Research report Electron microscopic evidence for coexistence of leucine5-enkephalin and γ-aminobutyric acid in a subpopulation of axon terminals in the rat locus coeruleus region

Brain Research

Volumn 746, Issue 1-2, 1997, Pages 171-182

  Van Bockstaele, Elisabeth J ^a   Chan, June ^b  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b Department of Obstetrics Gynecology   (United States)

Author keywords

Dorsal medulla; Inhibitory amino acid; Norepinephrine; Opioid peptide

Indexed keywords

4 AMINOBUTYRIC ACID; LEUCINE ENKEPHALIN;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ELECTRON MICROSCOPY; IMMUNOCYTOCHEMISTRY; LOCUS CERULEUS; MALE; NONHUMAN; NORADRENERGIC NERVE; PRIORITY JOURNAL; RAT; SYNAPSE; SYNAPSE VESICLE; ANIMAL; CHEMISTRY; CYTOLOGY; DENDRITE; IMMUNOELECTRON MICROSCOPY; IMMUNOHISTOCHEMISTRY; NERVE CELL; SILVER STAINING; SPRAGUE DAWLEY RAT; SYNAPTOSOME; ULTRASTRUCTURE;

ANIMALS; DENDRITES; ENKEPHALIN, LEUCINE; GAMMA-AMINOBUTYRIC ACID; IMMUNOHISTOCHEMISTRY; LOCUS COERULEUS; MALE; MICROSCOPY, IMMUNOELECTRON; NEURONS; PRESYNAPTIC TERMINALS; RATS; RATS, SPRAGUE-DAWLEY; SILVER STAINING;

EID: 0031584063     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-8993(96)01194-8     Document Type: Article

References (48)

