The direct response of the gonads to cues of stress in a temperate songbird species is season-dependent
The gonadotropin releasing hormone (GnRH) system in the hypothalamus is often considered the final point in integration of environmental cues as they pertain to the reproductive axis. However, cues such as stress and food availability are detectable in the plasma (as glucocorticoid and metabolic fue...
Main Authors: | , , |
---|---|
Format: | Article |
Language: | English |
Published: |
PeerJ Inc.
2013-08-01
|
Series: | PeerJ |
Subjects: | |
Online Access: | https://peerj.com/articles/139.pdf |
_version_ | 1827611064158650368 |
---|---|
author | Nicolette L. McGuire Annie Koh George E. Bentley |
author_facet | Nicolette L. McGuire Annie Koh George E. Bentley |
author_sort | Nicolette L. McGuire |
collection | DOAJ |
description | The gonadotropin releasing hormone (GnRH) system in the hypothalamus is often considered the final point in integration of environmental cues as they pertain to the reproductive axis. However, cues such as stress and food availability are detectable in the plasma (as glucocorticoid and metabolic fuel fluctuations). Vertebrate gonads express glucocorticoid receptor, therefore we hypothesized that the gonads can detect and respond directly to cues of stress. We provide evidence here that, in addition to regulation by the brain, the gonads of European starlings (Sturnus vulgaris) respond directly to fluctuations in corticosterone and metabolic fuels by modulating sex steroid secretion. Using a 4-h gonad culture, we show that physiologically-relevant concentrations of corticosterone and metabolic stress (via use of the glucose utilization inhibitor 2-deoxy-D-glucose and the fatty acid oxidation inhibitor ethyl 2-mercaptoacetate (2DG/MA)) can directly decrease testosterone and estradiol secretion from luteinizing hormone and follicle-stimulating hormone (LH/FSH)-stimulated testes and ovaries. This effect is regulated seasonally. Prior to the breeding season, testes and ovaries respond to corticosterone and 2DG/MA by significantly decreasing gonadal steroid release. Within the breeding season, the testes do not respond to these cues of stress, while the ovaries respond only to corticosterone. This seasonal difference in response may be due in part to the influence of these cues of stress on gonadal neuropeptide expression: corticosterone upregulates GnIH expression in the testes while metabolic stress upregulates GnIH in the ovaries. Thus the gonads can directly respond to fluctuations in corticosterone and metabolic fuels during a time of critical importance to the onset of breeding. |
first_indexed | 2024-03-09T08:00:44Z |
format | Article |
id | doaj.art-95f622c457474bc0ada6ea571baeb077 |
institution | Directory Open Access Journal |
issn | 2167-8359 |
language | English |
last_indexed | 2024-03-09T08:00:44Z |
publishDate | 2013-08-01 |
publisher | PeerJ Inc. |
record_format | Article |
series | PeerJ |
spelling | doaj.art-95f622c457474bc0ada6ea571baeb0772023-12-03T00:47:38ZengPeerJ Inc.PeerJ2167-83592013-08-011e13910.7717/peerj.139139The direct response of the gonads to cues of stress in a temperate songbird species is season-dependentNicolette L. McGuire0Annie Koh1George E. Bentley2Laboratory of Reproductive Neuroendocrinology, Department of Integrative Biology, University of California at Berkeley, USALaboratory of Reproductive Neuroendocrinology, Department of Integrative Biology, University of California at Berkeley, USALaboratory of Reproductive Neuroendocrinology, Department of Integrative Biology, University of California at Berkeley, USAThe gonadotropin releasing hormone (GnRH) system in the hypothalamus is often considered the final point in integration of environmental cues as they pertain to the reproductive axis. However, cues such as stress and food availability are detectable in the plasma (as glucocorticoid and metabolic fuel fluctuations). Vertebrate gonads express glucocorticoid receptor, therefore we hypothesized that the gonads can detect and respond directly to cues of stress. We provide evidence here that, in addition to regulation by the brain, the gonads of European starlings (Sturnus vulgaris) respond directly to fluctuations in corticosterone and metabolic fuels by modulating sex steroid secretion. Using a 4-h gonad culture, we show that physiologically-relevant concentrations of corticosterone and metabolic stress (via use of the glucose utilization inhibitor 2-deoxy-D-glucose and the fatty acid oxidation inhibitor ethyl 2-mercaptoacetate (2DG/MA)) can directly decrease testosterone and estradiol secretion from luteinizing hormone and follicle-stimulating hormone (LH/FSH)-stimulated testes and ovaries. This effect is regulated seasonally. Prior to the breeding season, testes and ovaries respond to corticosterone and 2DG/MA by significantly decreasing gonadal steroid release. Within the breeding season, the testes do not respond to these cues of stress, while the ovaries respond only to corticosterone. This seasonal difference in response may be due in part to the influence of these cues of stress on gonadal neuropeptide expression: corticosterone upregulates GnIH expression in the testes while metabolic stress upregulates GnIH in the ovaries. Thus the gonads can directly respond to fluctuations in corticosterone and metabolic fuels during a time of critical importance to the onset of breeding.https://peerj.com/articles/139.pdfStressGonadotropin inhibitory hormone (GnIH)CorticosteroneGonadotropin releasing hormone (GnRH)TestesEstradiol |
spellingShingle | Nicolette L. McGuire Annie Koh George E. Bentley The direct response of the gonads to cues of stress in a temperate songbird species is season-dependent PeerJ Stress Gonadotropin inhibitory hormone (GnIH) Corticosterone Gonadotropin releasing hormone (GnRH) Testes Estradiol |
title | The direct response of the gonads to cues of stress in a temperate songbird species is season-dependent |
title_full | The direct response of the gonads to cues of stress in a temperate songbird species is season-dependent |
title_fullStr | The direct response of the gonads to cues of stress in a temperate songbird species is season-dependent |
title_full_unstemmed | The direct response of the gonads to cues of stress in a temperate songbird species is season-dependent |
title_short | The direct response of the gonads to cues of stress in a temperate songbird species is season-dependent |
title_sort | direct response of the gonads to cues of stress in a temperate songbird species is season dependent |
topic | Stress Gonadotropin inhibitory hormone (GnIH) Corticosterone Gonadotropin releasing hormone (GnRH) Testes Estradiol |
url | https://peerj.com/articles/139.pdf |
work_keys_str_mv | AT nicolettelmcguire thedirectresponseofthegonadstocuesofstressinatemperatesongbirdspeciesisseasondependent AT anniekoh thedirectresponseofthegonadstocuesofstressinatemperatesongbirdspeciesisseasondependent AT georgeebentley thedirectresponseofthegonadstocuesofstressinatemperatesongbirdspeciesisseasondependent AT nicolettelmcguire directresponseofthegonadstocuesofstressinatemperatesongbirdspeciesisseasondependent AT anniekoh directresponseofthegonadstocuesofstressinatemperatesongbirdspeciesisseasondependent AT georgeebentley directresponseofthegonadstocuesofstressinatemperatesongbirdspeciesisseasondependent |