Ultrastructural localization of enkephalin and μ-opioid receptors in the rat ventral tegmental area

Neuroscience

Volumn 114, Issue 2, 2002, Pages 461-474

  Garzon M ^a,b   Pickel, V M ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

Author keywords

Mesocorticolimbic; Neuropeptides; Opiate; Reinforcement; Reward

Indexed keywords

ANTIGEN; ENKEPHALIN; LEUCINE ENKEPHALIN; MU OPIATE RECEPTOR; NEUROPEPTIDE; PEROXIDASE;

ANIMAL TISSUE; ARTICLE; AUTOREGULATION; BRAIN; CELL MEMBRANE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DENDRITE; ELECTRON MICROSCOPY; ENZYME ACTIVATION; ENZYME MECHANISM; IMMUNOCYTOCHEMISTRY; IMMUNOGOLD LABELING; IMMUNOREACTIVITY; MALE; NERVE ENDING; NONHUMAN; NONMYELINATED NERVE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; RAT; SYNAPSE; VENTRAL TEGMENTUM;

ANIMALS; AUTORECEPTORS; DENDRITES; ENKEPHALINS; IMMUNOHISTOCHEMISTRY; MALE; MICROSCOPY, ELECTRON; NERVE FIBERS, UNMYELINATED; NEURAL INHIBITION; PRESYNAPTIC TERMINALS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, OPIOID, MU; SYNAPTIC MEMBRANES; SYNAPTIC TRANSMISSION; VENTRAL TEGMENTAL AREA;

EID: 0036774054     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(02)00249-X     Document Type: Article

References (126)

1. Abou-Madi L., Pontarotti P., Tramu G., Cupo A., Eybalin M. Coexistence of putative neuroactive substances in lateral olivocochlear neurons of rat and guinea pig. Hear. Res. 30:1987;135-146.
2. Altschuler R.A., Fex J., Parakkal M.H., Eckenstein F. Colocalization of enkephalin-like and choline acetyltransferase-like immunoreactivities in olivocochlear neurons of the guinea pig. J. Histochem. Cytochem. 32:1984;839-843.
3. Arvidsson U., Riedl M., Chakrabarti S., Lee J.-H., Nakano A.H., Dado R., Loh H.H., Law P.-Y., Wessendorf M.W., Elde R. Distribution and targeting of a mu-opioid receptor (MOR1) in brain and spinal cord. J. Neurosci. 15:1995;3328-3341.
4. Bals-Kubik R., Ableitner A., Herz A., Shippenberg T.S. Neuroanatomical sites mediating the motivational effects of opioids as mapped by the conditioned place preference paradigm in rats. J. Pharmacol. Exp. Ther. 24:1987;328-337.
5. Bell K.M., Traynor J.R. Dynorphin A(1-8): stability and implications for in vitro opioid activity. Can. J. Physiol. Pharmacol. 76:1998;325-333.
6. Bonci A., Williams J.T. Increased probability of GABA release during withdrawal from morphine. J. Neurosci. 17:1997;796-803.
7. Bourinet E., Soong T.W., Stea A., Snutch T.P. Determinants of the G protein-dependent opioid modulation of neuronal calcium channels. Proc. Natl. Acad. Sci. USA. 93:1996;1486-1491.
8. Broekkamp C.L.E., Phillips A.G., Cools A.R. Stimulant effects of enkephalin microinjection into the dopaminergic A10 area. Nature. 278:1979;560-562.
9. Buckley K.M., Melikian H.E., Provoda C.J., Waring M.T. Regulation of neuronal function by protein trafficking: a role for the endosomal pathway. J. Physiol. 525:2000;11-19.
10. Cador M., Kelley A.E., Le Moal M., Stinus L. d-Ala-met-enkephalin injection into the ventral tegmental area: effect on investigatory and spontaneous motor behaviour in the rat. Psychopharmacology. 96:1988;332-342.
