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Sex differences in subcellular distribution of delta opioid receptors in the rat hippocampus in response to acute and chronic stress

Drug addiction requires associative learning processes that critically involve hippocampal circuits, including the opioid system. We recently found that acute and chronic stress, important regulators of addictive processes, affect hippocampal opioid levels and mu opioid receptor trafficking in a sex...

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Autores principales: Mazid, Sanoara, Hall, Baila S., Odell, Shannon C., Stafford, Khalifa, Dyer, Andreina D., Van Kempen, Tracey A., Selegean, Jane, McEwen, Bruce S., Waters, Elizabeth M., Milner, Teresa A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Elsevier 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5145913/
https://www.ncbi.nlm.nih.gov/pubmed/27981195
http://dx.doi.org/10.1016/j.ynstr.2016.11.002
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author Mazid, Sanoara
Hall, Baila S.
Odell, Shannon C.
Stafford, Khalifa
Dyer, Andreina D.
Van Kempen, Tracey A.
Selegean, Jane
McEwen, Bruce S.
Waters, Elizabeth M.
Milner, Teresa A.
author_facet Mazid, Sanoara
Hall, Baila S.
Odell, Shannon C.
Stafford, Khalifa
Dyer, Andreina D.
Van Kempen, Tracey A.
Selegean, Jane
McEwen, Bruce S.
Waters, Elizabeth M.
Milner, Teresa A.
author_sort Mazid, Sanoara
collection PubMed
description Drug addiction requires associative learning processes that critically involve hippocampal circuits, including the opioid system. We recently found that acute and chronic stress, important regulators of addictive processes, affect hippocampal opioid levels and mu opioid receptor trafficking in a sexually dimorphic manner. Here, we examined whether acute and chronic stress similarly alters the levels and trafficking of hippocampal delta opioid receptors (DORs). Immediately after acute immobilization stress (AIS) or one-day after chronic immobilization stress (CIS), the brains of adult female and male rats were perfusion-fixed with aldehydes. The CA3b region and the dentate hilus of the dorsal hippocampus were quantitatively analyzed by light microscopy using DOR immunoperoxidase or dual label electron microscopy for DOR using silver intensified immunogold particles (SIG) and GABA using immunoperoxidase. At baseline, females compared to males had more DORs near the plasmalemma of pyramidal cell dendrites and about 3 times more DOR-labeled CA3 dendritic spines contacted by mossy fibers. In AIS females, near-plasmalemmal DOR-SIGs decreased in GABAergic hilar dendrites. However, in AIS males, near-plasmalemmal DOR-SIGs increased in CA3 pyramidal cell and hilar GABAergic dendrites and the percentage of CA3 dendritic spines contacted by mossy fibers increased to about half that seen in unstressed females. Conversely, after CIS, near-plasmalemmal DOR-SIGs increased in hilar GABA-labeled dendrites of females whereas in males plasmalemmal DOR-SIGs decreased in CA3 pyramidal cell dendrites and near-plasmalemmal DOR-SIGs decreased hilar GABA-labeled dendrites. As CIS in females, but not males, redistributed DOR-SIGs near the plasmalemmal of hilar GABAergic dendrites, a subsequent experiment examined the acute affect of oxycodone on the redistribution of DOR-SIGs in a separate cohort of CIS females. Plasmalemmal DOR-SIGs were significantly elevated on hilar interneuron dendrites one-hour after oxycodone (3 mg/kg, I.P.) administration compared to saline administration in CIS females. These data indicate that DORs redistribute within CA3 pyramidal cells and dentate hilar GABAergic interneurons in a sexually dimorphic manner that would promote activation and drug related learning in males after AIS and in females after CIS.
