Ultrastructural immunocytochemical localization of μ-opioid receptors in dendritic targets of dopaminergic terminals in the rat caudate-putamen nucleus

Neuroscience

Volumn 81, Issue 3, 1997, Pages 757-771

  Wang, H ^a   Moriwaki, A ^b   Wang, J B ^b   Uhl, G R ^b   Pickel, V M ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Extrasynaptic site; Morphine; Nigrostriatal afferent; Stereotyped behaviour; Tyrosine hydroxylase; Ultrastructural localization

Indexed keywords

MU OPIATE RECEPTOR; TYROSINE 3 MONOOXYGENASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY LABELING; ARTICLE; DOPAMINERGIC TRANSMISSION; ELECTRON MICROSCOPY; IMMUNOCYTOCHEMISTRY; IMMUNOREACTIVITY; NERVE FIBER TRANSPORT; NERVE STIMULATION; NONHUMAN; PRESYNAPTIC NERVE; PRIORITY JOURNAL; RAT; RECEPTOR BINDING;

ANIMALS; AXONS; CAUDATE NUCLEUS; DENDRITES; DOPAMINE; IMMUNOHISTOCHEMISTRY; MALE; NERVE ENDINGS; PUTAMEN; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, OPIOID, MU; TISSUE DISTRIBUTION; TYROSINE 3-MONOOXYGENASE;

EID: 0031587264     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(97)00253-4     Document Type: Article

References (74)

