Temporal dynamics of pro-inflammatory cytokines and serum corticosterone following acute sleep fragmentation in male mice.

Obstructive sleep apnea is increasing worldwide, leading to disordered sleep patterns and inflammatory responses in brain and peripheral tissues that predispose individuals to chronic disease. Pro-inflammatory cytokines activate the inflammatory response and are normally regulated by glucocorticoids...

Full description

Bibliographic Details
Main Authors: Van Thuan Nguyen, Cameron J Fields, Noah T Ashley
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2023-01-01
Series:PLoS ONE
Online Access:https://doi.org/10.1371/journal.pone.0288889
_version_ 1797326241744814080
author Van Thuan Nguyen
Cameron J Fields
Noah T Ashley
author_facet Van Thuan Nguyen
Cameron J Fields
Noah T Ashley
author_sort Van Thuan Nguyen
collection DOAJ
description Obstructive sleep apnea is increasing worldwide, leading to disordered sleep patterns and inflammatory responses in brain and peripheral tissues that predispose individuals to chronic disease. Pro-inflammatory cytokines activate the inflammatory response and are normally regulated by glucocorticoids secreted from adrenal glands. However, the temporal dynamics of inflammatory responses and hypothalamic-pituitary-adrenal (HPA) axis activation in relation to acute sleep fragmentation (ASF) are undescribed. Male C57BL/6J mice were exposed to ASF or control conditions (no ASF) over specified intervals (1, 2, 6, or 24 h) and cytokine gene expression (IL-1β, TNF-α) in brain and peripheral tissues as well as serum glucocorticoid and interleukin-6 (IL-6) concentration were assessed. The HPA axis was rapidly activated, leading to elevated serum corticosterone from 1-24 h of ASF compared with controls. This activation was followed by elevated serum IL-6 concentration from 6-24 h of ASF. The tissue to first exhibit increased pro-inflammatory gene expression from ASF was heart (1 h of ASF). In contrast, pro-inflammatory gene expression was suppressed in hypothalamus from 1 h of ASF, but elevated at 6 h. Because the HPA axis was activated throughout ASF, this suggests that brain, but not peripheral, pro-inflammatory responses were rapidly inhibited by glucocorticoid immunosuppression.
first_indexed 2024-03-08T06:20:35Z
format Article
id doaj.art-9af2c1e071664dd3856702511a9a2e90
institution Directory Open Access Journal
issn 1932-6203
language English
last_indexed 2024-03-08T06:20:35Z
publishDate 2023-01-01
publisher Public Library of Science (PLoS)
record_format Article
series PLoS ONE
spelling doaj.art-9af2c1e071664dd3856702511a9a2e902024-02-04T05:31:25ZengPublic Library of Science (PLoS)PLoS ONE1932-62032023-01-011812e028888910.1371/journal.pone.0288889Temporal dynamics of pro-inflammatory cytokines and serum corticosterone following acute sleep fragmentation in male mice.Van Thuan NguyenCameron J FieldsNoah T AshleyObstructive sleep apnea is increasing worldwide, leading to disordered sleep patterns and inflammatory responses in brain and peripheral tissues that predispose individuals to chronic disease. Pro-inflammatory cytokines activate the inflammatory response and are normally regulated by glucocorticoids secreted from adrenal glands. However, the temporal dynamics of inflammatory responses and hypothalamic-pituitary-adrenal (HPA) axis activation in relation to acute sleep fragmentation (ASF) are undescribed. Male C57BL/6J mice were exposed to ASF or control conditions (no ASF) over specified intervals (1, 2, 6, or 24 h) and cytokine gene expression (IL-1β, TNF-α) in brain and peripheral tissues as well as serum glucocorticoid and interleukin-6 (IL-6) concentration were assessed. The HPA axis was rapidly activated, leading to elevated serum corticosterone from 1-24 h of ASF compared with controls. This activation was followed by elevated serum IL-6 concentration from 6-24 h of ASF. The tissue to first exhibit increased pro-inflammatory gene expression from ASF was heart (1 h of ASF). In contrast, pro-inflammatory gene expression was suppressed in hypothalamus from 1 h of ASF, but elevated at 6 h. Because the HPA axis was activated throughout ASF, this suggests that brain, but not peripheral, pro-inflammatory responses were rapidly inhibited by glucocorticoid immunosuppression.https://doi.org/10.1371/journal.pone.0288889
spellingShingle Van Thuan Nguyen
Cameron J Fields
Noah T Ashley
Temporal dynamics of pro-inflammatory cytokines and serum corticosterone following acute sleep fragmentation in male mice.
PLoS ONE
title Temporal dynamics of pro-inflammatory cytokines and serum corticosterone following acute sleep fragmentation in male mice.
title_full Temporal dynamics of pro-inflammatory cytokines and serum corticosterone following acute sleep fragmentation in male mice.
title_fullStr Temporal dynamics of pro-inflammatory cytokines and serum corticosterone following acute sleep fragmentation in male mice.
title_full_unstemmed Temporal dynamics of pro-inflammatory cytokines and serum corticosterone following acute sleep fragmentation in male mice.
title_short Temporal dynamics of pro-inflammatory cytokines and serum corticosterone following acute sleep fragmentation in male mice.
title_sort temporal dynamics of pro inflammatory cytokines and serum corticosterone following acute sleep fragmentation in male mice
url https://doi.org/10.1371/journal.pone.0288889
work_keys_str_mv AT vanthuannguyen temporaldynamicsofproinflammatorycytokinesandserumcorticosteronefollowingacutesleepfragmentationinmalemice
AT cameronjfields temporaldynamicsofproinflammatorycytokinesandserumcorticosteronefollowingacutesleepfragmentationinmalemice
AT noahtashley temporaldynamicsofproinflammatorycytokinesandserumcorticosteronefollowingacutesleepfragmentationinmalemice