Opioid-mediated regulation of A11 diencephalospinal dopamine neurons: Pharmacological evidence of activation by morphine

Neuropharmacology

Volumn 61, Issue 4, 2011, Pages 614-621

  Pappas, Samuel S ^a   Kennedy, Tom ^b   Goudreau, John L ^b,c   Lookingland, Keith J ^a,b  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b MICHIGAN STATE UNIVERSITY   (United States)

^c Michigan State University   (United States)

Author keywords

opioids; A11; Diencephalospinal; Dopamine; Morphine; Spinal cord

Indexed keywords

3,4 DIHYDROXYPHENYLACETIC ACID; DOPAMINE; MORPHINE SULFATE; MU OPIATE RECEPTOR; NALOXONE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIENCEPHALON; DOPAMINERGIC NERVE CELL; DOSE RESPONSE; DRUG MEGADOSE; FEMALE; LUMBAR SPINAL CORD; MALE; MOUSE; NERVE CELL STIMULATION; NERVE ENDING; NONHUMAN; PRIORITY JOURNAL; RECEPTOR BLOCKING; REGULATORY MECHANISM; SPINAL CORD NERVE CELL; THORACIC SPINAL CORD;

3,4-DIHYDROXYPHENYLACETIC ACID; ANALGESICS, OPIOID; ANIMALS; BRAIN; DIENCEPHALON; DOPAMINE; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; MALE; MICE; MORPHINE; NEURONS; SPINAL CORD;

EID: 79960021751     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2011.05.002     Document Type: Article

References (85)