11. Cador M., Rivet J.M., Kelley A.E., Le Moal M., Stinus L. Substance P, neurotensin and enkephalin injections into the ventral tegmental area: comparative study on dopamine turnover in several forebrain structures. Brain Res. 486:1989;357-363.
12. Capogna M., Gahwiler B.H., Thompson S.M. Mechanism of mu-opioid receptor-mediated presynaptic inhibition in the rat hippocampus in vitro. J. Physiol. 470:1993;539-558.
13. Carlin R.K., Grab D.J., Cohen R.S., Siekevitz P. Isolation and characterization of postsynaptic densities from various brain regions: enrichment of different types of postsynaptic densities. J. Cell Biol. 86:1980;831-845.
14. Carr D.B., Sesack S.R. GABA-containing neurons in the rat ventral tegmental area project to the prefrontal cortex. Synapse. 38:2000;114-123.
15. 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. Methods. 33:1990;113-127.
16. Chang K.J., Cooper B.R., Hazum E., Cuatrecasas P. Multiple opiate receptors: different regional distribution in the rat brain and differential binding of opiates and opioid peptides. Mol. Pharmacol. 16:1979;91-104.
17. Chavkin C., James I.F., Goldstein A. Dynorphin is a specific endogenous ligand of the kappa opioid receptor. Science. 215:1982;413-414.
18. Chen Y., Mestek A., Liu J., Hurley J.A., Yu L. Molecular cloning and functional expression of a mu-opioid receptor from rat brain. Mol. Pharmacol. 44:1993;8-12.
19. 5-enkephalin. J. Comp. Neurol. 371:1996;522-536.
20. 5-enkephalin. Brain Res. 731:1996;141-154.
21. Cuello A.C., Milstein C., Couture R., Wright B., Priestley J.V., Jarvis J. Characterization and immunocytochemical application of monoclonal antibodies against enkephalins. J. Histochem. Cytochem. 32:1984;947-957.
22. Dauge V., Kalivas P.W., Duffy T., Roques B.P. Effect of inhibiting enkephalin catabolism in the VTA on motor activity and extracellular dopamine. Brain Res. 599:1992;209-214.
23. 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.
24. Devine D.P., Leone P., Pocock D., Wise R.A. Differential involvement of ventral tegmental mu, delta and kappa opioid receptors in modulation of basal mesolimbic dopamine release: in vivo microdialysis studies. J. Pharmacol. Exp. Ther. 266:1993;1236-1246.
25. Devine D.P., Wise R.A. Self-administration of morphine, DAMGO, and DPDPE into the ventral tegmental area of rats. J. Neurosci. 14:1994;1978-1984.
26. Di Chiara G., Imperato A. Drugs abused by humans preferentially increase synaptic dopamine concentrations in the mesolimbic system of freely moving rats. Proc. Natl. Acad. Sci. USA. 85:1988;5274-5278.
27. Di Chiara G., North R.A. Neurobiology of opiate abuse. Trends Pharmacol. Sci. 13:1992;185-193.
28. DiFiglia M., Aronin N., Martin J.B. Light and electron microscopic localization of immunoreactive Leu-enkephalin in the monkey basal ganglia. J. Neurosci. 2:1982;303-320.
29. Dilts R.P., Kalivas P.W. Autoradiographic localization of mu-opioid and neurotensin receptors within the mesolimbic dopamine system. Brain Res. 488:1989;311-327.
30. Dolphin A.C. Voltage-dependent calcium channels and their modulation by neurotransmitters and G proteins. Exp. Physiol. 80:1995;1-36.
31. Dolphin A.C. Mechanisms of modulation of voltage-dependent calcium channels by G proteins. J. Physiol. 506:1998;3-11.
32. Eldred W.D., Zucker C., Karten H.J., Yazulla S. Comparison of fixation and penetration enhancement techniques for use in ultrastructural immunocytochemistry. J. Histochem. Cytochem. 31:1983;285-292.
