, B. G. Descending inhibitory influences from periaqueductal gray, nucleus raphe magnus, and adjacent reticular formation. II. Effects on medullary dorsal horn nociceptive and nonnociceptive neurons. J. Neurophysiol. 49: 948-960, 1983.
22. DUGGAN, A. W. AND GRIERSMITH, B. T. Inhibition of the spinal transmission of nociceptive information by supraspinal stimulation in the cat. Pain 6: 149-161, 1979.
23. FANG, F. AND PROUDFTT, H. K. Spinal cholinergic and monoamine receptors mediate the antinociceptive effect of morphine microinjected in the periaqueductal gray on the rat tail, but not the feet. Brain Res. 722: 95-108, 1996.
24. FIELDS, H. L. AND BASBAUM, A. I. Brainstem control of spinal pain-transmission neurons. Annu. Rev. Physiol. 40: 217-248, 1978.
25. FIELDS, H. L., EMSON, P. C., LEIGH, B. K., GILBERT, R. F., AND IVERSEN, L. L. Multiple opiate receptor sites on primary afferent fibres. Nature 284: 352-353, 1980.
26. FIELDS, H. L., HEINRICHER, M. M., AND MASON, P. Neurotransmitters in nociceptive modulatory circuits. Annu. Rev. Neurosci. 14: 219-245, 1991.
27. FIELDS, H. L., MALICK, A., AND BURSTEIN, R. Dorsal horn projection targets of ON and OFF Cells in the rostral ventromedial medulla. J. Neurophysiol. 14: 1742-1759, 1995.
28. GLAUM, S. R., MILLER, R. J., AND HAMMOND, D. L. Inhibitory actions of delta 1-, delta 2-, and mu-opioid receptor agonists on excitatory transmission in lamina II neurons of adult rat spinal cord. J. Neurosci. 14: 4965-4971, 1994.
29. GLAZER, E. J. AND BASBAUM, A. I. Immunohistochemical localization of leucine-enkephalin in the spinal cord of the cat: enkephalin-containing marginal neurons and pain modulation. J. Comp. Neurol. 196: 377-389, 1984.
30. GOLDSTEIN, A. AND NAIDU, A. Multiple opioid receptors: ligand selectivity profiles and binding site signatures. Mol. Pharmacol. 36: 265-272, 1989.
31. GRUDT, T. J. AND WILLIAMS, J. T. mu-Opioid agonists inhibit spinal trigeminal substantia gelatinosa neurons in guinea pig and rat. J. Neurosci. 14: 1646-1654, 1994.
32. 2 (CTOP) in mice. Eur. J. Pharmacol. 150: 355-360, 1988.
33. HENRY, J. L. Naloxone excites nociceptive units in the lumbar dorsal horn of the spinal cat. Neuroscience 4: 1485-1491, 1979.
34. HOPE, P. J., FLEETWOOD-WALKER, S. M., AND MITCHELL, R. Distinct antinociceptive actions mediated by different opioid receptors in the region of lamina I and laminae III-V of the dorsal horn of the rat. Brit. J. Pharmacol. 101: 477-483, 1990.
35. JEFTINIJA, S. Enkephalins modulate excitatory synaptic transmission in the superficial dorsal horn by acting at mu-opioid receptor sites. Brain Res. 460: 260-268, 1988.
36. JENSEN, T. S. AND YAKSH, T. L. Spinal monoamine and opiate systems partly mediate the antinociceptive effects produced by glutamate at brainstem sites. Brain Res. 321: 287-297, 1984.
37. JONES, S. L., SEDIVEC, M. J., AND LIGHT, A. R. Effects of iontophoresed opioids on physiologically characterized laminae I and II dorsal horn neurons in the cat spinal cord. Brain Res. 532: 160-174, 1990.
38. KIM, K.-W. AND Cox, B. M. Inhibition of norepinephrine release from rat cortex slices by opioids: differences among agonists in sensitivities to antagonists suggest receptor heterogeneity. J. Pharm. Exp. Ther. 267: 1153-1160, 1993.
39. KRAMER, T. H., SHOOK, J. E., KAZMIERSKI, W., AYRES, E. A., WIRE, W. S., HRUBY, V. J., AND BURKS, T. F. Novel peptidic mu opioid antagonists: Pharmacologic characterization in vitro and in vivo. J. Pharm. Exp. Ther. 249: 544-551, 1989.
