Ultrastructural immunocytochemical localization of μ opioid receptors and Leu5-enkephalin in the patch compartment of the rat caudate-putamen nucleus

Journal of Comparative Neurology

Volumn 375, Issue 4, 1996, Pages 659-674

  Wang, Hong ^a   Moriwaki, Akiyoshi ^b,c   Wang, Jia Bei ^b,c   Uhl, George R ^b,c   Pickel, Virginia M ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b NATIONAL INSTITUTE ON DRUG ABUSE   (United States)

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

Author keywords

electron microscopy; endogenous opioid; extrasynaptic site; morphine; stereotyped behavior

Indexed keywords

LEUCINE ENKEPHALIN; MU OPIATE RECEPTOR;

ANIMAL TISSUE; ARTICLE; CAUDATE NUCLEUS; CELL ULTRASTRUCTURE; IMMUNOCYTOCHEMISTRY; IMMUNOGOLD STAINING; IMMUNOPEROXIDASE STAINING; MALE; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN LOCALIZATION; PUTAMEN; RAT; TISSUE DISTRIBUTION;

ANIMALS; CAUDATE NUCLEUS; CELL COMMUNICATION; CELL MEMBRANE; DENDRITES; ENKEPHALIN, LEUCINE; IMMUNOHISTOCHEMISTRY; MALE; MICROSCOPY, IMMUNOELECTRON; PRESYNAPTIC TERMINALS; PUTAMEN; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, OPIOID, MU; SYNAPSES;

EID: 0029910853     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19961125)375:4<659::AID-CNE7>3.0.CO;2-0     Document Type: Article

References (61)