1. Agnati L. F., Zoli M., Stromberg I., Fuxe K. Intercellular communication in the brain: wiring versus volume transmission. Neuroscience. 69:1995;711-726.
2. Albin R. L., Young A. B., Penney J. B. The functional anatomy of basal ganglia disorders. Trends Neurosci. 12:1989;366-375.
3. Amalric M., Koob G. F. Functionally selective neurochemical afferents and efferents of the mesocorticolimbic and nigrostriatal dopamine system. Prog. Brain Res. 99:1993;209-226.
4. Arluison M., Dietl M., Thibault J. Ultrastructural morphology of dopaminergic nerve terminals and synapses in the striatum of the rat using tyrosine hydroxylase immunocytochemistry: a topographical study. Brain Res. Bull. 13:1984;269-285.
5. Bjelke B., Stromberg I., O'Connor W. T., Andbjer B., Agnati L. F., Fuxe K. Evidence for volume transmission in the dopamine denervated neostriatum of the rat after a unilateral nigral 6-OHDA microinjection. Studies with systemic D-amphetamine treatment. Brain Res. 662:1994;11-24.
6. Bolam J. P., Powell J. F., Wu J. Y., Smith A. D. Glutamate decarboxylase-immunoreactive structures in the rat neostriatum: a correlated light and electron microscopic study including a combination of Golgi impregnation with immunocytochemistry. J. comp. Neurol. 237:1985;1-20.
7. Bouyer J. J., Park D. H., Joh T. H., Pickel V. M. Chemical and structural analysis of the relation between cortical inputs and tyrosine hydroxylase-containing terminals in rat neostriatum. Brain Res. 302:1984;267-275.
8. Broderick P. A., Blaha C. D., Lane R. F. In vivo electrochemical evidence for an enkephalinergic modulation underlying stereotyped behavior: reversibility by naloxone. Brain Res. 269:1983;378-381.
9. Broderick P. A., Gardner E. L., van Praag H. M. In vivo electrochemical and behavioral evidence for specific neural substrates modulated differentially by enkephalin in rat stimulant stereotypy and locomotion. Biol. Psychiat. 19:1984;45-54.
10. Caillé I., Dumartin B., Bloch B. Ultrastructural localization of D1 dopamine receptor immunoreactivity in rat striatonigral neurons and its relation with dopaminergic innervation. Brain Res. 730:1996;17-31.
11. Campbell K., Bjorklund A. Prefrontal corticostriatal afferents maintain increased enkephalin gene expression in the dopamine-denervated rat striatum. Eur. J. Neurosci. 6:1994;1371-1383.
12. Cepeda C., Walsh J. P., Hull C. D., Howard S. G., Buchwald N. A., Levine M. S. Dye-coupling in the neostriatum of the rat: I. Modulation by dopamine-depleting lesions. Synapse. 4:1989;229-237.
13. Chan J., Aoki C., Pickel V. M. Optimization of differential immunogold-silver and peroxidase labeling with maintenance of ultrastructure in brain sections before plastic embedding. J. Neurosci. Meth. 33:1990;113-127.
14. 5-enkephalin. Brain Res. 731:1996;141-154.
15. Chesselet M. F., Cheramy A., Reisine T. D., Glowinski J. Morphine and delta-opiate agonists locally stimulate in vivo dopamine release in cat caudate nucleus. Nature. 291:1981;320-322.
16. 7 (YGGFMRF) content elicited by long-term treatment with haloperidol. J. Pharmac. exp. Ther. 229:1984;171-174.
17. Delfs J. M., Kong H., Mestek A., Chen Y., Yu L., Reisine T., Chesselet M.-F. Expression of mu opioid receptor mRNA in rat brain: An in situ hybridization study at the single cell level. J. comp. Neurol. 345:1994;46-68.
18. De Vries T. J., Jonker A. J., Voorn P., Mulder A. H., Schoffelmeer A. N. M. Adaptive changes in rat striatal preproenkephalin expression and dopamine-opioid interactions upon chronic haloperidol treatment during different developmental stages. Devl Brain Res. 78:1994;175-181.
19. Di Chiara G., Imperato A. Drugs abused by humans preferentially increase synaptic dopamine concentrations in the mesolimbic system of freely moving rats. Proc. natn. Acad. Sci. U.S.A. 85:1988;5274-5278.
20. Difiglia M., Pasik T., Pasik P. Ultrastructure of Golgi-impregnated and gold-toned spiny and aspiny neurons in the monkey neostriatum. J. Neurocytol. 9:1980;471-492.
21. Dourmap N., Michael-Titus A., Costentin J. Local enkephalins tonically modulate dopamine release in the striatum: a microdialysis study. Brain Res. 524:1990;153-155.
22. Freund T. F., Powell J. F., Smith A. D. Tyrosine hydroxylase-immunoreactive boutons in synaptic contact with identified striatonigral neurons, with particular reference to dendritic spines. Neuroscience. 13:1984;1189-1215.
23. Girault J. A., Barbeito L., Spampinato U., Gozlan H., Glowinski J., Besson M. J. In vivo release of endogenous amino acids from the rat striatum: further evidence for a role of glutamate and aspartate in corticostriatal neurotransmission. J. Neurochem. 47:1986;98-106.
