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Electron microscopic evidence for coexistence of leucine5-enkephalin and gamma-aminobutyric acid in a subpopulation of axon terminals in the rat locus coeruleus region.
Brain Res. 1997 Jan 23; 746(1-2):171-82.BR

Abstract

We recently described ultrastructural evidence for morphologically heterogeneous axon terminals containing the endogenous opioid peptide, methionine5-enkephalin (ENK), that formed synapses with neurons containing the catecholamine synthesizing enzyme, tyrosine hydroxylase, in the locus coeruleus (LC) of the rat brain. The morphological characteristics of these terminals suggested that ENK may be co-localized with either an excitatory or inhibitory amino acid. To further test this hypothesis, we combined immunogold-silver localization of gamma-aminobutyric acid (GABA) and immunoperoxidase labeling for ENK in single sections through the LC, in the present study, to determine whether ENK and GABA were contained within single axon terminals. Light microscopic analysis of ENK and GABA immunoreactivities in the LC indicated that both transmitters were enriched in the dorsal pons. Although electron microscopy revealed that ENK and GABA were located primarily in axon terminals, some dendrites also contained immunolabeling for GABA. The dense core vesicles were consistently the most immunoreactive in ENK containing axon terminals and were identified toward the periphery of the axon terminal distal to the synaptic specialization. Axon terminals containing either ENK or GABA immunoreactivities contained pleomorphic vesicles as well as large dense core vesicles, varied in size and formed heterogeneous types of synaptic specializations (i.e. asymmetric vs. symmetric). Approximately 38% (n = 76) of the axon terminals containing ENK immunoreactivity (n = 200) also contained GABA. Some axon terminals containing peroxidase labeling for ENK (22%; n = 44) converged on common targets with GABA-labeled axon terminals. Finally, a few ENK-labeled axon terminals (14%; n = 28) formed asymmetric (excitatory-type) synapses with dendrites containing gold-silver labeling for GABA. The results, therefore, indicate that the opioid peptide, ENK, and the inhibitory amino acid, GABA, may influence LC neurons by concerted actions via (1) release from a common axon terminal, and (2) via separate sets of afferents converging on similar portions of the plasmalemma of target neurons. Furthermore, these studies also suggest a cellular substrate for opioid inhibition of LC neurons via activation (i.e. asymmetric synapses) of inhibitory GABAergic neurons. Future studies are required to determine whether the receptive sites for ENK and GABA are located at similar sites on the plasma membranes of LC neurons pre- or postsynaptically and whether there is differential release of either transmitter from single terminals in the LC.

Authors+Show Affiliations

Department of Pathology, Anatomy and Cell Biology, Jefferson Medical College, Thomas Jefferson University, Philadelphia, PA 19107, USA.No affiliation info available

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, P.H.S.

Language

eng

PubMed ID

9037496

Citation

Van Bockstaele, E J., and J Chan. "Electron Microscopic Evidence for Coexistence of Leucine5-enkephalin and Gamma-aminobutyric Acid in a Subpopulation of Axon Terminals in the Rat Locus Coeruleus Region." Brain Research, vol. 746, no. 1-2, 1997, pp. 171-82.
Van Bockstaele EJ, Chan J. Electron microscopic evidence for coexistence of leucine5-enkephalin and gamma-aminobutyric acid in a subpopulation of axon terminals in the rat locus coeruleus region. Brain Res. 1997;746(1-2):171-82.
Van Bockstaele, E. J., & Chan, J. (1997). Electron microscopic evidence for coexistence of leucine5-enkephalin and gamma-aminobutyric acid in a subpopulation of axon terminals in the rat locus coeruleus region. Brain Research, 746(1-2), 171-82.
Van Bockstaele EJ, Chan J. Electron Microscopic Evidence for Coexistence of Leucine5-enkephalin and Gamma-aminobutyric Acid in a Subpopulation of Axon Terminals in the Rat Locus Coeruleus Region. Brain Res. 1997 Jan 23;746(1-2):171-82. PubMed PMID: 9037496.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Electron microscopic evidence for coexistence of leucine5-enkephalin and gamma-aminobutyric acid in a subpopulation of axon terminals in the rat locus coeruleus region. AU - Van Bockstaele,E J, AU - Chan,J, PY - 1997/1/23/pubmed PY - 1997/1/23/medline PY - 1997/1/23/entrez SP - 171 EP - 82 JF - Brain research JO - Brain Res. VL - 746 IS - 1-2 N2 - We recently described ultrastructural evidence for morphologically heterogeneous axon terminals containing the endogenous opioid peptide, methionine5-enkephalin (ENK), that formed synapses with neurons containing the catecholamine synthesizing enzyme, tyrosine hydroxylase, in the locus coeruleus (LC) of the rat brain. The morphological characteristics of these terminals suggested that ENK may be co-localized with either an excitatory or inhibitory amino acid. To further test this hypothesis, we combined immunogold-silver localization of gamma-aminobutyric acid (GABA) and immunoperoxidase labeling for ENK in single sections through the LC, in the present study, to determine whether ENK and GABA were contained within single axon terminals. Light microscopic analysis of ENK and GABA immunoreactivities in the LC indicated that both transmitters were enriched in the dorsal pons. Although electron microscopy revealed that ENK and GABA were located primarily in axon terminals, some dendrites also contained immunolabeling for GABA. The dense core vesicles were consistently the most immunoreactive in ENK containing axon terminals and were identified toward the periphery of the axon terminal distal to the synaptic specialization. Axon terminals containing either ENK or GABA immunoreactivities contained pleomorphic vesicles as well as large dense core vesicles, varied in size and formed heterogeneous types of synaptic specializations (i.e. asymmetric vs. symmetric). Approximately 38% (n = 76) of the axon terminals containing ENK immunoreactivity (n = 200) also contained GABA. Some axon terminals containing peroxidase labeling for ENK (22%; n = 44) converged on common targets with GABA-labeled axon terminals. Finally, a few ENK-labeled axon terminals (14%; n = 28) formed asymmetric (excitatory-type) synapses with dendrites containing gold-silver labeling for GABA. The results, therefore, indicate that the opioid peptide, ENK, and the inhibitory amino acid, GABA, may influence LC neurons by concerted actions via (1) release from a common axon terminal, and (2) via separate sets of afferents converging on similar portions of the plasmalemma of target neurons. Furthermore, these studies also suggest a cellular substrate for opioid inhibition of LC neurons via activation (i.e. asymmetric synapses) of inhibitory GABAergic neurons. Future studies are required to determine whether the receptive sites for ENK and GABA are located at similar sites on the plasma membranes of LC neurons pre- or postsynaptically and whether there is differential release of either transmitter from single terminals in the LC. SN - 0006-8993 UR - https://www.unboundmedicine.com/medline/citation/9037496/Electron_microscopic_evidence_for_coexistence_of_leucine5_enkephalin_and_gamma_aminobutyric_acid_in_a_subpopulation_of_axon_terminals_in_the_rat_locus_coeruleus_region_ L2 - https://linkinghub.elsevier.com/retrieve/pii/S0006-8993(96)01194-8 DB - PRIME DP - Unbound Medicine ER -