1. Z.B. Andrews, and D.R. Grattan Opioid receptor subtypes involved in the regulation of prolactin secretion during pregnancy and lactation J. Neuroendocrinol. 15 2003 227 236 (Pubitemid 36266889)
2. B. Attali, D. Saya, and Z. Vogel Kappa-opiate agonists inhibit adenylate cyclase and produce heterologous desensitization in rat spinal cord J. Neurochem. 52 1989 360 369 (Pubitemid 19037597)
3. S. Barasi, and N. Duggal The effect of local and systemic application of dopaminergic agents on tail flick latency in the rat Eur. J. Pharmacol. 117 3 1985 287 294 (Pubitemid 16208092)
4. H. Barbeau, and S. Rossignol Initiation and modulation of the locomotor pattern in the adult chronic spinal cat by noradrenergic, serotonergic, and dopaminergic drugs Brain Res. 546 1991 250 260
5. A.C. Barrett, E.S. Smith, and M.J. Picker Sex-related differences in mechanical nociception and antinociception produced by mu- and kappa-opioid receptor agonists in rats Eur. J. Pharmacol. 452 2002 163 173 (Pubitemid 35283927)
6. G. Barriere, N. Mellen, and J.R. Cazalets Neuromodulation of the locomotor network by dopamine in the isolated spinal cord of newborn rat Eur. J. Neurosci. 19 2004 1325 1335 (Pubitemid 38387209)
7. G. Barriere, J.R. Cazalets, B. Bioulac, F. Tison, and I. Ghorayeb The restless legs syndrome Prog. Neurobiol. 77 2005 139 165 (Pubitemid 41677621)
8. A.I. Basbaum, F. Godefroy, and J. Weil-Fugazza A new microdissection technique for regional biochemical analysis of the rat spinal cord: serotonin, norepinephrine, dopamine, and uric acid Brain Res. 419 1987 229 238 (Pubitemid 17153414)
9. D. Besse, M.C. Lombard, J.M. Zajac, B.P. Roques, and J.M. Besson Pre- and postsynaptic distribution of mu, delta, and kappa opioid receptors in the superficial layers of the cervical dorsal horn of the rat spinal cord Brain Res. 521 1-2 1990 15 22 (Pubitemid 20208729)
10. D. Besse, M.C. Lombard, and J.M. Besson 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 1-2 1991 287 291
11. A. Bergerot, R.J. Storer, and P.J. Goadsby Dopamine inhibits trigeminovascular transmission in the rat Ann. Neurol. 61 2007 251 262 (Pubitemid 46557349)
12. A. Bjorklund, and G. Skagerberg Evidence for a major spinal cord projection from the diencephalic A11 dopamine cell group in the rat using transmitter-specific fluorescent retrograde tracing Brain Res. 177 1979 170 175 (Pubitemid 10249887)
13. E.M. Brown, R.J. Carroll, and G.D. Aurbach Dopaminergic stimulation of cyclic AMP accumulation and parathyroid hormone release from dispersed bovine parathyroid cells Proc. Natl. Acad. Sci. U.S.A. 74 10 1977 4210 4213 (Pubitemid 8228383)
14. P. Callahan, M.H. Baumann, and J. Rabii Inhibition of tuberoinfundibular dopaminergic neural activity during suckling: involvement of mu and kappa opiate receptor subtypes J. Neuroendocrinol. 8 1996 771 776 (Pubitemid 26331801)
15. A.R. Charbit, S. Akerman, P.R. Holland, and P.J. Goadsby Neurons of the dopaminergic/calcitonin gene-related peptide A11 cell group modulate neuronal firing in the trigeminocervical complex: an electrophysiological and immunohistochemical study J. Neurosci. 29 40 2009 12532 12541
16. T.J. Cicero, B. Nock, and E.R. Meyer Sex-related differences in morphine's antinociceptive activity: relationship to serum and brain morphine concentrations J. Pharmacol. Exp. Ther. 282 1997 939 944 (Pubitemid 27340198)
17. A.R. Cools, and J.M. Van Rossum Excitation-mediating and inhibition-mediating dopamine-receptors: a new concept towards a better understanding of electrophysiological, biochemical, pharmacological, functional and clinical data Psychopharmacologia 45 3 1976 243 254
18. J.W. Commissiong, C.L. Galli, and N.H. Neff Differentiation of dopaminergic and noradrenergic neurons in rat spinal cord J. Neurochem. 30 1978 1095 1099 (Pubitemid 8367697)
19. J.W. Commissiong Mass fragmentographic analysis of monoamine metabolites in the spinal cord of rat after the administration of morphine J. Neurochem. 41 1983 1313 1318 (Pubitemid 14228949)
20. M. Connor, and M.J. Christie Opioid receptor signaling mechanisms Clin. Exp. Pharmacol. Physiol. 26 1999 493 499
21. P. De Camilli, D. Macconi, and A. Spada Dopamine inhibits adenylate cyclase in human prolactin-secreting pituitary adenomas Nature 278 5701 1979 252 254 (Pubitemid 9129071)
