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Selective Inhibition of Orexin-2 Receptors Prevents Stress-Induced ACTH Release in Mice

Orexins peptides exert a prominent role in arousal-related processes including stress responding, by activating orexin-1 (OX1R) and orexin-2 (OX2R) receptors located widely throughout the brain. Stress or orexin administration stimulates hyperarousal, adrenocorticotropic hormone (ACTH) and corticost...

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Autores principales: Yun, Sujin, Wennerholm, Michelle, Shelton, Jonathan E., Bonaventure, Pascal, Letavic, Michael A., Shireman, Brock T., Lovenberg, Timothy W., Dugovic, Christine
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5420581/
https://www.ncbi.nlm.nih.gov/pubmed/28533747
http://dx.doi.org/10.3389/fnbeh.2017.00083
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author Yun, Sujin
Wennerholm, Michelle
Shelton, Jonathan E.
Bonaventure, Pascal
Letavic, Michael A.
Shireman, Brock T.
Lovenberg, Timothy W.
Dugovic, Christine
author_facet Yun, Sujin
Wennerholm, Michelle
Shelton, Jonathan E.
Bonaventure, Pascal
Letavic, Michael A.
Shireman, Brock T.
Lovenberg, Timothy W.
Dugovic, Christine
author_sort Yun, Sujin
collection PubMed
description Orexins peptides exert a prominent role in arousal-related processes including stress responding, by activating orexin-1 (OX1R) and orexin-2 (OX2R) receptors located widely throughout the brain. Stress or orexin administration stimulates hyperarousal, adrenocorticotropic hormone (ACTH) and corticosterone release, and selective OX1R blockade can attenuate several stress-induced behavioral and cardiovascular responses but not the hypothalamic-pituitary-adrenal (HPA) axis activation. As opposed to OX1R, OX2R are preferentially expressed in the paraventricular hypothalamic nucleus which is involved in the HPA axis regulation. In the present study, we investigated the effects of a psychological stress elicited by cage exchange (CE) on ACTH release in two murine models (genetic and pharmacological) of selective OX2R inhibition. CE-induced stress produced a significant increase in ACTH serum levels. Mice lacking the OX2R exhibited a blunted stress response. Stress-induced ACTH release was absent in mice pre-treated with the selective OX2R antagonist JNJ-42847922 (30 mg/kg po), whereas pre-treatment with the dual OX1/2R antagonist SB-649868 (30 mg/kg po) only partially attenuated the increase of ACTH. To assess whether the intrinsic and distinct sleep-promoting properties of each antagonist could account for the differential stress response, a separate group of mice implanted with electrodes for standard sleep recording were orally dosed with JNJ-42847922 or SB-649868 during the light phase. While both compounds reduced the latency to non-rapid eye movement (NREM) sleep without affecting its duration, a prevalent REM-sleep promoting effect was observed only in mice treated with the dual OX1/2R antagonist. These data indicate that in a psychological stress model, genetic or pharmacological inhibition of OX2R markedly attenuated stress-induced ACTH secretion, as a separately mediated effect from the NREM sleep induction of OX2R antagonism.
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spelling pubmed-54205812017-05-22 Selective Inhibition of Orexin-2 Receptors Prevents Stress-Induced ACTH Release in Mice Yun, Sujin Wennerholm, Michelle Shelton, Jonathan E. Bonaventure, Pascal Letavic, Michael A. Shireman, Brock T. Lovenberg, Timothy W. Dugovic, Christine Front Behav Neurosci Neuroscience Orexins peptides exert a prominent role in arousal-related processes including stress responding, by activating orexin-1 (OX1R) and orexin-2 (OX2R) receptors located widely throughout the brain. Stress or orexin administration stimulates hyperarousal, adrenocorticotropic hormone (ACTH) and corticosterone release, and selective OX1R blockade can attenuate several stress-induced behavioral and cardiovascular responses but not the hypothalamic-pituitary-adrenal (HPA) axis activation. As opposed to OX1R, OX2R are preferentially expressed in the paraventricular hypothalamic nucleus which is involved in the HPA axis regulation. In the present study, we investigated the effects of a psychological stress elicited by cage exchange (CE) on ACTH release in two murine models (genetic and pharmacological) of selective OX2R inhibition. CE-induced stress produced a significant increase in ACTH serum levels. Mice lacking the OX2R exhibited a blunted stress response. Stress-induced ACTH release was absent in mice pre-treated with the selective OX2R antagonist JNJ-42847922 (30 mg/kg po), whereas pre-treatment with the dual OX1/2R antagonist SB-649868 (30 mg/kg po) only partially attenuated the increase of ACTH. To assess whether the intrinsic and distinct sleep-promoting properties of each antagonist could account for the differential stress response, a separate group of mice implanted with electrodes for standard sleep recording were orally dosed with JNJ-42847922 or SB-649868 during the light phase. While both compounds reduced the latency to non-rapid eye movement (NREM) sleep without affecting its duration, a prevalent REM-sleep promoting effect was observed only in mice treated with the dual OX1/2R antagonist. These data indicate that in a psychological stress model, genetic or pharmacological inhibition of OX2R markedly attenuated stress-induced ACTH secretion, as a separately mediated effect from the NREM sleep induction of OX2R antagonism. Frontiers Media S.A. 2017-05-08 /pmc/articles/PMC5420581/ /pubmed/28533747 http://dx.doi.org/10.3389/fnbeh.2017.00083 Text en Copyright © 2017 Yun, Wennerholm, Shelton, Bonaventure, Letavic, Shireman, Lovenberg and Dugovic. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Neuroscience
Yun, Sujin
Wennerholm, Michelle
Shelton, Jonathan E.
Bonaventure, Pascal
Letavic, Michael A.
Shireman, Brock T.
Lovenberg, Timothy W.
Dugovic, Christine
Selective Inhibition of Orexin-2 Receptors Prevents Stress-Induced ACTH Release in Mice
title Selective Inhibition of Orexin-2 Receptors Prevents Stress-Induced ACTH Release in Mice
title_full Selective Inhibition of Orexin-2 Receptors Prevents Stress-Induced ACTH Release in Mice
title_fullStr Selective Inhibition of Orexin-2 Receptors Prevents Stress-Induced ACTH Release in Mice
title_full_unstemmed Selective Inhibition of Orexin-2 Receptors Prevents Stress-Induced ACTH Release in Mice
title_short Selective Inhibition of Orexin-2 Receptors Prevents Stress-Induced ACTH Release in Mice
title_sort selective inhibition of orexin-2 receptors prevents stress-induced acth release in mice
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5420581/
https://www.ncbi.nlm.nih.gov/pubmed/28533747
http://dx.doi.org/10.3389/fnbeh.2017.00083
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