33. Fallon J.H., Leslie F.M. Distribution of dynorphin and enkephalin peptides in the rat brain. J. Comp. Neurol. 249:1986;293-336.
34. Fallon J.H., Moore R.Y. Catecholamine innervation of the basal forebrain. IV. Topography of the dopamine projection to the basal forebrain and neostriatum. J. Comp. Neurol. 180:1978;545-580.
35. Finley J.C., Maderdrut J.L., Petrusz P. The immunocytochemical localization of enkephalin in the central nervous system of the rat. J. Comp. Neurol. 198:1981;541-565.
36. Fukuda K., Kato S., Mori K., Nishi M., Takeshima H. Primary structures and expression from cDNAs of rat opioid receptor delta- and mu-subtypes. FEBS Lett. 327:1993;311-314.
37. Garzón M., Pickel V.M. Plasmalemma mu-opioid receptor distribution mainly in non-dopaminergic neurons in the rat ventral tegmental area. Synapse. 41:2001;311-328.
38. Garzón M., Vaughan R.A., Uhl G.R., Kuhar M.J., Pickel V.M. Cholinergic axon terminals in the ventral tegmental area target a subpopulation of neurons expressing low levels of the dopamine transporter. J. Comp. Neurol. 410:1999;197-210.
39. Gaudriault G., Nouel D., Dal Farra C., Beaudet A., Vincent J.P. Receptor-induced internalization of selective peptidic mu and delta opioid ligands. J. Biol. Chem. 272:1997;2880-2888.
40. German D.C., Speciale S.G., Manaye K.F., Sadeq M. Opioid receptors in midbrain dopaminergic regions of the rat: I. Mu receptor autoradiography. J. Neural Transm. Gen. Sect. 91:1993;39-52.
41. Gintzler A.R., Xu H. Opioids can produce a concentration-dependent naloxone-reversible enhancement of inhibition of evoked enkephalin release. NIDA Res. Monogr. 105:1991;27-33.
42. Goldstein A., Tachibana S., Lowney L.L., Hunkapiller M., Hood L. Dynorphin-(1-13), an extraordinarily potent opioid peptide. Proc. Natl. Acad. Sci. USA. 76:1979;6666-6670.
43. 3H]beta-endorphin binding in brain. Brain Res. 288:1983;334-337.
44. Goodman R.R., Snyder S.H., Kuhar M.J., Young W.S. Differentiation of delta and mu opiate receptor localizations by light microscopic autoradiography. Proc. Natl. Acad. Sci. USA. 77:1980;6239-6243.
45. Gracy K.N., Svingos A.L., Pickel V.M. Dual ultrastructural localization of mu-opioid receptors and NMDA-type glutamate receptors in the shell of the rat nucleus accumbens. J. Neurosci. 17:1997;4839-4848.
46. Gray E.G. Axosomatic and axo-dendritic synapses of the cerebral cortex: an electron microscopic study. J. Anat. 93:1959;420-433.
47. Gysling K., Wang R.Y. Morphine-induced activation of A10 dopamine neurons in the rat. Brain Res. 277:1983;119-127.
48. Herkenham M. Mismatches between neurotransmitter and receptor localizations in brain: observations and implications. Neuroscience. 23:1987;1-38.
49. 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.
50. Hökfelt T., Broberger C., Xu Z.Q., Sergeyev V., Ubink R., D'ez M. Neuropeptides - An overview. Neuropharmacology. 39:2000;1337-1356.
51. Hsu S.M., Raine L., Fanger H. The use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase technique: a comparison between ABC and unlabeled antibody (peroxidase) procedures. J. Histochem. Cytochem. 29:1981;577-599.
52. Hughes J., Smith T.W., Kosterlitz H.W., Fothergill L.A., Morgan B.A., Morris H.R. Identification of two related pentapeptides from the brain with potent opiate agonist activity. Nature. 258:1975;577-580.
53. Johnson R.P., Sar M., Stumpf W.E. A topographic localization of enkephalin on the dopamine neurons of the rat substantia nigra and ventral tegmental area demonstrated by combined histofluorescence-immunocytochemistry. Brain Res. 194:1980;566-571.