22. S.N. Deyo, R.M. Swift, and R.J. Miller Morphine and endorphins modulate dopamine turnover in rat median eminence Proc. Natl. Acad. Sci. U. S. A. 76 6 1979 3006 3009 (Pubitemid 10245222)
23. G. Di Chiara, and A. Imperato Drugs abused by humans preferentially increase synaptic dopamine concentration in the mesolimbic system of freely moving rats Proc. Natl. Acad. Sci. U. S. A. 85 1988 5274 5278
24. C.C. Felder, P.A. Jose, and J. Axelrod The dopamine-1 agonist, SKF 82526, stimulates phospholipase-C activity independent of adenylate cyclase J. Pharmacol. Exp. Ther. 248 1 1989 171 175 (Pubitemid 19063485)
25. S.M. Fleetwood-Walker, and J.H. Coote Contribution of noradrenaline-, dopamine-, and adrenaline-containing axons to the innervation of different regions of the spinal cord of the cat Brain Res. 206 1981 95 106 (Pubitemid 11143577)
26. S.M. Fleetwood-Walker, P.J. Hope, and R. Mitchell Antinociceptive actions of descending dopaminergic tracts on cat and rat dorsal horn somatosensory neurons J. Physiol. 399 1988 335 348
27. X. Gao, Y. Zhang, and G. Wu Effects of dopaminergic agents on carrageenan hyperalgesia after intrathecal administration to rats Eur. J. Pharmacol. 418 1-2 2001 73 77 (Pubitemid 32378812)
28. L. Garau, S. Govoni, E. Stefanini, M. Trabucchi, and P.F. Spano Dopamine receptors: pharmacological and anatomical evidences indicate that two distinct dopamine receptor populations are present in rat striatum Life Sci. 23 17-18 1978 1745 1750 (Pubitemid 9062538)
29. F. Giuliano, J. Allard, O. Rampin, S. Droupy, G. Benoit, L. Alexandre, and J. Bernabe Spinal proerectlie effect of apomorphine in the anesthetized rat Int. J. Impot. Res. 13 2001 11 115
30. F. Giuliano, J. Allard, O. Rampin, S. Droupy, G. Benoit, L. Alexandre, and J. Bernabe Pro-erectile effect of systemic apomorphine: existence of a spinal site of action J. Urol. 167 2002 402 406 (Pubitemid 34024593)
31. C. Gouarderes, and J. Cros Opioid binding sites in different levels of rat spinal cord Neuropeptides 5 1-3 1984 113 116 (Pubitemid 15160659)
32. C. Gouarderes, J. Cros, and R. Quirion Autoradiographic localization of mu, delta and kappa opioid receptor binding sites in rat and guinea pig spinal cord Neuropeptides 6 4 1985 331 342 (Pubitemid 15021861)
33. G.A. Gudelsky, E. Passaro, and H.Y. Meltzer Delayed activation of tuberoinfundibular dopamine neurons and suppression of prolactin secretion in the rat after morphine administration J. Pharmacol. Exp. Ther. 236 3 1986 641 645 (Pubitemid 16080060)
34. J.T. Haskins, G.A. Gudelsky, R.L. Moss, and J.C. Porter Iontophoresis of morphine into the arcuate nucleus: effects on dopamine concentrations in hypophysial portal plasma and serum prolactin concentrations Endocrinology 108 3 1981 767 771 (Pubitemid 11142253)
35. R.H. Hasue, and S.J. Shammah-Lagnado Origin of the dopaminergic innervation of the central extended amygdala and accumbens shell: a combined retrograde tracing and immunohistochemical study in the rat J. Comp. Neurol. 454 1 2002 15 33 (Pubitemid 35278452)
36. M. Herkeham, and C.B. Pert In vitro autoradiography of opiate receptors in rat brain suggests loci of "opiatergic" pathways Proc. Natl. Acad. Sci. U. S. A. 77 9 1980 5532 5536 (Pubitemid 11249679)
37. J.C. Holstege, H. VanDijken, R.M. Buijs, H. Goedknegt, T. Gosens, and C.M.H. Bongers Distribution of dopamine immunoreactivity in rat, cat, and monkey spinal cord J. Comp. Neurol. 376 1996 631 652 (Pubitemid 27009845)
38. K. Ikeda, T. Kobayashi, T. Kumanishi, R. Yano, I. Sora, and H. Niki Molecular mechanisms of analgesia induced by opioids and ethanol: is the GIRK channel one of the keys? Neurosci. Res. 44 2002 121 131 (Pubitemid 38365954)
39. K. Iwatsubo, and D.H. Clouet Effects of morphine and haloperidol on the electrical activity of rat nigrostriatal neurons J. Pharmacol. Exp. Ther. 202 2 1977 429 436 (Pubitemid 8168206)
40. T.S. Jensen, and T.L. Yaksh Effects of an intrathecal dopamine agonist, apomorphine on thermal and chemical evoked noxious responses in rats Brain Res. 296 1984 285 293 (Pubitemid 14161603)
41. S.W. Johnson, and R.A. North Opioids excite dopamine neurons by hyperpolarization of local interneurons J. Neurosci. 12 1992 483 488
42. F. Karoum, R.J. Wyatt, and E. Costa A comparative study on the effects of morphine on central, peripheral, and ganglionic stores of catecholamines J. Pharmacol. Exp. Ther. 216 2 1981 321 328 (Pubitemid 11130191)
