The role of the microbiota in acute stress-induced myeloid immune cell trafficking

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dc.contributor.author van de Wouw, Marcel
dc.contributor.author Lyte, Joshua M.
dc.contributor.author Boehme, Marcus
dc.contributor.author Sichetti, Marzia
dc.contributor.author Moloney, Gerard
dc.contributor.author Goodson, Michael S.
dc.contributor.author Kelley-Loughnane, Nancy
dc.contributor.author Dinan, Timothy G.
dc.contributor.author Clarke, Gerard
dc.contributor.author Cryan, John F.
dc.date.accessioned 2020-01-10T15:44:37Z
dc.date.available 2020-01-10T15:44:37Z
dc.date.issued 2019-12-05
dc.identifier.citation van de Wouw, M., Lyte, J. M., Boehme, M., Sichetti, M., Moloney, G., Goodson, M. S., Kelley-Loughnane, N., Dinan, T. G., Clarke, G. and Cryan, J. F. (2019) 'The role of the microbiota in acute stress-induced myeloid immune cell trafficking', Brain, Behavior, and Immunity, doi: 10.1016/j.bbi.2019.12.003 en
dc.identifier.startpage 1 en
dc.identifier.endpage 9 en
dc.identifier.issn 0889-1591
dc.identifier.uri http://hdl.handle.net/10468/9488
dc.identifier.doi 10.1016/j.bbi.2019.12.003 en
dc.description.abstract There has been a growing recognition of the involvement of the gastrointestinal microbiota in the development of stress-related disorders. Acute stress leads to activation of neuroendocrine systems, which in turn orchestrate a large-scale redistribution of innate immune cells. Both these response systems are independently known to be primed by the microbiota, even though much is still unclear about the role of the gastrointestinal microbiota in acute stress-induced immune activation. In this study, we investigated whether the microbiota influences acute stress-induced changes in innate immunity using conventionally colonised mice, mice devoid of any microbiota (i.e. germ-free, GF), and colonised GF mice (CGF). We also explored the kinetics of stress-induced immune cell mobilisation in the blood, the spleen and mesenteric lymph nodes (MLNs). Mice were either euthanised prior to stress or underwent restraint stress and were then euthanised at various time points (i.e. 0, 45- and 240-minutes) post-stress. Plasma adrenaline and noradrenaline levels were analysed using ELISA and immune cell levels were quantified using flow cytometry. GF mice had increased baseline levels of adrenaline and noradrenaline, of which adrenaline was normalised in CGF mice. In tandem, GF mice had decreased circulating levels of LY6Chi and LY6Cmid, CCR2+ monocytes, and granulocytes, but not LY6C−, CX3CR1+ monocytes. These deficits were normalised in CGF mice. Acute stress decreased blood LY6Chi and LY6Cmid, CCR2+ monocytes while increasing granulocyte levels in all groups 45 min post-stress. However, only GF mice showed stress-induced changes in LY6Chi monocytes and granulocytes 240 min post-stress, indicating impairments in the recovery from acute stress-induced changes in levels of specific innate immune cell types. LY6C−, CX3CR1+ monocytes remained unaffected by stress, indicating that acute stress impacts systemic innate immunity in a cell-type-specific manner. Overall, these data reveal novel cell-type-specific changes in the innate immune system in response to acute stress, which in turn are impacted by the microbiota. In conclusion, the microbiota influences the priming and recovery of the innate immune system to an acute stressor and may inform future microbiota-targeted therapeutics aimed at modulating stress-induced immune activation in stress-related disorders. en
dc.description.sponsorship European Office of Aerospace Research and Development, Air Force Office of Scientific Research and 711Human Performance Wing, Air Force Research Laboratory (collaborative agreement (FA9550-17-1-0016), (Air Force approval number: AFOSR-2016-0018A)); Science Foundation Ireland (Joint Programming Initiative- a healthy diet for a healthy life(JPI-HDHL)-investigating Nutrition and Cognitive Function (NutriCog)by SFI Grant“A Menu for Brain Responses Opposing Stress-InducedAlternations in Cognition”(AMBROSIAC) 15/JPHDHL/3270) en
dc.format.mimetype application/pdf en
dc.language.iso en en
dc.publisher Elsevier en
dc.relation.uri http://www.sciencedirect.com/science/article/pii/S0889159119311869
dc.rights © 2019 Elsevier Ltd. All rights reserved. This manuscript version is made available under the CC BY-NC-ND 4.0 licence. en
dc.rights.uri https://creativecommons.org/licenses/by-nc-nd/4.0/ en
dc.subject Metagenome en
dc.subject Obesity en
dc.subject Microbial composition en
dc.subject Microbiota en
dc.subject Stress-related disorders en
dc.title The role of the microbiota in acute stress-induced myeloid immune cell trafficking en
dc.type Article (peer-reviewed) en
dc.internal.authorcontactother John F Cryan, Department Of Anatomy & Neuroscience, University College Cork, Cork, Ireland. +353-21-490-3000 Email: j.cryan@ucc.ie en
dc.internal.availability Full text available en
dc.check.info Access to this article is restricted until 12 months after publication by request of the publisher en
dc.check.date 2020-12-05
dc.date.updated 2020-01-10T15:13:46Z
dc.description.version Accepted Version en
dc.internal.rssid 500173550
dc.contributor.funder Science Foundation Ireland en
dc.contributor.funder International Science and Technology Center en
dc.contributor.funder European Office of Aerospace Research and Development en
dc.contributor.funder Air Force Office of Scientific Research en
dc.contributor.funder Air Force Research Laboratory en
dc.contributor.funder 711th Human Performance Wing en
dc.description.status Peer reviewed en
dc.identifier.journaltitle Brain, Behavior, and Immunity en
dc.internal.copyrightchecked Yes
dc.internal.licenseacceptance Yes en
dc.internal.IRISemailaddress j.cryan@ucc.ie en
dc.internal.IRISemailaddress g.clarke@ucc.ie en
dc.internal.IRISemailaddress marcus.boehme@ucc.ie en
dc.internal.IRISemailaddress g.moloney@ucc.ie en
dc.internal.IRISemailaddress t.dinan@ucc.ie en
dc.internal.IRISemailaddress marcel.vandewouw@ucc.ie en
dc.internal.bibliocheck In press. Check vol / issue / page range. Amend citation as necessary. en
dc.relation.project info:eu-repo/grantAgreement/SFI/SFI Research Centres/12/RC/2273/IE/Alimentary Pharmabiotic Centre (APC) - Interfacing Food & Medicine/ en
dc.relation.project info:eu-repo/grantAgreement/RCUK/MRC/MR/N029488/1/GB/AMBROSIAC - A Menu for Brain Responses Opposing Stress-Induced Alterations in Cognition/ en


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© 2019 Elsevier Ltd. All rights reserved. This manuscript version is made available under the CC BY-NC-ND 4.0 licence. Except where otherwise noted, this item's license is described as © 2019 Elsevier Ltd. All rights reserved. This manuscript version is made available under the CC BY-NC-ND 4.0 licence.
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