Sex and chronic stress alter delta opioid receptor distribution within rat hippocampal CA1 pyramidal cells following behavioral challenges

Following oxycodone (Oxy) conditioned place preference (CPP), delta opioid receptors (DORs) differentially redistribute in hippocampal CA3 pyramidal cells in female and male rats in a manner that would promote plasticity and opioid-associative learning processes. However, following chronic immobiliz...

Full description

Bibliographic Details
Main Authors: Batsheva R. Rubin, Megan A. Johnson, Jared M. Berman, Ellen Goldstein, Vera Pertsovskaya, Yan Zhou, Natalina H. Contoreggi, Andreina G. Dyer, Jason D. Gray, Elizabeth M. Waters, Bruce S. McEwen, Mary Jeanne Kreek, Teresa A. Milner
Format: Article
Language:English
Published: Elsevier 2020-11-01
Series:Neurobiology of Stress
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2352289520300266
_version_ 1818325429469052928
author Batsheva R. Rubin
Megan A. Johnson
Jared M. Berman
Ellen Goldstein
Vera Pertsovskaya
Yan Zhou
Natalina H. Contoreggi
Andreina G. Dyer
Jason D. Gray
Elizabeth M. Waters
Bruce S. McEwen
Mary Jeanne Kreek
Teresa A. Milner
author_facet Batsheva R. Rubin
Megan A. Johnson
Jared M. Berman
Ellen Goldstein
Vera Pertsovskaya
Yan Zhou
Natalina H. Contoreggi
Andreina G. Dyer
Jason D. Gray
Elizabeth M. Waters
Bruce S. McEwen
Mary Jeanne Kreek
Teresa A. Milner
author_sort Batsheva R. Rubin
collection DOAJ
description Following oxycodone (Oxy) conditioned place preference (CPP), delta opioid receptors (DORs) differentially redistribute in hippocampal CA3 pyramidal cells in female and male rats in a manner that would promote plasticity and opioid-associative learning processes. However, following chronic immobilization stress (CIS), males do not acquire Oxy-CPP and the trafficking of DORs in CA3 pyramidal neurons is attenuated. Here, we examined the subcellular distribution of DORs in CA1 pyramidal cells using electron microscopy in these same cohorts. CPP: Saline (Sal)-females compared to Sal-males have more cytoplasmic and total DORs in dendrites and more DOR-labeled spines. Following Oxy-CPP, DORs redistribute from near-plasmalemma pools in dendrites to spines in males. CIS: Control females compared to control males have more near-plasmalemmal dendritic DORs. Following CIS, dendritic DORs are elevated in the cytoplasm in females and near-plasmalemma in males. CIS plus CPP: CIS Sal-females compared to CIS Sal-males have more DORs on the plasmalemma of dendrites and in spines. After Oxy, the distribution of DORs does not change in either females or males. Conclusion: Following Oxy-CPP, DORs within CA1 pyramidal cells remain positioned in naïve female rats to enhance sensitivity to DOR agonists and traffic to dendritic spines in naïve males where they can promote plasticity processes. Following CIS plus behavioral enrichment, DORs are redistributed within CA1 pyramidal cells in females in a manner that could enhance sensitivity to DOR agonists. Conversely, CIS plus behavioral enrichment does not alter DORs in CA1 pyramidal cells in males, which may contribute to their diminished capacity to acquire Oxy-CPP.