1. Aronin, N., M. DiFiglia, G.A. Graveland, W.J. Schwartz, and J.-Y. Wu (1984) Localization of immunoreactive enkephalins in GABA synthesizing neurons of the rat neostriatum. Brain Res. 300:376-380.
2. Arvidsson, U., M. Riedl, S. Chakrabarti, J.-H. Lee, A.H. Nakano, R.J. Dado, H.H. Loh, P.-Y. Law, M.W. Wessendorf, and R. Elde (1995) Distribution and targeting of a μ-opioid receptor (MOR1) in brain and spinal cord. J. Neurosci. 15:3328-3341.
3. Atweh, S.F., and M.J. Kuhar (1983) Distribution and physiological significance of opioid receptors in the brain. Br. Med. Bull. 39:47-52.
4. Beier, K. (1992) Light microscopic morphometric analysis of peroxisomes by automatic image analysis: Advantages of immunostaining over the alkaline DAB method. J. Histochem. Cytochem. 40:115-121.
5. Bolam, J.P., J.F. Powell, J.Y. Wu, and A.D. Smith (1985) 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. 237:1-20.
6. Bouyer, J.J., R.J. Miller, and V.M. Pickel (1984) Ultrastructural relation between cortical efferents and terminals containing enkephalin-like immunoreactivity in rat neostriatum. Regulatory Peptides 8:105-115.
7. Branchereau, P., E.J. Van Bockstaele, J. Chan, and V.M. Pickel (1995) Ultrastructural characterization of neurons recorded intracellularly in vivo and injected with lucifer yellow: Advantages of immunogold-silver vs. immunoperoxidase labeling. Microsc. Res. Tech. 30:427-436.
8. Broadwell, R.D., and A.M. Cataldo (1983) The neuronal endoplasmic reticulum: Its cytochemistry and contribution to the endomembrane system. I. Cell bodies and dendrites. J. Histochem. Cytochem. 31:1077-1088.
9. Carlin, R.K., D.J. Grab, R.S. Cohen, and P. Siekevitz (1980) Isolation and characterization of postsynaptic densities from various brain regions: Enrichment of different types of postsynaptic densities. J. Cell Biol. 86:831-845.
10. Chan, J., C. Aoki, and V.M. Pickel (1990) Optimization of differential immunogold-silver and peroxidase labeling with maintenance of ultrastructure in brain sections before plastic embedding. J. Neurosci. Methods 33:113-127.
11. Chen, Y., A. Mestek, J. Liu, J.A. Hurley, and L. Yu (1993) Molecular cloning and functional expression of a μ-opioid receptor from rat brain. Mol. Pharmacol. 44:8-12.
12. 5-enkephalin. Brain Res. (in press).
13. Dana, C., M. Vial, K. Leonard, A. Beauregard, P. Kitabgi, J.P. Vincent, W. Rostene, and A. Beaudet (1989) Electron microscopic localization of neurotensin binding sites in the midbrain tegmentum of the rat. I. Ventral tegmental area and the interfascicular nucleus. J. Neurosci. 9:2247-57.
14. Delfs, J.M., H. Kong, A. Mestek, Y. Chen, L. Yu, T. Reisine, and M.-F. Chesselet (1994) Expression of mu opioid receptor mRNA in rat brain: An in situ hybridization study at the single cell level. J. Comp. Neurol. 345:46-68.
15. Difiglia, M., T. Pasik, and P. Pasik (1980) Ultrastructure of Golgi-impregnated and gold-toned spiny and aspiny neurons in the monkey neostriatum. J. Neurocytol. 9:471-92.
16. Donoghue, J.P., and M. Herkenham (1986) Neostriatal projections from individual cortical fields conform to histochemically distinct striatal compartments in the rat. Brain Res. 365:397-403.
17. Fan, S.F., and S.M. Crain (1995) Dual regulation by mu, delta and kappa opioid receptor agonists of K+ conductance of DRG neurons and neuroblastoma X DRG neuron hybrid F11 cells. Brain Res. 696:97-105.
18. Faure, M.-P., D. Nouel, and A. Beaudet (1995) Axonal and dendritic transport of internalized neurotensin in rat mesostriatal dopaminergic neurons. Neuroscience 65:519-529.
19. Freund, T.F., J.F. Powell, and A.D. Smith (1984) Tyrosine hydroxylase-immunoreactive boutons in synaptic contact with identified striatonigral neurons, with particular reference to dendritic spines. Neuroscience 13:1189-1215.
20. Gerfen, C.R. (1984) The neostriatal mosaic: Compartmentalization of corticostriatal input and striatonigral output systems. Nature 311:461-464.
21. Gerfen, C.R. (1985) The neostriatal mosaic. I. compartmental organization of projections from the striatum to the substantia nigra in the rat. J. Comp. Neurol. 236:454-476.
22. Gerfen, C.R. (1989) The neostriatal mosaic: Striatal patch-matrix organization is related to cortical lamination. Science 246:385-388.
23. Gerfen, C.R., and W.S. Young III (1988) Distribution of striatonigral and striatopallidal peptidergic neurons in both patch and matrix compartments: An in situ hybridization histochemistry and fluorescent retrograde tracing study. Brain Res. 460:161-167.
24. Gerfen, C.R., M. Herkenham, and J. Thibault (1987) The neostriatal mosaic: II. Patch- and matrix-directed mesostriatal dopaminergic and non-dopaminergic systems. J. Neurosci. 7:3915-3934.
25. Hamel, E., and A. Beaudet (1987) Opioid receptors in rat neostriatum: Radioautographic distribution at the electron microscopic level. Brain Res. 401:239-257.
26. Herkenham, M. (1987) Mismatches between neurotransmitter and receptor localizations in brain: Observations and implications. Neuroscience 23:1-38.
27. Herkenham, M., and C.B. Pert (1982) Light microscopic localization of brain opiate receptors: A general autoradiographic method which preserves tissue quality. J. Neurosci. 2:1129-1149.
28. Jacob, M.H., and D.K. Berg (1983) The ultrastructural localization of alpha-bungarotoxin binding sites in relation to synapses of chick ciliary ganglion neurons. J. Neurosci. 3:260-271.
29. Jiang, Z.G., and R.A. North (1992) Pre- and Postsynaptic inhibition by opioids in rat striatum. J. Neurosci. 12:356-361.
30. Kaneko, T., M. Minami, M. Satoh, and N. Mizuno (1995) Immunocytochemical localization of μ-opioid receptor in the rat caudate-putamen. Neurosci. Lett. 184:149-152.