1. Aston-Jones, G., Shipley, M.T. and Grzanna, R., The locus coeruleus, A5, and A7 noradrenergic cell groups. In G. Paxinos (Ed.), The Rat Nervous System, 2nd edn., Academic Press, New York, 1995, pp. 183-206.
2. Aston-Jones, G., Shipley, M.T., Chouvet, G., Ennis, M., Van Bockstaele, E., Pieribone, V., Shiekhattar, R., Akaoka, H., Drolet, G. and Astier, B., Afferent regulation of locus coeruleus neurons: anatomy, physiology and pharmacology, Prog. Brain Res., 88 (1991) 47-75.
3. Bird, S.J. and Kuhar, M.J., Iontophoretic application of opiates to the locus coeruleus, Brain Res., 122 (1977) 523-533.
4. Bloom, F.E., Battenberg, E., Rossier, J., Ling, N. and Guillemin, R., Neurons containing β-endorphin in rat brain exist separately from those containing enkephalin: immunocytochemical studies, Proc. Natl. Acad. Sci. USA, 75 (1978) 1591-1595.
5. Carlin, R.K., Grab, D.J., Cohen, R.S. and Siekevitz, P., Isolation and characterization of postsynaptic densities from various brain regions: Enrichment of different types of postsynaptic densities, J. Cell Biol., 86 (1980) 831-832.
6. Chan, J., Aoki, C. and 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.
7. Charnay, Y., Leger, L., Dray, F., Berod, A., Jouvet, M., Pujol J.-F. and Dubois, P.M., Evidence for the presence of enkephalin in catecholaminergic neurons of the cat locus coeruleus, Neurosci. Lett., 30 (1982) 147-151.
8. Commons, K. and Milner, T.A., Ultrastructural heterogeneity of enkephalin-containing terminals in the rat hippocampal formation, J. Comp. Neurol., 358 (1995) 324-342.
9. Drolet, G., Van Bockstaele, E.J. and Aston-Jones, G., Robust enkephalin innervation of the locus coeruleus from the rostral medulla, J. Neurosci., 12 (1992) 3162-3174.
10. Ennis, M. and Aston-Jones, G., GABA-mediated inhibition of locus coeruleus from the dorsomedial rostral medulla, J. Neurosci., 9 (1989) 2973-2981.
11. Fallon, J.H. and Leslie, F.M., Distribution of dynorphin and enkephalin peptides in the rat brain, J. Comp. Neurol., 249 (1986) 293-336.
12. Finley, J.C.W., Maderdrut, J.L. and Petrusz, P., The immunocytochemical localization of enkephalin in the central nervous system of the rat, J. Comp. Neurol., 198 (1981) 541-565.
13. Goldman, J.E. and Abramson, B., Cyclic AMP-induced shape changes of astrocytes are accompanied by rapid depolymerization of actin, Brain Res., 582 (1990) 189-196.
14. Gray, E.G., Axosomatic and axo-dendritic synapses of the cerebral cortex: an electron microscopic study, J. Anat., 93 (1959) 420-433.
15. 2-Met-enkephalinamide in primary astroglial cultures from various brain areas, visualized by autoradiography, Brain Res., 289 (1983) 189-196.
16. B receptors on cultured astrocytes of rat CNS: autoradiographic binding studies, Exp. Brain Res., 80 (1990) 621-625.
17. Hsu, S.M., Raine, L. and Fanger, H., Use of avidin-biotin peroxidase complex (ABC) in immunoperoxidase techniques: A comparison between ABC and unlabeled antibody (PAP) procedures, J. Histochem. Cytochem., 29 (1981) 557-580.
18. Iijima, K., Kobayahi, R. and Kojima, N., Immunohistochemical studies on GABAergic neurons in the rat locus coeruleus, with special reference to their relationship to astrocytes, Acta Anat., 129 (1988) 116-122.
19. Khachaturian, H., Lewis, M.E. and Watson, S.J., Enkephalin systems in diencephalon and brainstem of the rat, J. Comp. Neurol., 220 (1983) 310-320.
20. Lauder, J.M., Han, V.K., Henderson, P., Verdoom, T. and Towle, A.C., Prenatal ontogeny of the GABAergic system in the rat brain: an immunohistochemical study, Neuroscience, 19 (1986) 465-493.
21. Leranth, C. and Pickel, V.M., Electron microscopic pre-embedding double immunostaining methods. In L. Heimer and L. Zaborsky (Eds.), Tract-tracing Methods 2, Recent Progress, Plenum Press, New York, 1989, pp. 129-172.
22. Lima, D., Avelino, A. and Coimbra, A., Morphological characterization of marginal (lamina I) neurons immunoreactive for substance P, enkephalin, dynorphin and γ-aminobutyric acid in the rat spinal cord, J. Chem. Neuroanat., 6 (1993) 43-52.
23. Maneuf, Y.P., Mitchell, I.J., Crossman, A.R. and Brotchie, J.M., On the role of enkephalin cotransmission in the GABAergic striatal efferents to the globus pallidus, Exp. Neurol., 125 (1994) 65-71.
24. Milner, T.A., Pickel, V.M. and Reis, D.J., Ultrastructural basis for interactions between central opioids and catecholamines. I. Rostral ventrolateral medulla, J. Neurosci., 9 (1989) 2114-2130.