54. Johnson S.W., North R.A. Opioids excite dopamine neurons by hyperpolarization of local interneurons. J. Neurosci. 12:1992;483-488.
55. Johnson S.W., North R.A. Two types of neurone in the rat ventral tegmental area and their synaptic inputs. J. Physiol. 450:1992;455-468.
56. Joyce E.M., Koob G.F., Strecker R., Iversen S.D., Bloom F.E. The behavioural effects of enkephalin analogues injected into the ventral tegmental area and globus pallidus. Brain Res. 221:1981;359-370.
57. Kalivas P.W., Abhold R. Enkephalin release into the ventral tegmental area in response to stress: modulation of mesocorticolimbic dopamine. Brain Res. 414:1987;339-348.
58. Kalivas P.W., Churchill L., Klitenick M.A. GABA and enkephalin projection from the nucleus accumbens and ventral pallidum to the ventral tegmental area. Neuroscience. 57:1993;1047-1060.
59. Kalivas P.W., Richardson-Carlson R. Endogenous enkephalin modulation of dopamine neurons in ventral tegmental area. Am. J. Physiol. 251:1986;R243-R249.
60. Kalivas P.W., Widerlov E., Stanley D., Breese G., Prange A.J. Jr. Enkephalin action on the mesolimbic system: a dopamine-dependent and a dopamine-independent increase in locomotor activity. J. Pharmacol. Exp. Ther. 227:1983;229-237.
61. Keith D.E., Anton B., Murra S.R., Zaki P.A., Chu P.C., Lissin D.V., Monteillet-Agius G., Stewart P.L., Evans C.J., von Zastrow M. Mu-opioid receptor internalization: opiate drugs have differential effects on a conserved endocytic mechanisms in vitro and in the mammalian brain. Mol. Pharmacol. 53:1998;377-384.
62. Kelley A.E., Stinus L., Iversen S.D. Interactions between D-ala-met-enkephalin, A10 dopaminergic neurones, and spontaneous behaviour in the rat. Behav. Brain Res. 1:1980;3-24.
63. Khachaturian H., Lewis M.E., Watson S.J. Enkephalin systems in diencephalon and brainstem of the rat. J. Comp. Neurol. 220:1983;310-320.
64. Latimer L.G., Duffy P., Kalivas P.W. Mu opioid receptor involvement in enkephalin activation of dopamine neurons in the ventral tegmental area. J. Pharmacol. Exp. Ther. 241:1987;328-337.
65. Leranth, C., Pickel, V.M., 1989. Electron microscopic pre-embedding double immnunostaining methods. In: Heimer, L., Zaborsky, L. (Eds.), Tract Tracing Methods 2, Recent Progress. Plenum, New York, pp. 129-172.
66. Lindvall O., Björklund A. The organization of the ascending catecholamine neuron systems in the rat brain as revealed by the glyoxylic acid fluorescence method. Acta Physiol. Scand. 412:(Suppl.):1974;1-48.
67. Lord J.A., Waterfield A.A., Hughes J., Kosterlitz H.W. Endogenous opioid peptides: multiple agonists and receptors. Nature. 267:1977;495-499.
68. 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.
69. Mansour A., Fox C.A., Burke S., Akil H., Watson S.J. Immunohistochemical localization of the cloned mu-opioid receptor in the rat CNS. J. Chem. Neuroanat. 8:1995;283-305.
70. 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.
71. Matthews R.T., German D.C. Electrophysiological evidence for excitation of rat ventral tegmental area dopamine neurons by morphine. Neuroscience. 11:1984;617-625.
72. Milner T.A., Pickel V.M., Reis D.J. Ultrastructural basis for interactions between central opioids and catecholamines. I. Rostral ventrolateral medulla. J. Neurosci. 9:1989;2114-2130.