24. Goldman-Rakic P., Leranth C., Williams S. M., Mons N., Geffard M. Dopamine synaptic complex with pyramidal neurons in primate cerebral cortex. Proc. natn. Acad. Sci. U.S.A. 86:1989;9015-9019.
25. Hersch S. M., Ciliax B. J., Gutekunst C.-A., Rees H. D., Heilman C. J., Yung K. K. L., Bolam J. P., Ince E., Yi H., Levey A. I. Electron microscopic analysis of D1 and D2 dopamine receptor proteins in the dorsal striatum and their synaptic relationships with motor corticostriatal afferents. J. Neurosci. 15:1995;5222-5237.
26. Ingham C. A., Hood S. H., Arbuthnott G. W. A light and electron microscopical study of enkephalin-immunoreactive structures in the rat neostriatum after removal of the nigrostriatal dopaminergic pathway. Neuroscience. 42:1991;715-730.
27. Kelley A. E., Delfs J. M. Excitatory amino acid receptors mediate the orofacial stereotypy elicited by dopaminergic stimulation of the ventrolateral striatum. Neuroscience. 60:1994;85-95.
28. Kemp J. M., Powell T. P. S. The synaptic organization of the caudate nucleus. Phil. Trans. R. Soc. 262:1971;403-412.
29. Koch C., Poggio T. Electrical properties of dendritic spines. Trends Neurosci. 6:1983;80-83.
30. Lee J. M., De Leon-Jones F., Fields J. Z., Ritzmann R. F. Cyclo (Leu-Gly) attenuates the striatal dopaminergic supersensitivity induced by chronic morphine. Alcohol Drug Res. 7:1987;1-10.
31. Leranth C. and Pickel V. M. (1989) Electron microscopic pre-embedding double immunostaining methods. In Tract Tracing Methods 2 (eds Heimer L. and Zaborsky L.), Recent Progress, pp. 129-172. Plenum, New York.
32. Lloyd K. G. Special chemistry of the basal ganglia. 1. Monoamines. Pharmac. Ther. 1:1975;49-61.
33. Lubetzki C., Chesselet M. F., Glowinski J. Modulation of dopamine release in rat striatal slices by delta opiate agonists. J. Pharmac. exp. Ther. 222:1982;435-440.
34. Mansour A., Fox C. A., Thompson R. C., Akil H., Watson S. J. μ-opioid receptor mRNA expression in the rat CNS: comparison to μ-receptor binding. Brain Res. 643:1994;245-265.
35. 2), a potent μ-opioid peptide agonist, affects various patterns of locomotor activities. Pharmac. Biochem. Behav. 51:1995;149-151.
36. Meyer M. E., Meyer M. E. Behavioral effects of the mu-opioid peptide agonists DAMGO, DALDA, and PL017 on locomotor activities. Pharmac. Biochem. Behav. 46:1993;391-395.
37. Miller R., Beninger R. J. On the interpretation of asymmetries of posture and locomotion produced with dopamine agonists in animals with unilateral depletion of striatal dopamine. Prog. Neurobiol. 36:1991;229-256.
38. Mitchell I. J., Lawson S., Moser B., Laidlaw S. M., Cooper A. J., Walkinshaw G., Waters C. M. Glutamate-induced apoptosis results in a loss of striatal neurons in the parkinsonian rat. Neuroscience. 63:1994;1-5.
39. Mocchetti I., Schwartz J. P., Costa E. Use of mRNA hybridization and radioimmunoassay to study mechanisms of drug-induced accumulation of enkephalins in rat brain structures. Molec. Pharmac. 28:1985;86-91.
40. Moriwaki A., Wang J.-B., Svingos A., van Bockstaele E., Cheng P., Pickel V., Uhl G. R. μ opiate receptor immunoreactivity in rat central nervous system. Neurochem. Res. 21:1996;1315-1330.
41. Murrin L. C., Ferrer J. R. Ontogeny of the rat stratum: correspondence of dopamine terminals, opiate receptors and acetylcholinesterase. Neurosci. Lett. 47:1984;155-160.
42. Nestler E. J. Hard target: understanding dopaminergic neurotransmission. Cell. 79:1994;923-926.
43. Nirenberg M. J., Vaughan R. A., Uhl G. R., Kuhar M. J., Pickel V. M. The dopamine transporter is localized to dendritic and axonal plasma membranes of nigrostriatal dopaminergic neurons. J. Neurosci. 16:1996;436-447.
44. Normand E., Popovici T., Onteniente B., Fellmann D., Piatier-Tonneau D., Auffray C., Bloch B. Dopaminergic neurons of the substantia nigra modulate preproenkephalin A gene expression in rat striatal neurons. Brain Res. 439:1988;39-46.
45. Paxinos G. and Watson C. (1986) The Rat Brain in Stereotaxic Coordinates. Academic Press, Orlando, FL.
46. Pert C. B., Kuhar M. J., Snyder S. H. Opiate receptor: autoradiographic localization in rat brain. Proc. natn. Acad. Sci. U.S.A. 73:1976;3729-3733.
47. Peters A., Palay S. L. and Webster H. deF. (1991) The Fine Structure of the Nervous System: Neurons and Their Supporting Cells. Oxford University Press, New York.
48. Pickel V. M., Beckley S. C., Joh T. H., Reis D. J. Ultrastructural immunocytochemical localization of tyrosine hydroxylase in the neostriatum. Brain Res. 225:1981;373-385.
49. Pickel V. M., Chan J., Sesack S. R. Cellular basis for interactions between catecholaminergic afferents and neurons containing Leu-enkephalin-like immunoreactivity in rat caudate-putamen nuclei. J. Neurosci. Res. 31:1992;212-230.