25. Mugnaini, E. and Oertel, W.H., An atlas of the distribution of GABAergic neurons and terminals in the rat CNS as revealed by GAD immunohistochemistry. In A. Bjorklund and T. Hokfelt (Eds.), Handbook of Chemical Neuroanatomy, Vol. 4, Elsevier, Amsterdam, 1985, pp. 436-608.
26. North, R.A. and Williams, J.T., On the potassium conductance increase by opioids in rat locus coeruleus neurons, J. Physiol., 364 (1985) 265-280.
27. Osmanovic, S.S. and Shefner, S.A., γ-Aminobutyric acid responses in rat locus coeruleus neurons in vitro: a current clamp and voltage clamp study, J. Physiol., 421 (1990) 151-170.
28. Pepper, C.M. and Henderson, G., Opiates and opioid peptides hyperpolarize locus coeruleus neurons in vitro, Science, 209 (1980) 394-396.
29. Peters, A., Palay, S.L. and Webster, H.deF., The Fine Structure of the Nervous System, Oxford University Press, New York, 1991.
30. Pickel, V.M. and Chan, J., Met-enkephalin is localized within axon terminals in the subfornical organ: vascular contacts and interactions with neurons containing γ-aminobutyric acid, J. Neurosci. Res., 37 (1994) 735-749.
31. Pickel, V.M., Chan, J., Veznedaroglu, E. and Milner, T.A., Neuropeptide Y and dynorphin immunoreactive large dense core vesicles are strategically localized for presynaptic modulation in the hippocampal formation and substantia nigra, Synapse, 19 (1996) 160-169.
32. Ribak, C.E. and Roberts, R.C., The GABAergic synapses in the brain identified with antisera to GABA and its synthesizing enzyme, glutamate decarboxylase, J. Electron Microsc. Techn., 15 (1990) 34-48.
33. Sesack, S.R. and Pickel, V.M., Ultrastructural relationships between terminals immunoreactive for enkephalin, GABA, or both transmitters in the rat ventral tegmental area, Brain Res., 672 (1995) 261-275.
34. Simantov, R., Kuhar, M.J., Uhl, G.R. and Snyder, S.H., Opioid peptide enkephalin: immunohistochemical mapping in rat central nervous system, Proc. Natl. Acad. Sci. USA, 74 (1977) 2167-2171.
35. Stiene-Martin, A., Mattson, M.P. and Hauser, K.F., Opiates selectively increase intracellular calcium in developing type-1 astrocytes: role of calcium in morphine induced morphologic differentiation, Dev. Brain Res., 76 (1993) 189-196.
36. Swanson, L.W., The locus coeruleus: a cytoarchitectonic, golgi and immunohistochemical study in the albino rat, Brain Res., 110 (1976) 39-56.
37. Tempel, A. and 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, 844 (1987) 4308-4312.
38. Thureson-Klein, A.K. and Klein, R.L., Exocytosis from neuronal large dense cored vesicles, Int. Res. Cytol., 121 (1990) 207-211.
39. Todd, A.J., Spike R.C., Russell G. and Johnston, H.M., Immunohistochemical evidence that Met-enkephalin and GABA co-exist in some neurons in rat dorsal horn, Brain Res., 584 (1992) 149-156.
40. Van Bockstaele, E.J., Colago, E.E.O., Cheng, P.Y., Moriwaki, A., Uhl, G.R. and Pickel, V.M., Ultrastructural evidence for prominent distribution of the μ-opioid recpetor at extrasynaptic sites on noradrenergic dendrites in the rat nucleus locus coeruleus, J. Neurosci., 16 (1996) 5037-5048.
41. Van Bockstaele, E.J., Branchereau, P. and Pickel, V.M., Morphologically heterogenous methionine-enkephalin terminals form synapses with tyrosine hydroxylase-containing dendrites in the rat nucleus locus coeruleus, J. Comp. Neurol., 363 (1995) 423-438.
42. Van Bockstaele, E.J., Sesack, S.R. and Pickel, V.M., Dynorphin-immunoreactive terminals in the rat nucleus accumbens: cellular sites for modulation of target neurons and interactions with catecholamine afferents, J. Comp. Neurol., 341 (1994) 1-15.
43. Wang, Q.P., Guan, J.L. and Nakai, Y., Immunoelectron microscopy of enkephalinergic innervation of GABAergic neurons in the periaqueductal gray, Brain Res., 665 (1994) 39-46.
44. Wang, Q.P. and Nakai, Y., Enkephalinergic innervation of GABAergic neurons in the dorsal raphe nucleus of the rat, Brain Res. Bull., 32 (1993) 315-320.
45. Watt, C.B. and Glazebrook, P.A., Interaction between enkephalin and γ-aminobutyric acid in the chicken retina: a double label immunoelectron microscopic analysis, J. Comp. Neurol., 342 (1994) 378-388.
46. Watt, C.B. and Florack, V.J., Interaction between enkephalin and GABA in the chicken retina: further analyses of coexisting relationships, Brain Res., 634 (1994) 317-324.
47. Williams, J.T., Egan, T.M. and North, R.A., Enkephalin opens potassium channels on mammalian central neurons, Nature, 299 (1982) 74-77.
48. Williams, J.T., Bobker, D.H. and Harris, G.C., Synaptic potentials in locus coeruleus neurons in brain slices, Prog. Brain Res., 88 (1991) 167-172.