31. Lee, J.M., F. De Leon-Jones, J.Z. Fields, and R.F. Ritzmann (1987) Cyclo (Leu-Gly) attenuates the striatal dopaminergic supersensitivity induced by chronic morphine. Alcohol Drug Res. 7:1-10.
32. Leranth, C., and V.M. Pickel (1989) Electron microscopic pre-embedding double immunostaining methods. In L. Heimer and L. Zaborsky (eds): Tract Tracing Methods 2, Recent Progress. New York: Plenum, pp. 129-172.
33. Lewis, M.E., H. Khachaturian, and S.J. Watson (1985) Combined autoradiographic-immunocytochemical analysis of opioid receptors and opioid peptide neuronal systems in brain. Peptides 6 Suppl. 1:37-47.
34. Loose, M.D., O.K. Ronnekleiv, and M.J. Kelly (1991) Neurons in the rat arcuate nucleus are hyperpolarized by GABAB and mu-opioid receptor agonists: Evidence for convergence at a ligand-gated potassium conductance. Neuroendocrinology 54:537-544.
35. Maloteaux, J.M., and E. Hermans (1994) Agonist-induced muscarinic cholinergic receptor internalization, recycling and degradation in cultured neuronal cells. Cellular mechanisms and role in desensitization. Biochem. Pharmacol. 47:77-88.
36. Mansour, A., H. Khachaturian, M.E. Lewis, H. Akil, and S.J. Watson (1987) Autoradiographic differentiation of mu, delta, and kappa opioid receptors in the rat forebrain and midbrain. J. Neurosci. 7:2445-2464.
37. Mansour, A., C.A. Fox, R.C. Thompson, H. Akil, and S.J. Watson (1994) μ-oipiod receptor mRNA expression in the rat CNS: Comparison to μ-receptor binding. Brain Res. 643:245-265.
38. Mansour, A., C.A. Fox, S. Burke, H. Akil, and S.J. Watson (1995) Immunohistochemical localization of the cloned μ opioid receptor in the rat CNS. J. Chem. Neuroanat. 8:283-305.
39. Marcel, D., H. Pollard, P. Verroust, J.C. Schwartz, and A. Beaudet (1990) Electron microscopic localization of immunoreactive enkephalinase (EC 3.4.24.11) in the neostriatum of the rat. J. Neurosci. 10:2804-2817.
40. Martin, W.R., C.G. Eades, J.A. Thompson, R.E. Huppler, and P.E. Gilbert (1976) The effects of morphine- and nalorphine-like drugs in the nondependent and morphine-dependent chronic spinal dog. J. Pharmacol. Exp. Ther. 197:517-532.
41. McLean, S. (1988) Axonal transport of opiate receptor subtypes. Peptides 9 Suppl. 1:85-89.
42. Milner, T.A., V.M. Pickel, and D.J. Reis (1989) Ultrastructural basis for interactions between central opioids and catecholamines. I. Rostral ventrolateral medulla. J. Neurosci. 9:2114-2130.
43. A receptors of cerebellar granule cells as determined by a quantitative immunogold method. J. Neurosci. 15:2948-2960.
44. Pasquini, F., P. Bochet, C. Garbay-Jaureguiberry, B.R. Roques, J. Rossier, and A. Beaudet (1992) Electron microscopic localization of photoaffinity-labelled delta opioid receptors in the neostriatum of the rat. J. Comp. Neurol. 326:229-244.
45. Paxinos, G., and C. Watson (1986) The Rat Brain in Stereotaxic Coordinates. Orlando, FL: Academic Press.
46. Peters, A., S.L. Palay, and H. deF. Webster (1991) The Fine Structure of the Nervous System. New York: Oxford University Press.
47. Pickel, V.M., and J. Chan (1990) Spiny neurons lacking choline acetyltransferase immunoreactivity are major targets of cholinergic and catecholaminergic terminals in rat striatum. J. Neurosci. Res. 25:263-280.
48. Pickel, V.M., K.K. Sumal, S.C. Beckley, R.J. Miller, and D.J. Reis (1980) Immunocytochemical localization of enkephalin in the neostriatum of rat brain: A light and electron microscopic study. J. Comp. Neurol. 189:721-738.
49. Pickel, V.M., J. Chan, and C. Aoki (1993) Electron microscopic immunocytochemical labeling of endogenous and/or transported antigens in rat brain using silver-intensified one-nanometre colloidal gold. In A.C. Cuello (ed): Immunohistochemistry II. Chichester: Wiley, pp. 265-280.
50. Raynor, K., H. Kong, Y. Chen, K. Yasuda, L. Yu, G.I. Bell, and T. Reisine (1994) Pharmacological characterization of the cloned kappa, delta and mu opioid receptors. Mol. Pharmacol. 45:330-334.
51. Reynolds, E.S. (1963) The use of lead citrate and high pH as an electron-opaque stain in electron microscopy. J. Cell Biol. 17:208-212.
52. Schmitt, F.O. (1984) Molecular regulators of brain function: A new view. Neuroscience 13:991-1001.
53. Stefani, A., D.J. Surmeier, and G. Bernardi (1994) Opioids decrease high-voltage activated calcium currents in acutely dissociated neostriatal neurons. Brain Res. 642:339-343.
54. Surratt, C.K., P.S. Johnson, A. Moriwaki, B.K. Seidleck, C.J. Blaschak, J.B. Wang, and G.R. Uhl (1994) - μ opiate receptor. Charged transmembrane domain amino acids are critical for agonist recognition and intrinsic activity. J. Biol. Chem. 269:20548-20553.
55. 5-enkephalin. J. Neurosci. 16:4162-4173.
56. Thompson, R.C., A. Mansour, H. Akil, and S.J. Watson (1993) Cloning and pharmacological characterization of a rat μ opioid receptor. Neuron 11:1-20.
57. Trovero, F., D. Herve, M. Desban, J. Glowinski, and J.-P. Tassin (1990) Striatal opiate mu-receptors are not located on dopamine nerve endings in the rat. Neuroscience 39:313-321.
58. Walter, S., and K. Kuschinsky (1989) Conditioning of morphine-induced locomotor activity and stereotyped behaviour in rats. J. Neural Transm. Gen. Sect. 78:231-247.
59. Wang, J.B., Y. Imai, C.M. Eppler, P. Gregor, C.E. Spivak, and G.R. Uhl (1993) μ opiate receptor: cDNA cloning and expression. Proc. Natl. Acad. Sci. U.S.A. 90:10230-10234.
60. 2+ channels. J. Neurosci. 75:4124-4132.
61. Young, W.S., J.K. Wamsley, M.A. Zarbiw, and M.J. Kuhar (1980) Opioid receptors undergo axonal transport. Science 210:76-77.