73. Mizoguchi A., Kim S., Ueda T., Kikuchi A., Yorifuji H., Hirokawa N., Takai Y. Localization and subcellular distribution of smg p25A, a ras p21-like GTP-binding protein, in rat brain. J. Biol. Chem. 265:1990;11872-11879.
74. Monory K., Bourin M.C., Spetea M., Tömböly C., Tóth G., Matthes H.W., Kieffer B.L., Hanoune J., Borsodi A. Specific activation of the μ opioid receptor (MOR) by endomorphin 1 and endomorphin 2. Eur. J. Neurosci. 12:2000;577-584.
75. Moriwaki A., Wang J.-B., Svingos A., Van Bockstaele E., Cheng P., Pickel V., Uhl G.R. Mu-opiate receptor immunoreactivity in rat central nervous system. Neurochem. Res. 21:1996;1315-1331.
76. Napier T.C., Mitrovic I. Opioid modulation of ventral pallidal inputs. Ann. NY Acad. Sci. 877:1999;176-201.
77. Ng G.Y., O'Dowd B.F., George S.R. Genotypic differences in mesolimbic enkephalin gene expression in DBA/2J and C57BL/6J inbred mice. Eur. J. Pharmacol. 311:1996;45-52.
78. Nock, B., 1995. Kappa and delta opioid receptor binding. In: Tseng, L.F. (Ed.), The Pharmacology of Opioid Peptides. Harwood Academic, New York, pp. 29-56.
79. Noel M.B., Gratton A. Electrochemical evidence of increased dopamine transmission in prefrontal cortex and nucleus accumbens elicited by ventral tegmental mu-opioid receptor activation in freely behaving rats. Synapse. 21:1995;110-122.
80. Oades R.D., Halliday G.M. Ventral tegmental (A10) system: neurobiology. 1. Anatomy and connectivity. Brain Res. Rev. 12:1987;117-165.
81. Pak Y., Kouvelas A., Scheideler M.A., Rasmussen J., O'Dowd B.F., George S.R. Agonist-induced functional desensitization of the mu-opioid receptor is mediated by loss of membrane receptors rather than uncoupling from G protein. Mol. Pharmacol. 50:1996;1214-1222.
82. Paxinos, G., Watson, C., 1986. The Rat Brain in Stereotaxic Coordinates. Academic, San Diego, CA.
83. Pelletier G., Leclerc R. Localization of Leu-enkephalin in dense core vesicles of axon terminals. Neurosci. Lett. 12:1979;159-163.
84. Peters, A., Palay, S.L., Webster, H.D., 1991. The Fine Structure of the Nervous System: Neurons and their Supporting Cells. Oxford University, Oxford, pp. 1-494.
85. Phillipson O.T. Afferent projections to the ventral tegmental area of Tsai and interfascicular nucleus: a horseradish peroxidase study in the rat. J. Comp. Neurol. 187:1979;117-143.
86. Pickel V.M., Colago E.E.O. Presence of mu-opioid receptors in targets of efferent projections from the central nucleus of the amygdala to the nucleus of the solitary tract. Synapse. 33:1999;141-152.
87. Pickel V.M., Joh T.H., Reis D.J., Leeman S.E., Miller R.J. Electron microscopic localization of substance P and enkephalin in axon terminals related to dendrites of catecholaminergic neurons. Brain Res. 160:1979;387-400.
88. Pickel V.M., Sumal K.K., Beckley S.C., Miller R.J., Reis D.J. Immunocytochemical localization of enkephalin in the neostriatum of rat brain: a light and electron microscopic study. J. Comp. Neurol. 189:1980;721-740.
89. 2+ channels in GH3 cells by cloned mu- and delta-opioid receptors. Mol. Pharmacol. 50:1996;947-956.
90. Reynolds E.S. The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J. Cell Biol. 17:1963;208.
91. Safieddine S., Prior A.M., Eybalin M. Choline acetyltransferase, glutamate decarboxylase, tyrosine hydroxylase, calcitonin gene-related peptide and opioid peptides coexist in lateral efferent neurons of rat and guinea-pig. Eur. J. Neurosci. 9:1997;356-367.
