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Prenatal androgen treatment impairs the suprachiasmatic nucleus arginine-vasopressin to kisspeptin neuron circuit in female mice

Polycystic ovary syndrome (PCOS) is associated with elevated androgen and luteinizing hormone (LH) secretion and with oligo/anovulation. Evidence indicates that elevated androgens impair sex steroid hormone feedback regulation of pulsatile LH secretion. Hyperandrogenemia in PCOS may also disrupt the...

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Autores principales: Jamieson, Bradley B., Moore, Aleisha M., Lohr, Dayanara B., Thomas, Simone X., Coolen, Lique M., Lehman, Michael N., Campbell, Rebecca E., Piet, Richard
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9388912/
https://www.ncbi.nlm.nih.gov/pubmed/35992143
http://dx.doi.org/10.3389/fendo.2022.951344
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author Jamieson, Bradley B.
Moore, Aleisha M.
Lohr, Dayanara B.
Thomas, Simone X.
Coolen, Lique M.
Lehman, Michael N.
Campbell, Rebecca E.
Piet, Richard
author_facet Jamieson, Bradley B.
Moore, Aleisha M.
Lohr, Dayanara B.
Thomas, Simone X.
Coolen, Lique M.
Lehman, Michael N.
Campbell, Rebecca E.
Piet, Richard
author_sort Jamieson, Bradley B.
collection PubMed
description Polycystic ovary syndrome (PCOS) is associated with elevated androgen and luteinizing hormone (LH) secretion and with oligo/anovulation. Evidence indicates that elevated androgens impair sex steroid hormone feedback regulation of pulsatile LH secretion. Hyperandrogenemia in PCOS may also disrupt the preovulatory LH surge. The mechanisms through which this might occur, however, are not fully understood. Kisspeptin (KISS1) neurons of the rostral periventricular area of the third ventricle (RP3V) convey hormonal cues to gonadotropin-releasing hormone (GnRH) neurons. In rodents, the preovulatory surge is triggered by these hormonal cues and coincident timing signals from the central circadian clock in the suprachiasmatic nucleus (SCN). Timing signals are relayed to GnRH neurons, in part, via projections from SCN arginine-vasopressin (AVP) neurons to RP3V(KISS1) neurons. Because rodent SCN cells express androgen receptors (AR), we hypothesized that these circuits are impaired by elevated androgens in a mouse model of PCOS. In prenatally androgen-treated (PNA) female mice, SCN Ar expression was significantly increased compared to that found in prenatally vehicle-treated mice. A similar trend was seen in the number of Avp-positive SCN cells expressing Ar. In the RP3V, the number of kisspeptin neurons was preserved. Anterograde tract-tracing, however, revealed reduced SCN(AVP) neuron projections to the RP3V and a significantly lower proportion of RP3V(KISS1) neurons with close appositions from SCN(AVP) fibers. Functional assessments showed, on the other hand, that RP3V(KISS1) neuron responses to AVP were maintained in PNA mice. These findings indicate that PNA changes some of the neural circuits that regulate the preovulatory surge. These impairments might contribute to ovulatory dysfunction in PNA mice modeling PCOS.
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spelling pubmed-93889122022-08-20 Prenatal androgen treatment impairs the suprachiasmatic nucleus arginine-vasopressin to kisspeptin neuron circuit in female mice Jamieson, Bradley B. Moore, Aleisha M. Lohr, Dayanara B. Thomas, Simone X. Coolen, Lique M. Lehman, Michael N. Campbell, Rebecca E. Piet, Richard Front Endocrinol (Lausanne) Endocrinology Polycystic ovary syndrome (PCOS) is associated with elevated androgen and luteinizing hormone (LH) secretion and with oligo/anovulation. Evidence indicates that elevated androgens impair sex steroid hormone feedback regulation of pulsatile LH secretion. Hyperandrogenemia in PCOS may also disrupt the preovulatory LH surge. The mechanisms through which this might occur, however, are not fully understood. Kisspeptin (KISS1) neurons of the rostral periventricular area of the third ventricle (RP3V) convey hormonal cues to gonadotropin-releasing hormone (GnRH) neurons. In rodents, the preovulatory surge is triggered by these hormonal cues and coincident timing signals from the central circadian clock in the suprachiasmatic nucleus (SCN). Timing signals are relayed to GnRH neurons, in part, via projections from SCN arginine-vasopressin (AVP) neurons to RP3V(KISS1) neurons. Because rodent SCN cells express androgen receptors (AR), we hypothesized that these circuits are impaired by elevated androgens in a mouse model of PCOS. In prenatally androgen-treated (PNA) female mice, SCN Ar expression was significantly increased compared to that found in prenatally vehicle-treated mice. A similar trend was seen in the number of Avp-positive SCN cells expressing Ar. In the RP3V, the number of kisspeptin neurons was preserved. Anterograde tract-tracing, however, revealed reduced SCN(AVP) neuron projections to the RP3V and a significantly lower proportion of RP3V(KISS1) neurons with close appositions from SCN(AVP) fibers. Functional assessments showed, on the other hand, that RP3V(KISS1) neuron responses to AVP were maintained in PNA mice. These findings indicate that PNA changes some of the neural circuits that regulate the preovulatory surge. These impairments might contribute to ovulatory dysfunction in PNA mice modeling PCOS. Frontiers Media S.A. 2022-08-05 /pmc/articles/PMC9388912/ /pubmed/35992143 http://dx.doi.org/10.3389/fendo.2022.951344 Text en Copyright © 2022 Jamieson, Moore, Lohr, Thomas, Coolen, Lehman, Campbell and Piet https://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) and the copyright owner(s) 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 Endocrinology
Jamieson, Bradley B.
Moore, Aleisha M.
Lohr, Dayanara B.
Thomas, Simone X.
Coolen, Lique M.
Lehman, Michael N.
Campbell, Rebecca E.
Piet, Richard
Prenatal androgen treatment impairs the suprachiasmatic nucleus arginine-vasopressin to kisspeptin neuron circuit in female mice
title Prenatal androgen treatment impairs the suprachiasmatic nucleus arginine-vasopressin to kisspeptin neuron circuit in female mice
title_full Prenatal androgen treatment impairs the suprachiasmatic nucleus arginine-vasopressin to kisspeptin neuron circuit in female mice
title_fullStr Prenatal androgen treatment impairs the suprachiasmatic nucleus arginine-vasopressin to kisspeptin neuron circuit in female mice
title_full_unstemmed Prenatal androgen treatment impairs the suprachiasmatic nucleus arginine-vasopressin to kisspeptin neuron circuit in female mice
title_short Prenatal androgen treatment impairs the suprachiasmatic nucleus arginine-vasopressin to kisspeptin neuron circuit in female mice
title_sort prenatal androgen treatment impairs the suprachiasmatic nucleus arginine-vasopressin to kisspeptin neuron circuit in female mice
topic Endocrinology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9388912/
https://www.ncbi.nlm.nih.gov/pubmed/35992143
http://dx.doi.org/10.3389/fendo.2022.951344
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