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Acute restraint stress rapidly impacts reproductive neuroendocrinology and downstream gonad function in big brown bats (Eptesicus fuscus)

Animals face unpredictable challenges that require rapid, facultative physiological reactions to support survival but may compromise reproduction. Bats have a long-standing reputation for being highly sensitive to stressors, with sensitivity and resilience varying both within and among species, yet...

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Autores principales: Alonge, Mattina M., Greville, Lucas J. S., Ma, Xuehao, Faure, Paul A., Bentley, George E.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Company of Biologists Ltd 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10629485/
https://www.ncbi.nlm.nih.gov/pubmed/37827114
http://dx.doi.org/10.1242/jeb.245592
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author Alonge, Mattina M.
Greville, Lucas J. S.
Ma, Xuehao
Faure, Paul A.
Bentley, George E.
author_facet Alonge, Mattina M.
Greville, Lucas J. S.
Ma, Xuehao
Faure, Paul A.
Bentley, George E.
author_sort Alonge, Mattina M.
collection PubMed
description Animals face unpredictable challenges that require rapid, facultative physiological reactions to support survival but may compromise reproduction. Bats have a long-standing reputation for being highly sensitive to stressors, with sensitivity and resilience varying both within and among species, yet little is known about how stress affects the signaling that regulates reproductive physiology. Here, we provide the first description of the molecular response of the hypothalamic–pituitary–gonadal (HPG) axis of male big brown bats (Eptesicus fuscus) in response to short-term stress using a standardized restraint manipulation. This acute stressor was sufficient to upregulate plasma corticosterone and resulted in a rapid decrease in circulating testosterone. While we did not find differences in the mRNA expression of key steroidogenic enzymes (StAR, aromatase, 5-alpha reductase), seminiferous tubule diameter was reduced in stressed bats coupled with a 5-fold increase in glucocorticoid receptor (GR) mRNA expression in the testes. These changes, in part, may be mediated by RFamide-related peptide (RFRP) because fewer immunoreactive cell bodies were detected in the brains of stressed bats compared with controls – suggesting a possible increase in secretion – and increased RFRP expression locally in the gonads. The rapid sensitivity of the bat testes to stress may be connected to deleterious impacts on tissue health and function as supported by significant transcriptional upregulation of key pro-apoptotic signaling molecules (Bax, cytochrome c). Experiments like this broadly contribute to our understanding of the stronger ecological predictions regarding physiological responses of bats within the context of stress, which may impact decisions surrounding animal handling and conservation approaches.
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spelling pubmed-106294852023-11-08 Acute restraint stress rapidly impacts reproductive neuroendocrinology and downstream gonad function in big brown bats (Eptesicus fuscus) Alonge, Mattina M. Greville, Lucas J. S. Ma, Xuehao Faure, Paul A. Bentley, George E. J Exp Biol Research Article Animals face unpredictable challenges that require rapid, facultative physiological reactions to support survival but may compromise reproduction. Bats have a long-standing reputation for being highly sensitive to stressors, with sensitivity and resilience varying both within and among species, yet little is known about how stress affects the signaling that regulates reproductive physiology. Here, we provide the first description of the molecular response of the hypothalamic–pituitary–gonadal (HPG) axis of male big brown bats (Eptesicus fuscus) in response to short-term stress using a standardized restraint manipulation. This acute stressor was sufficient to upregulate plasma corticosterone and resulted in a rapid decrease in circulating testosterone. While we did not find differences in the mRNA expression of key steroidogenic enzymes (StAR, aromatase, 5-alpha reductase), seminiferous tubule diameter was reduced in stressed bats coupled with a 5-fold increase in glucocorticoid receptor (GR) mRNA expression in the testes. These changes, in part, may be mediated by RFamide-related peptide (RFRP) because fewer immunoreactive cell bodies were detected in the brains of stressed bats compared with controls – suggesting a possible increase in secretion – and increased RFRP expression locally in the gonads. The rapid sensitivity of the bat testes to stress may be connected to deleterious impacts on tissue health and function as supported by significant transcriptional upregulation of key pro-apoptotic signaling molecules (Bax, cytochrome c). Experiments like this broadly contribute to our understanding of the stronger ecological predictions regarding physiological responses of bats within the context of stress, which may impact decisions surrounding animal handling and conservation approaches. The Company of Biologists Ltd 2023-10-12 /pmc/articles/PMC10629485/ /pubmed/37827114 http://dx.doi.org/10.1242/jeb.245592 Text en © 2023. Published by The Company of Biologists Ltd https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0 (https://creativecommons.org/licenses/by/4.0/) ), which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
spellingShingle Research Article
Alonge, Mattina M.
Greville, Lucas J. S.
Ma, Xuehao
Faure, Paul A.
Bentley, George E.
Acute restraint stress rapidly impacts reproductive neuroendocrinology and downstream gonad function in big brown bats (Eptesicus fuscus)
title Acute restraint stress rapidly impacts reproductive neuroendocrinology and downstream gonad function in big brown bats (Eptesicus fuscus)
title_full Acute restraint stress rapidly impacts reproductive neuroendocrinology and downstream gonad function in big brown bats (Eptesicus fuscus)
title_fullStr Acute restraint stress rapidly impacts reproductive neuroendocrinology and downstream gonad function in big brown bats (Eptesicus fuscus)
title_full_unstemmed Acute restraint stress rapidly impacts reproductive neuroendocrinology and downstream gonad function in big brown bats (Eptesicus fuscus)
title_short Acute restraint stress rapidly impacts reproductive neuroendocrinology and downstream gonad function in big brown bats (Eptesicus fuscus)
title_sort acute restraint stress rapidly impacts reproductive neuroendocrinology and downstream gonad function in big brown bats (eptesicus fuscus)
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10629485/
https://www.ncbi.nlm.nih.gov/pubmed/37827114
http://dx.doi.org/10.1242/jeb.245592
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