92. Sesack S.R., Pickel V.M. Dual ultrastructural localization of enkephalin and tyrosine hydroxylase immunoreactivity in the rat ventral tegmental area: multiple substrates for opiate-dopamine interactions. J. Neurosci. 12:1992;1335-1350.
93. Sesack S.R., Pickel V.M. Ultrastructural relationships between terminals immunoreactive for enkephalin, GABA, or both neurotransmitters in the rat ventral tegmental area. Brain Res. 672:1995;261-275.
94. Shippenberg T.S., Herz A. Place preference conditioning reveals the involvement of D1-dopamine receptors in the motivational properties of mu- and kappa-opioid agonists. Brain Res. 436:1987;169-172.
95. Shoji Y., Delfs J., Williams J.T. Presynaptic inhibition of GABA(B)-mediated synaptic potentials in the ventral tegmental area during morphine withdrawal. J. Neurosci. 19:1999;2347-2355.
96. Smith A.P., Lee N.M. Pharmacology of dynorphin. Annu. Rev. Pharmacol. Toxicol. 28:1988;123-140.
97. Smythe E., Warren G. The mechanism of receptor-mediated endocytosis. Eur. J. Biochem. 202:1991;689-699.
98. Somogyi P., Priestly J.V., Cuello A.C., Smith A.D., Takagi H. Synaptic connections of enkephalin-immunoreactive nerve terminals in the neostriatum: a correlated light and electron microscopic study. J. Neurocytol. 11:1982;779-807.
99. Spanagel R., Herz A., Shippenberg T.S. The effects of opioid peptides on dopamine release in the nucleus accumbens: an in vivo microdialysis study. J. Neurochem. 55:1990;1734-1740.
100. Spanagel R., Herz A., Shippenberg T.S. Opposing tonically active endogenous opioid systems modulate the mesolimbic dopaminergic pathway. Proc. Natl. Acad. Sci. USA. 89:1992;2046-2050.
101. Steffensen S.C., Svingos A.L., Pickel V.M., Henriksen S.J. Electrophysiological characterization of GABAergic neurons in the ventral tegmental area. J. Neurosci. 18:1998;8003-8015.
102. Sternini C., Brecha N.C., Minnis J., D'Agostino G., Balestra B., Fiori E., Tonini M. Role of agonist-dependent receptor internalization in the regulation of mu opioid receptors. Neuroscience. 98:2000;233-241.
103. Sternini C., Spann M., Anton B., Keith D.E. Jr., Bunnett N.W., von Zastrow M., Evans C., Brecha N.C. Agonist-selective endocytosis of mu opioid receptor by neurons in vivo. Proc. Natl. Acad. Sci. USA. 93:1996;9241-9246.
104. Stinus L., Koob G.F., Ling N., Bloom F.E., Le Moal M. Locomotor activation induced by infusion of endorphins into the ventral tegmental area: Evidence for opiate-dopamine interactions. Proc. Natl. Acad. Sci. USA. 77:1980;2323-2327.
105. Sudhof T.C. The synaptic vesicle cycle revisited. Neuron. 28:2000;317-320.
106. Sumal K.K., Pickel V.M., Miller R.J., Reis D.J. Enkephalin-containing neurons in substantia gelatinosa of spinal trigeminal complex: ultrastructure and synaptic interaction with primary sensory afferents. Brain Res. 248:1982;223-236.
107. Svingos A.L., Garzón M., Colago E.E., Pickel V.M. Mu-Opioid receptors in the ventral tegmental area are targeted to presynaptically and directly modulate mesocortical projection neurons. Synapse. 41:2001;221-229.
108. 5-enkephalin. J. Neurosci. 16:1996;4162-4173.
109. Swanson L.W. The projections of the ventral tegmental area and adjacent regions: a combined fluorescent retrograde tracer and immunofluorescence study in the rat. Brain Res. Bull. 9:1982;321-353.