50. 5-enkephalin terminals in the caudate-putamen nuclei of adult rats receiving neonatal intranigral 6-hydroxydopamine. Devl Brain Res. 83:1994;163-180.
51. Piepponen T. P., Ahtee L. Effects of selective opioid receptor antagonists on morphine-induced changes in striatal and limbic dopamine metabolism. Pharmac. Toxicol. 77:1995;204-208.
52. Preston R. J., Bishop G. A., Kitai S. T. Medium spiny neuron projection from the rat striatum: an intercellular horseradish peroxidase study. Brain Res. 183:1980;253-263.
53. Romano G. J., Shivers B. D., Harlan R. E., Howells R. D., Pfaff D. W. Haloperidol increases proenkephalin mRNA levels in the caudate-putamen of the rat: a quantitative study at the cellular level using in situ hybridization. Molec. Brain Res. 2:1987;33-41.
54. 2 receptor-like immunoreactivity in midbrain dopamine neurons and their striatal targets. J. Neurosci. 14:1994;88-106.
55. Smith A. D., Bolam J. P. The neural network of the basal ganglia as revealed by the study of synaptic connections of identified neurones. Trends Neurosci. 13:1990;259-265.
56. Smith J. A. M., Leslie F. M., Broide R. S., Loughlin S. E. Long-term changes in striatal opioid systems after 6-hydroxydopamine lesion of rat substantia nigra. Neuroscience. 55:1993;935-951.
57. Surratt C. K., Johnson P. S., Moriwaki A., Seidleck B. K., Blaschak C. J., Wang J. B., Uhl G. R. μ opiate receptor. Charged transmembrane domain amino acids are critical for agonist recognition and intrinsic activity. J. biol. Chem. 269:1994;20548-20553.
58. 5-enkephalin. J. Neurosci. 16:1996;4162-4173.
59. Swanson L. W., Hartman B. K. The central adrenergic system. An immunofluorescence study of the location of cell bodies and their efferent connections in the rat utilizing dopamine-beta-hydroxylase as a marker. J. comp. Neurol. 163:1975;467-505.
60. Tang F., Costa E., Schwartz J. P. Increase of proenkephalin mRNA and enkephalin content of rat striatum after daily injection of haloperidol for 2 to 3 weeks. Proc. natn. Acad. Sci. U.S.A. 80:1983;3841-3844.
61. Tennyson V. M., Heikkila R., Mytilineou C., Cote L., Cohen G. 5-Hydroxydopamine "tagged" neuronal boutons in rabbit neostriatum: interrelationship between vesicles and axonal membrane. Brain Res. 82:1974;341-348.
62. Trovero F., Herve D., Desban M., Glowinski J., Tassin J.-P. Striatal opiate mu-receptors are not located on dopamine nerve endings in the rat. Neuroscience. 39:1990;313-321.
63. Unterwald E. M., Horne-King J., Kreek M. J. Chronic cocaine alters brain mu opioid receptors. Brain Res. 584:1992;314-318.
64. Unterwald E. M., Rubenfeld J. M., Kreek M. J. Repeated cocaine administration upregulates kappa and mu, but not delta, opioid receptors. NeuroReport. 5:1994;1613-1616.
65. Van Bockstaele E. J., Colago E. E. O., Cheng P., Moriwaki A., Uhl G. R., Pickel V. M. Ultrastructural evidence for prominent distribution of the μ-opioid receptor at extrasynaptic sites on noradrenergic dendrites in the rat nucleus locus coeruleus. J. Neurosci. 16:1996;5037-5048.
66. Vaughan D. W., Peters A. A three dimensional study of layer I of the rat parietal cortex. J. comp. Neurol. 149:1973;355-370.
67. Verney C., Alvarez C., Geffard M., Berger B. Ultrastructural double-labelling study of dopamine terminals and GABA-containing neurons in rat anteromedial cerebral cortex. Eur. J. Neurosci. 2:1990;960-972.
68. Voorn P., Jorritsma-Byham B., Van Dijk C., Buijs R. M. The dopaminergic innervation of the ventral striatum in the rat: a light and electron microscopical study with antibodies against dopamine. J. comp. Neurol. 251:1986;84-99.
69. Voorn P., Roest G., Groenewegen H. J. Increase of enkephalin and decrease of substance P immunoreactivity in the dorsal and ventral striatum of the rat midbrain 6-hydroxydopamine lesions. Brain Res. 412:1987;391-396.
70. Walsh J. P., Cepeda C., Hull C. D., Fisher R. S., Levine M. S., Buchwald N. A. Dye-coupling in the neostriatum of the rat. II. Decreased coupling between neurons during development. Synapse. 4:1989;238-247.
71. Walter S., Kuschinsky K. Conditioning of morphine-induced locomotor activity and stereotyped behaviour in rats. J. neural Transm. 78:1989;231-247.
72. 5-enkephalin in the patch compartment of the rat caudate-putamen nucleus. J. comp. Neurol. 375:1996;659-674.
73. Young W. S. III, Bonner T. I., Brann M. R. Mesencephalic dopamine neurons regulate the expression of neuropeptide mRNAs in the rat forebrain. Proc. natn. Acad. Sci. U.S.A. 83:1986;9827-9831.
74. 2 dopamine receptors in the basal ganglia of the rat: light and electron microscopy. Neuroscience. 65:1995;709-730.