43. J.W. Kebabian, and D.B. Calne Multiple receptors for dopamine Nature 277 5692 1979 93 96 (Pubitemid 9093798)
44. J.W. Kebabian, and P. Greengard Dopamine-sensitive adenyl cyclase: possible role in synaptic transmission Science 174 16 1971 1346 1349
45. C.S. Konkoy, and S.R. Childers Dynorphin-selective inhibition of adenylyl cyclase in guinea pig cerebellum membranes Mol. Pharmacol. 36 1989 627 633 (Pubitemid 19273840)
46. M.G. Lacey, N.B. Mercuri, and R.A. North Dopamine acts on D2 receptors to increase potassium conductance in neurones of the rat substantia nigra zona compacta J. Physiol. 392 1987 397 416 (Pubitemid 18014315)
47. S. Lahlou, P. Peteijean, G. Pellissier, P. Mouchet, C. Feuerstein, and P. Demenge Rostrocaudal localization of cardiovascular responses induced by intrathecal administration of apomorphine in conscious, freely moving rats J. Cardiovasc. Pharmacol. 16 1990 331 337 (Pubitemid 20222657)
48. M.E. Lajiness, C.L. Chio, and R.M. Huff D2 dopamine receptor stimulation of mitogenesis in transfected Chinese hamster ovary cells: relationship to dopamine stimulation of tyrosine phosphorylation J. Pharmacol. Exp. Ther. 267 3 1993 1573 1581 (Pubitemid 24068737)
49. B. Levant, and K.E. McCarson D3 dopamine receptors in rat spinal cord: implications for sensory and motor function Neurosci. Lett. 303 2001 9 12 (Pubitemid 32285455)
50. M.E. Lewis, H. Khachaturian, and S.J. Watzon Comparative distribution of opiate receptors and three opioid peptide neuronal systems in rhesus monkey central nervous system Life Sci. 33 Suppl. 1 1983 239 242 (Pubitemid 14209258)
51. S.E. Lindley, J.W. Gunnet, K.J. Lookingland, and K.E. Moore 3,4-Dihydroxyphenylacetic acid concentrations in the intermediate lobe and neural lobe of the posterior pituitary gland as an index of tuberohypophysial dopaminergic neuronal activity Brain Res. 506 1 1990 133 138 (Pubitemid 20020085)
52. H.H. Loh, and A.P. Smith Annu. Rev. Pharmacol. Toxicol. 30 1990 123 147
53. K.J. Lookingland, and K.E. Moore Differential effects of morphine on the rates of dopamine turnover in the neural and intermediate lobes of the rat pituitary gland Life Sci. 37 13 1985 1225 1229 (Pubitemid 16243147)
54. K.J. Lookingland, and K.E. Moore Functional neuroanatomy of hypothalamic dopaminergic neuroendocrine systems S.B. Dunnet, Handbook of Chemical Neuroanatomy vol. 21 2005 Elsevier Amsterdam 435 523
55. M.D. Loose, and M.J. Kelly Opioids act at μ-receptors to hyperpolarize arcuate neurons via an inwardly rectifying potassium conductance Brain Res. 513 1990 15 23 (Pubitemid 20144268)
56. J.A. Lord, A.A. Waterfield, J. Hughes, and H.W. Kosterlitz Endogenous opioid peptides: multiple agonists and receptors Nature 267 1977 495 499 (Pubitemid 8098466)
57. O.H. Lowry, N.J. Rosebrough, A.L. Farr, and R.J. Randall Protein measurement with the Folin phenol reagent J. Biol. Chem. 193 1951 265 275
58. V.A. Maisky, and N.Z. Doroshenko Catecholamine projections to the spinal cord in the rat and their relationship to central cardiovascular neurons J. Auton. Nerv. Syst. 34 2-3 1991 119 128
59. W.R. Martin, C.G. Eades, J.A. Thompson, R.E. Huppler, and P.E. Gilbert The effects of morphine- and nalorphine-like drugs in the nondependent and morphine-dependent chronic spinal dog J. Pharmacol. Exp. Ther. 197 3 1976 517 532
60. H. Meunier, and F. Labrie The dopamine receptor in the intermediate lobe of the rat pituitary gland is negatively coupled to adenylate cyclase Life Sci. 30 11 1982 963 968 (Pubitemid 12100864)
61. C. Missale, S.R. Nash, S.W. Robinson, M. Jaber, and M.G. Caron Dopamine receptors: from structure to function Physiol. Rev. 78 1998 189 225 (Pubitemid 28070979)
62. F.J. Monsma, L.C. Mahan, L.D. McVittie, C.R. Gerfen, and D.R. Sibley Molecular cloning and expression of a D1 dopamine receptor linked to adenylyl cyclase activation Proc. Natl. Acad. Sci. U.S.A. 87 17 1990 6723 6727
63. T. Moriizumi, and B. Leduc-Cross Is there a dopaminergic projection from the A11 catecholamine cell group to the amygdala? Exp. Brain Res. 88 1992 451 454
64. P. Mouchet, B. Guerin, and C. Feuerstein Dissociate destruction of noradrenaline and dopamine descending projections in the thoracic spinal cord of the rat Life Sci. 30 1982 373 381 (Pubitemid 12107796)
