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

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dc.contributor.authorvan de Wouw, Marcel
dc.contributor.authorLyte, Joshua M.
dc.contributor.authorBoehme, Marcus
dc.contributor.authorSichetti, Marzia
dc.contributor.authorMoloney, Gerard M.
dc.contributor.authorGoodson, Michael S.
dc.contributor.authorKelley-Loughnane, Nancy
dc.contributor.authorDinan, Timothy G.
dc.contributor.authorClarke, Gerard
dc.contributor.authorCryan, John F.
dc.contributor.funderScience Foundation Irelanden
dc.contributor.funderInternational Science and Technology Centeren
dc.contributor.funderEuropean Office of Aerospace Research and Developmenten
dc.contributor.funderAir Force Office of Scientific Researchen
dc.contributor.funderAir Force Research Laboratoryen
dc.contributor.funder711th Human Performance Wingen
dc.date.accessioned2020-01-10T15:44:37Z
dc.date.available2020-01-10T15:44:37Z
dc.date.issued2019-12-05
dc.date.updated2020-01-10T15:13:46Z
dc.description.abstractThere 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.sponsorshipEuropean 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.description.statusPeer revieweden
dc.description.versionAccepted Versionen
dc.format.mimetypeapplication/pdfen
dc.identifier.citationvan 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.2019.12.003en
dc.identifier.doi10.1016/j.bbi.2019.12.003en
dc.identifier.endpage9en
dc.identifier.issn0889-1591
dc.identifier.journaltitleBrain, Behavior, and Immunityen
dc.identifier.startpage1en
dc.identifier.urihttps://hdl.handle.net/10468/9488
dc.language.isoenen
dc.publisherElsevieren
dc.relation.projectinfo:eu-repo/grantAgreement/SFI/SFI Research Centres/12/RC/2273/IE/Alimentary Pharmabiotic Centre (APC) - Interfacing Food & Medicine/en
dc.relation.projectinfo:eu-repo/grantAgreement/RCUK/MRC/MR/N029488/1/GB/AMBROSIAC - A Menu for Brain Responses Opposing Stress-Induced Alterations in Cognition/en
dc.relation.urihttp://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.urihttps://creativecommons.org/licenses/by-nc-nd/4.0/en
dc.subjectMetagenomeen
dc.subjectObesityen
dc.subjectMicrobial compositionen
dc.subjectMicrobiotaen
dc.subjectStress-related disordersen
dc.titleThe role of the microbiota in acute stress-induced myeloid immune cell traffickingen
dc.typeArticle (peer-reviewed)en
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