40. LIGHT, A. R. The Initial Processing of Pain and its Descending Control: Spinal and Trigeminal Systems. Basel: Krager, 1992.
41. LOMBARD, M. C. AND BESSON, J. M. Electrophysiological evidence for a tonic activity of the spinal cord intrinsic opioid systems in a chronic pain model. Brain Res. 477: 48-56, 1989.
42. MACDONALD, R. L. AND NELSON, P. G. Specific opiate-induced depression of transmitter release from dorsal root ganglion cells in culture. Science 199: 1449-1451, 1978.
43. MANSOUR, A., FOX, C. A., BURKE, S., AKIL, H., AND WATSON, S. J. Immunohistochemical localization of the cloned mu opioid receptor in the rat CNS. J. Chem. Neuroanat. 8: 283-305, 1995.
44. MANSOUR, A., FOX, C. A., THOMPSON, R. C., AKIL, H., AND WATSON, S. J. mu-Opioid receptor mRNA expression in the rat CNS: comparison to mu-receptor binding. Brain Res. 643: 245-265, 1994.
45. 0-type GTP-binding protein. J. Neurosci. 14: 3842-3851, 1994.
46. MOKHA, S. S. Differential influence of naloxone on the responses of nociceptive neurons in the superficial versus the deeper dorsal horn of the medulla in the rat. Pain 49: 405-413, 1992.
47. MORGAN, M. M., GOLD, M. S., LIEBESKIND, J. C., AND STEIN, C. Periaqueductal gray stimulation produces a spinally mediated, opioid antinociception for the inflamed hindpaw of the rat. Brain Res. 545: 17-23, 1991.
48. MUDGE, A. W., LEEMAN, S. E., AND FISCHBACH, G. D. Enkephalin inhibits release of substance P from sensory neurons in culture and decreases action potential duration. Proc. Natl. Acad. Sci. USA. 76: 526-530, 1979.
49. OMOTE, K., KITAHATA, L. M., COLLINS, J. G., NAKATANI, K., AND NAKAOAWA, I. The antinociceptive role of mu- and delta-opiate receptors and their interactions in the spinal dorsal horn of cats. Anesth. Analg. 71: 23-28, 1990.
50. OSSIPOV, M. H., KOVELOWSKI, C. J., WHEELER-ACETO, H., COWAN, A., HUNTER, J. C., LAI, J., MALAN, T. P., JR., AND PORRECA, F. Opioid antagonists and antisera to endogenous opioids increase the nociceptive response to formalin: demonstration of an opioid kappa and delta inhibitory tone. J. Pharmacol. Exp. Ther. 277: 784-788, 1996.
51. PAXINOS, G. AND WATSON, C. The Rat Brain in Stereotaxic Coordinates. New York: Academic, 1986.
52. RANDIC, M., CHENG, G., AND KOJIC, L. Kappa-opioid receptor agonists modulate excitatory transmission in substantia gelatinosa neurons of the rat spinal cord. J. Neurosci. 15: 6809-6826, 1995.
53. REN, K., RANDICH, A., AND GEBHART, G. F. Spinal serotonergic and kappa opioid receptors mediate facilitation of the tail flick reflex produced by vagal afferent stimulation. Pain 45: 321-329, 1991.
54. RIVOT, J. P., CHAOUCH, A., AND BESSON, J. M. The influence of naloxone on the C fiber response of dorsal horn neurons and their inhibitory control by raphe magnus stimulation. Brain Res. 176: 355-364, 1979.
55. ROYCHOWDHURY, S. M. AND FIELDS, H. L. Endogenous opioids acting at a medullary mu-opioid receptor contribute to the behavioral antinociception produced by GABA antagonism in the midbrain periaqueductal grey. Neuroscience 74: 863-872, 1996.
56. RUDA, M. A. Opiates and pain pathways: demonstration of enkephalin synapses on dorsal horn projection neurons. Science 215: 1523-1525, 1982.
57. RUDA, M. A., COFFIELD, J., AND DUBNER, R. Demonstration of postsynaptic opioid modulation of thalamic projection neurons by the combined techniques of retrograde horseradish peroxidase and enkephalin immunocytochemistry. J. Neurosci. 4: 2117-2132, 1984.