110. Tempel A., Zukin R.S. Neuroanatomical patterns of the mu-, delta-, and kappa-opioid receptors of rat brain as determined by quantitative in vitro autoradiography. Proc. Natl. Acad. Sci. USA. 84:1987;4308-4312.
111. Thompson R.C., Mansour A., Akil H., Watson S.J. Cloning and pharmacological characterization of a rat mu opioid receptor. Neuron. 11:1993;903-913.
112. Thureson-Klein A.K., Klein R.L. Exocytosis from neuronal large dense-cored vesicles. Int. Rev. Cytol. 121:1990;67-126.
113. Van Bockstaele E.J., Branchereau P., Pickel V.M. Morphologically heterogeneous met-enkephalin terminals form synapses with tyrosine hydroxylase-containing dendrites in the rat nucleus locus coeruleus. J. Comp. Neurol. 363:1995;423-438.
114. Van Bockstaele E.J., Pickel V.M. Ultrastructure of serotonin-immunoreactive terminals in the core and shell of the rat nucleus accumbens: cellular substrates for interactions with catecholamine afferents. J. Comp. Neurol. 334:1993;603-617.
115. Van Bockstaele E.J., Saunders A., Commons K.G., Liu X.-B., Peoples J. Evidence for coexistence of enkephalin and glutamate in axon terminals and cellular sites for functional interactions of their receptors in the rat locus coeruleus. J. Comp. Neurol. 417:2000;103-114.
116. Wang H., Gracy K.N., Pickel V.M. mu-opioid and NMDA-type glutamate receptors are often colocalized in spiny neurons within patches of the caudate-putamen nucleus. J. Comp. Neurol. 412:1999;132-146.
117. 5-enkephalin in the patch compartment of the rat caudate-putamen nucleus. J. Comp. Neurol. 375:1996;659-674.
118. Wang H., Moriwaki A., Wang J.B., Uhl G.R., Pickel V.M. Ultrastructural immunocytochemical localization of mu-opioid receptors in dendritic targets of dopaminergic terminals in the rat caudate-putamen nucleus. Neuroscience. 81:1997;757-771.
119. Wang J.B., Imai Y., Eppler C.M., Gregor P., Spivak C.E., Uhl G.R. Mu-opiate receptor: cDNA cloning and expression. Proc. Natl. Acad. Sci. USA. 90:1993;10230-10234.
120. Watson E.L. GTP-binding proteins and regulated exocytosis. Crit. Rev. Oral Biol. Med. 10:1999;284-306.
121. Westenbroek R.E., Hell J.W., Warner C., Dubel S.J., Snutch T.P., Catterall W.A. Biochemical properties and subcellular distribution of an N-type calcium channel alpha 1 subunit. Neuron. 9:1992;1099-1115.
122. Westenbroek R.E., Sakurai T., Elliott E.M., Hell J.W., Starr T.V., Snutch T.P., Catterall W.A. Immunochemical identification and subcellular distribution of the alpha 1A subunits of brain calcium channels. J. Neurosci. 15:1995;6403-6418.
123. Wise R.A. Opiate reward: sites and substrates. Neurosci. Biobehav. Rev. 13:1989;129-133.
124. Xu H., Smolens I., Gintzler A.R. Opioids can enhance and inhibit the electrically evoked release of methionine-enkephalin. Brain Res. 504:1989;36-42.
125. Zamir N., Palkovits M., Brownstein M. Distribution of immunoreactive Met-enkephalin-Arg6-Gly7-Leu8 and Leu-enkephalin in discrete regions of the rat brain. Brain Res. 326:1985;1-8.
126. Zhang J., Ferguson S.S., Barak L.S., Bodduluri S.R., Laporte S.A., Law P.Y., Caron M.G. Role for G protein-coupled receptor kinase in agonist-specific regulation of mu-opioid receptor responsiveness. Proc. Natl. Acad. Sci. USA. 95:1998;7157-7162.