65. P. Onali, M.C. Olianas, and G.L. Gessa Characterization of dopamine receptors mediating inhibition of adenylate cyclase activity in rat striatum Mol. Pharmacol. 28 2 1985 138 145 (Pubitemid 16244113)
66. S.S. Pappas, B. Behrouz, K.L. Janis, J.L. Goudreau, and K.J. Lookingland Lack of D2 receptor mediated regulation of dopamine synthesis in A11 diencephalospinal neurons in male and female mice Brain Res. 1214 2008 1 10
67. S.S. Pappas, C.T. Tiernan, B. Behrouz, C.L. Jordan, S.M. Breedlove, J.L. Goudreau, and K.J. Lookingland Neonatal androgen dependent sex differences in lumbar spinal cord DA concentrations and the number of A11 diencephalospinal dopamine neurons J. Comp. Neurol. 518 13 2010 2423 2436
68. C. Peyron, P.H. Luppi, K. Kitahama, P. Fort, D.M. Hermann, and M. Jouvet Origin of the dopaminergic innervation of the rat dorsal raphe nucleus Neuroreport 6 18 1995 2527 2531 (Pubitemid 26031196)
69. S. Qu, W.G. Ondo, X. Zhang, W.J. Xie, T.H. Pan, and W.D. Le Projections of diencephalic dopamine neurons into the spinal cord in mice Exp. Brain Res. 168 1-2 2006 152 156 (Pubitemid 41752820)
70. J.L. Ridet, F. Sandillon, N. Rajaofetra, M. Geffard, and A. Privat Spinal dopaminergic system of the rat: light and electron microscopic study using an antiserum against dopamine, with particular emphasis on synaptic incidence Brain Res. 598 1992 233 241 (Pubitemid 23013065)
71. G. Skagerberg, A. Bjorklund, O. Lindvall, and R.H. Schmidt Origin and termination of the diencephalospinal dopamine system in the rat Brain Res. Bull. 9 1982 237 244 (Pubitemid 13225269)
72. G. Skagerberg, and O. Lindvall Organization of diencephalic dopamine neurones projecting to the spinal cord in the rat Brain Res. 342 1985 340 351 (Pubitemid 16241913)
73. M. Tavakoli-Nezhad, and L.A. Arbogast Mu and kappa opioid receptor expression in the mediobasal hypothalamus and effectiveness of selective antagonists on prolactin release during lactation Neuroscience 166 2 2010 359 367
74. J.R. Traynor, and M.S. Wood Distribution of opioid binding sites in spinal cord Neuropeptides 10 4 1987 313 320 (Pubitemid 17165905)
75. C. Trenkwalder, and W. Paulus The restless legs syndrome Lancet Neurol. 4 2005 465 475 (Pubitemid 40982457)
76. A.S. Undie, and E. Friedman Stimulation of a dopamine D1 receptor enhances inositol phosphates formation in rat brain J. Pharmacol. Exp. Ther. 253 2 1990 987 992 (Pubitemid 20209354)
77. A.S. Undie, and E. Friedman Selective dopaminergic mechanism of dopamine and SKF38393 stimulation of inositol phosphate formation in rat brain Eur. J. Pharmacol. 226 4 1992 297 302
78. A.S. Undie, J. Weinstock, H.M. Sarau, and E. Friedman Evidence for a distinct D1-like dopamine receptor that couples to activation of phosphoinositide metabolism in brain J. Neurochem. 62 5 1994 2045 2048
79. H.Y. Wang, A.S. Undie, and E. Friedman Evidence for the coupling of Gq protein to D1-like dopamine sites in rat striatum: possible role in dopamine-mediated inositol phosphate formation Mol. Pharmacol. 48 6 1995 988 994
80. M. Waldhoer, S.E. Bartlett, and J.L. Whistler Opioid receptors Annu. Rev. Biochem. 73 2004 953 990 (Pubitemid 39050391)
81. H. Wei, H. Viisanena, and A. Pertovaara Descending modulation of neuropathic hypersensitivity by dopamine D2 receptors in or adjacent to the hypothalamic A11 cell group Pharmacol. Res. 59 5 2009 355 363
82. J. Weil-Fugazza, and F. Godefroy Further evidence for the involvement of the diencephalo-dopaminergic system in pain modulation: a neurochemical study on the effect of morphine in the arthritic rat Int. J. Tissue React. 13 6 1991 305 310
83. C. Yokoyama, H. Okamura, T. Nakajima, J. Taguchi, and Y. Ibata Autoradiographical distribution of [3H]YM-09151-2, a high affinity and selective antagonist ligand for the dopamine D2 receptor group in the rat brain and spinal cord J. Comp. Neurol. 344 1994 121 136
84. M. Yoshida, and M. Tanaka Existence of a new dopaminergic terminal plexus in the rat spinal cord: assessment by immunohistochemistry using anti-dopamine serum Neurosci. Lett. 94 1988 5 9
85. H. Zhu, S. Clemens, M. Sawchuk, and S. Hochman Expression and distribution of all dopamine receptor subtypes (D1-D5) in the mouse lumbar spinal cord: a real-time polymerase chain reaction and non-autoradiographic in situ hybridization study Neuroscience 149 2007 885 897 (Pubitemid 350122885)