first_indexed 2024-12-13T11:44:20Z
format Article
id doaj.art-5dbdbc6efce8429e9a258232eb7e0889
institution Directory Open Access Journal
issn 2352-2895
language English
last_indexed 2024-12-13T11:44:20Z
publishDate 2020-11-01
publisher Elsevier
record_format Article
series Neurobiology of Stress
spelling doaj.art-5dbdbc6efce8429e9a258232eb7e08892022-12-21T23:47:33ZengElsevierNeurobiology of Stress2352-28952020-11-0113100236Sex and chronic stress alter delta opioid receptor distribution within rat hippocampal CA1 pyramidal cells following behavioral challengesBatsheva R. Rubin0Megan A. Johnson1Jared M. Berman2Ellen Goldstein3Vera Pertsovskaya4Yan Zhou5Natalina H. Contoreggi6Andreina G. Dyer7Jason D. Gray8Elizabeth M. Waters9Bruce S. McEwen10Mary Jeanne Kreek11Teresa A. Milner12Feil Family Brain and Mind Research Institute, Weill Cornell Medicine, 407 East 61st Street, New York, NY, 10065, United StatesFeil Family Brain and Mind Research Institute, Weill Cornell Medicine, 407 East 61st Street, New York, NY, 10065, United StatesFeil Family Brain and Mind Research Institute, Weill Cornell Medicine, 407 East 61st Street, New York, NY, 10065, United StatesFeil Family Brain and Mind Research Institute, Weill Cornell Medicine, 407 East 61st Street, New York, NY, 10065, United StatesFeil Family Brain and Mind Research Institute, Weill Cornell Medicine, 407 East 61st Street, New York, NY, 10065, United StatesThe Laboratory of the Biology of Addictive Diseases, The Rockefeller University, 1230 York Avenue, New York, NY, 10065, United StatesFeil Family Brain and Mind Research Institute, Weill Cornell Medicine, 407 East 61st Street, New York, NY, 10065, United StatesFeil Family Brain and Mind Research Institute, Weill Cornell Medicine, 407 East 61st Street, New York, NY, 10065, United StatesHarold and Margaret Milliken Hatch Laboratory of Neuroendocrinology, The Rockefeller University, 1230 York Avenue, New York, NY, 10065, United StatesHarold and Margaret Milliken Hatch Laboratory of Neuroendocrinology, The Rockefeller University, 1230 York Avenue, New York, NY, 10065, United StatesHarold and Margaret Milliken Hatch Laboratory of Neuroendocrinology, The Rockefeller University, 1230 York Avenue, New York, NY, 10065, United StatesThe Laboratory of the Biology of Addictive Diseases, The Rockefeller University, 1230 York Avenue, New York, NY, 10065, United StatesFeil Family Brain and Mind Research Institute, Weill Cornell Medicine, 407 East 61st Street, New York, NY, 10065, United States; Harold and Margaret Milliken Hatch Laboratory of Neuroendocrinology, The Rockefeller University, 1230 York Avenue, New York, NY, 10065, United States; Corresponding author. Feil Family Brain and Mind Research Institute, Weill Cornell Medicine, 407 East 61st Street, RM 307 New York, NY 10065, United States.Following oxycodone (Oxy) conditioned place preference (CPP), delta opioid receptors (DORs) differentially redistribute in hippocampal CA3 pyramidal cells in female and male rats in a manner that would promote plasticity and opioid-associative learning processes. However, following chronic immobilization stress (CIS), males do not acquire Oxy-CPP and the trafficking of DORs in CA3 pyramidal neurons is attenuated. Here, we examined the subcellular distribution of DORs in CA1 pyramidal cells using electron microscopy in these same cohorts. CPP: Saline (Sal)-females compared to Sal-males have more cytoplasmic and total DORs in dendrites and more DOR-labeled spines. Following Oxy-CPP, DORs redistribute from near-plasmalemma pools in dendrites to spines in males. CIS: Control females compared to control males have more near-plasmalemmal dendritic DORs. Following CIS, dendritic DORs are elevated in the cytoplasm in females and near-plasmalemma in males. CIS plus CPP: CIS Sal-females compared to CIS Sal-males have more DORs on the plasmalemma of dendrites and in spines. After Oxy, the distribution of DORs does not change in either females or males. Conclusion: Following Oxy-CPP, DORs within CA1 pyramidal