58. A receptors in the midbrain periaqueductal gray abolishes nociceptive spinal dorsal horn neuronal activity. Eur. J. Pharmacol. 160: 163-166, 1989.
59. SANDKUHLER, J., WILLMANN, E., AND FU, Q. G. Characteristics of midbrain control of spinal nociceptive neurons and nonsomatosensory parameters in the pentobarbital-anesthetized rat. J. Neurophysiol. 65: 33-48, 1991.
60. SESSLE, B. J. AND HU, J. W. Raphe-induced suppression of the jaw-opening reflex and single neurons in trigeminal subnucleus oralis, and influence of naloxone and subnucleus caudalis. Pain 10: 19-36, 1981.
61. SHEN, Q., PENG, Y. B., REES, H., AND WILLIS, W. D. Naloxone reduces the ventral periaqueductal gray-induced inhibition of dorsal horn neurons in rats. Soc. Neurosci. Abstr. 22: 1364, 1996.
62. TADDESE, A., NAH, S. Y., AND MCCLESKEY, E. W. Selective opioid inhibition of small nociceptive neurons. Science 270: 1366-1369, 1995.
63. TANG, R., STOCKMAN, R., CAMARA, A., FUJIMOTO, J. M., AND TSENG, L. F. Brainstem sites sensitive to beta endorphin and morphine for analgesia and spinal release of methionine enkephalin in anesthetized rats (Abstract). FASEB J. 3: A422, 1989.
64. TORTORICI, V., VÁSQUEZ, E., AND VANEGAS, H. Naloxone partial reversal of the antinociception produced by dipyrone microinjected into the periaqueductal gray of rats. Possible involvement of medullary off- and on-cells. Brain Res. 725: 106-110, 1996.
65. TSENG, L. F. AND TANG, R. Differential actions of the blockade of spinal opioid, adrenergic and serotonergic receptors on the tail-flick inhibition induced by morphine microinjected into dorsal raphe and central gray in rats. Neuroscience 33: 93-100, 1989.
66. WANG, Z., BILSKY, E. J., PORRECA, F., AND SADEE, W. Constitutive mu opioid receptor activation as a regulatory mechanism underlying narcotic tolerance and dependence. Life Sci. 54: 339-350, 1994.
67. WANG, L. AND GINTZLER, A. R. Bimodal opioid regulation of cyclic AMP formation: implications for positive and negative coupling of opiate receptors to adenylyl cyclase. J. Neurochem. 63: 1726-1730, 1994.
68. WANG, X.-M. AND MOKHA, S. S. Opioids modulate N-methyl-D-aspartic acid (NMDA)-evoked responses of trigeminothalamic neurons. J. Neurophysiol. 76: 2093-2096, 1996.
69. WERZ, M. A., GREGA, D. S., AND MACDONALD, R. L. Actions of mu, delta and kappa opioid agonists and antagonists on mouse primary afferent neurons in culture. J. Pharmacol. Exp. Ther. 243: 258-263, 1987.
70. WILLCOCKSON, W. S., KIM, J., SHIN, H. K., CHUNG, J. M., AND WILLIS, W. D. Actions of opioids on primate spinothalamic tract neurons. J. Neurosci. 6: 2509-2520, 1986.
71. WILLIS, W. D. AND COGGESHALL, R. E. Sensory Mechanisms of the Spinal Cord. (2nd ed.). New York: Plenum, 1991.
72. YAKSH, T. L. AND CHIPKIN, R. E. Studies on the effect of SCH-34826 and thiorphan on [methionine] enkephalin levels and release in rat spinal cord. Eur. J. Pharmacol. 167: 367-374, 1989.
73. YOSHIMURA, M. AND NORTH, R. A. Substantia gelatinosa neurones hyperpolarized in vitro by enkephalin. Nature 305: 529-530, 1983.
74. ZHANG, K.-M., WANG, X.-M., AND MOKHA, S. S. Opioids modulate N-methyl-D-aspartic acid (NMDA)-evoked responses of neurons in the superficial and deeper dorsal horn of the medulla (trigeminal nucleus caudalis). Brain Res. 719: 223-229, 1996.
75. ZORMAN, G., BELCHER, G., ADAMS, J. E., AND FIELDS, H. L. Lumbar intrathecal naloxone blocks analgesia produced by microstimulation of the ventromedial medulla in the rat. Brain Res. 236: 77-84, 1982.