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spelling pubmed-51459132016-12-15 Sex differences in subcellular distribution of delta opioid receptors in the rat hippocampus in response to acute and chronic stress Mazid, Sanoara Hall, Baila S. Odell, Shannon C. Stafford, Khalifa Dyer, Andreina D. Van Kempen, Tracey A. Selegean, Jane McEwen, Bruce S. Waters, Elizabeth M. Milner, Teresa A. Neurobiol Stress Original Research Article Drug addiction requires associative learning processes that critically involve hippocampal circuits, including the opioid system. We recently found that acute and chronic stress, important regulators of addictive processes, affect hippocampal opioid levels and mu opioid receptor trafficking in a sexually dimorphic manner. Here, we examined whether acute and chronic stress similarly alters the levels and trafficking of hippocampal delta opioid receptors (DORs). Immediately after acute immobilization stress (AIS) or one-day after chronic immobilization stress (CIS), the brains of adult female and male rats were perfusion-fixed with aldehydes. The CA3b region and the dentate hilus of the dorsal hippocampus were quantitatively analyzed by light microscopy using DOR immunoperoxidase or dual label electron microscopy for DOR using silver intensified immunogold particles (SIG) and GABA using immunoperoxidase. At baseline, females compared to males had more DORs near the plasmalemma of pyramidal cell dendrites and about 3 times more DOR-labeled CA3 dendritic spines contacted by mossy fibers. In AIS females, near-plasmalemmal DOR-SIGs decreased in GABAergic hilar dendrites. However, in AIS males, near-plasmalemmal DOR-SIGs increased in CA3 pyramidal cell and hilar GABAergic dendrites and the percentage of CA3 dendritic spines contacted by mossy fibers increased to about half that seen in unstressed females. Conversely, after CIS, near-plasmalemmal DOR-SIGs increased in hilar GABA-labeled dendrites of females whereas in males plasmalemmal DOR-SIGs decreased in CA3 pyramidal cell dendrites and near-plasmalemmal DOR-SIGs decreased hilar GABA-labeled dendrites. As CIS in females, but not males, redistributed DOR-SIGs near the plasmalemmal of hilar GABAergic dendrites, a subsequent experiment examined the acute affect of oxycodone on the redistribution of DOR-SIGs in a separate cohort of CIS females. Plasmalemmal DOR-SIGs were significantly elevated on hilar interneuron dendrites one-hour after oxycodone (3 mg/kg, I.P.) administration compared to saline administration in CIS females. These data indicate that DORs redistribute within CA3 pyramidal cells and dentate hilar GABAergic interneurons in a sexually dimorphic manner that would promote activation and drug related learning in males after AIS and in females after CIS. Elsevier 2016-11-10 /pmc/articles/PMC5145913/ /pubmed/27981195 http://dx.doi.org/10.1016/j.ynstr.2016.11.002 Text en © 2016 The Authors http://creativecommons.org/licenses/by-nc-nd/4.0/ This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
spellingShingle Original Research Article
Mazid, Sanoara
Hall, Baila S.
Odell, Shannon C.
Stafford, Khalifa
Dyer, Andreina D.
Van Kempen, Tracey A.
Selegean, Jane
McEwen, Bruce S.
Waters, Elizabeth M.
Milner, Teresa A.
Sex differences in subcellular distribution of delta opioid receptors in the rat hippocampus in response to acute and chronic stress
title Sex differences in subcellular distribution of delta opioid receptors in the rat hippocampus in response to acute and chronic stress
title_full Sex differences in subcellular distribution of delta opioid receptors in the rat hippocampus in response to acute and chronic stress
title_fullStr Sex differences in subcellular distribution of delta opioid receptors in the rat hippocampus in response to acute and chronic stress
title_full_unstemmed Sex differences in subcellular distribution of delta opioid receptors in the rat hippocampus in response to acute and chronic stress
title_short Sex differences in subcellular distribution of delta opioid receptors in the rat hippocampus in response to acute and chronic stress
title_sort sex differences in subcellular distribution of delta opioid receptors in the rat hippocampus in response to acute and chronic stress
topic Original Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5145913/
https://www.ncbi.nlm.nih.gov/pubmed/27981195
http://dx.doi.org/10.1016/j.ynstr.2016.11.002
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