cells remain positioned in naïve female rats to enhance sensitivity to DOR agonists and traffic to dendritic spines in naïve males where they can promote plasticity processes. Following CIS plus behavioral enrichment, DORs are redistributed within CA1 pyramidal cells in females in a manner that could enhance sensitivity to DOR agonists. Conversely, CIS plus behavioral enrichment does not alter DORs in CA1 pyramidal cells in males, which may contribute to their diminished capacity to acquire Oxy-CPP.http://www.sciencedirect.com/science/article/pii/S2352289520300266Delta opioid receptorElectron microscopyPyramidal cellsOxycodone associative-learning
spellingShingle Batsheva R. Rubin
Megan A. Johnson
Jared M. Berman
Ellen Goldstein
Vera Pertsovskaya
Yan Zhou
Natalina H. Contoreggi
Andreina G. Dyer
Jason D. Gray
Elizabeth M. Waters
Bruce S. McEwen
Mary Jeanne Kreek
Teresa A. Milner
Sex and chronic stress alter delta opioid receptor distribution within rat hippocampal CA1 pyramidal cells following behavioral challenges
Neurobiology of Stress
Delta opioid receptor
Electron microscopy
Pyramidal cells
Oxycodone associative-learning
title Sex and chronic stress alter delta opioid receptor distribution within rat hippocampal CA1 pyramidal cells following behavioral challenges
title_full Sex and chronic stress alter delta opioid receptor distribution within rat hippocampal CA1 pyramidal cells following behavioral challenges
title_fullStr Sex and chronic stress alter delta opioid receptor distribution within rat hippocampal CA1 pyramidal cells following behavioral challenges
title_full_unstemmed Sex and chronic stress alter delta opioid receptor distribution within rat hippocampal CA1 pyramidal cells following behavioral challenges
title_short Sex and chronic stress alter delta opioid receptor distribution within rat hippocampal CA1 pyramidal cells following behavioral challenges
title_sort sex and chronic stress alter delta opioid receptor distribution within rat hippocampal ca1 pyramidal cells following behavioral challenges
topic Delta opioid receptor
Electron microscopy
Pyramidal cells
Oxycodone associative-learning
url http://www.sciencedirect.com/science/article/pii/S2352289520300266
work_keys_str_mv AT batshevarrubin sexandchronicstressalterdeltaopioidreceptordistributionwithinrathippocampalca1pyramidalcellsfollowingbehavioralchallenges
AT meganajohnson sexandchronicstressalterdeltaopioidreceptordistributionwithinrathippocampalca1pyramidalcellsfollowingbehavioralchallenges
AT jaredmberman sexandchronicstressalterdeltaopioidreceptordistributionwithinrathippocampalca1pyramidalcellsfollowingbehavioralchallenges
AT ellengoldstein sexandchronicstressalterdeltaopioidreceptordistributionwithinrathippocampalca1pyramidalcellsfollowingbehavioralchallenges
AT verapertsovskaya sexandchronicstressalterdeltaopioidreceptordistributionwithinrathippocampalca1pyramidalcellsfollowingbehavioralchallenges
AT yanzhou sexandchronicstressalterdeltaopioidreceptordistributionwithinrathippocampalca1pyramidalcellsfollowingbehavioralchallenges
AT natalinahcontoreggi sexandchronicstressalterdeltaopioidreceptordistributionwithinrathippocampalca1pyramidalcellsfollowingbehavioralchallenges
AT andreinagdyer sexandchronicstressalterdeltaopioidreceptordistributionwithinrathippocampalca1pyramidalcellsfollowingbehavioralchallenges
AT jasondgray sexandchronicstressalterdeltaopioidreceptordistributionwithinrathippocampalca1pyramidalcellsfollowingbehavioralchallenges
AT elizabethmwaters sexandchronicstressalterdeltaopioidreceptordistributionwithinrathippocampalca1pyramidalcellsfollowingbehavioralchallenges
AT brucesmcewen sexandchronicstressalterdeltaopioidreceptordistributionwithinrathippocampalca1pyramidalcellsfollowingbehavioralchallenges
AT maryjeannekreek sexandchronicstressalterdeltaopioidreceptordistributionwithinrathippocampalca1pyramidalcellsfollowingbehavioralchallenges
AT teresaamilner sexandchronicstressalterdeltaopioidreceptordistributionwithinrathippocampalca1pyramidalcellsfollowingbehavioralchallenges