Immunometabolic adaptation in monocytes underpins functional changes during pregnancy

Rees, April; Jenkins, Benjamin; Angelini, Roberto; Davies, Luke; Cronin, James; Jones, Nick; Thornton, Cathy

doi:10.1016/j.isci.2024.109779

Journal article 343 views 55 downloads

Immunometabolic adaptation in monocytes underpins functional changes during pregnancy

April Rees

, Benjamin Jenkins, Roberto Angelini

, Luke Davies

, James Cronin

, Nick Jones

, Cathy Thornton

iScience, Volume: 27, Issue: 5, Start page: 109779

Swansea University Authors: April Rees , Benjamin Jenkins, Roberto Angelini , Luke Davies , James Cronin , Nick Jones , Cathy Thornton

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DOI (Published version): 10.1016/j.isci.2024.109779

Abstract

Metabolic heterogeneity is a determinant of immune cell function. The normal physiological metabolic reprogramming of pregnancy that ensures the fuel requirements of mother and baby are met, might also underpin changes in immunity that occur with pregnancy and manifest as altered responses to pathog...

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Published in:	iScience
ISSN:	2589-0042
Published:	Elsevier BV 2024
Online Access:	Check full text
URI:	https://cronfa.swan.ac.uk/Record/cronfa66076

first_indexed	2024-04-18T14:25:07Z
last_indexed	2024-11-25T14:17:27Z
id	cronfa66076
recordtype	SURis
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The normal physiological metabolic reprogramming of pregnancy that ensures the fuel requirements of mother and baby are met, might also underpin changes in immunity that occur with pregnancy and manifest as altered responses to pathogens and changes to autoimmune disease symptoms. Using peripheral blood from pregnant women at term, we reveal that monocytes lose M2-like and gain M1-like properties accompanied by reductions in mitochondrial mass, maximal respiration and cardiolipin content in pregnancy; glycolysis is unperturbed. We establish that muramyl dipeptide (MDP)-stimulated cytokine production relies on oxidative metabolism, then show in pregnancy reduced cytokine production in response to MDP but not LPS. 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spelling	2024-05-23T12:09:52.3591118 v2 66076 2024-04-17 Immunometabolic adaptation in monocytes underpins functional changes during pregnancy ae088f7f8609d2b2ea4666f9b52b3c15 0000-0002-4408-634X April Rees April Rees true false 90f7cfd66781feba615436189178a528 Benjamin Jenkins Benjamin Jenkins true false 6405b7880498750d41c93c6ff89cff96 0000-0001-5136-5921 Roberto Angelini Roberto Angelini true false ff080296775381560053d5e3a6e81745 0000-0001-7767-4060 Luke Davies Luke Davies true false 9cfd17551c0d1f7438895121e4fbb6e8 0000-0002-0590-9462 James Cronin James Cronin true false 0fce0f7ddbdbfeb968f4e2f1e3f86744 0000-0003-4846-5117 Nick Jones Nick Jones true false c71a7a4be7361094d046d312202bce0c 0000-0002-5153-573X Cathy Thornton Cathy Thornton true false 2024-04-17 MEDS Metabolic heterogeneity is a determinant of immune cell function. The normal physiological metabolic reprogramming of pregnancy that ensures the fuel requirements of mother and baby are met, might also underpin changes in immunity that occur with pregnancy and manifest as altered responses to pathogens and changes to autoimmune disease symptoms. Using peripheral blood from pregnant women at term, we reveal that monocytes lose M2-like and gain M1-like properties accompanied by reductions in mitochondrial mass, maximal respiration and cardiolipin content in pregnancy; glycolysis is unperturbed. We establish that muramyl dipeptide (MDP)-stimulated cytokine production relies on oxidative metabolism, then show in pregnancy reduced cytokine production in response to MDP but not LPS. Overall, mitochondrially centred metabolic capabilities of late gestation monocytes are downregulated revealing natural plasticity in monocyte phenotype and function that could reveal targets for improving pregnancy outcomes but also yield alternative therapeutic approaches to diverse metabolic and/or immune-mediated diseases beyond pregnancy. Journal Article iScience 27 5 109779 Elsevier BV 2589-0042 Reproductive medicine; Physiology; Immunology; cell biology 17 5 2024 2024-05-17 10.1016/j.isci.2024.109779 COLLEGE NANME Medical School COLLEGE CODE MEDS Swansea University SU College/Department paid the OA fee Research Wales Innovation Fund (RWIF) of the Higher Education Funding Council Wales (HEFCW) EE6 2024-05-23T12:09:52.3591118 2024-04-17T18:49:34.3203418 Faculty of Medicine, Health and Life Sciences Swansea University Medical School - Biomedical Science April Rees 0000-0002-4408-634X 1 Benjamin Jenkins 2 Roberto Angelini 0000-0001-5136-5921 3 Luke Davies 0000-0001-7767-4060 4 James Cronin 0000-0002-0590-9462 5 Nick Jones 0000-0003-4846-5117 6 Cathy Thornton 0000-0002-5153-573X 7 66076__30426__c45620ad79de4064ba11ed4be0959a68.pdf 66076.VoR.pdf 2024-05-21T14:56:56.8356731 Output 4036814 application/pdf Version of Record true Copyright: 2024 The Author(s). This is an open access article under the CC BY license. true eng http://creativecommons.org/licenses/by/4.0/
title	Immunometabolic adaptation in monocytes underpins functional changes during pregnancy
spellingShingle	Immunometabolic adaptation in monocytes underpins functional changes during pregnancy April Rees Benjamin Jenkins Roberto Angelini Luke Davies James Cronin Nick Jones Cathy Thornton
title_short	Immunometabolic adaptation in monocytes underpins functional changes during pregnancy
title_full	Immunometabolic adaptation in monocytes underpins functional changes during pregnancy
title_fullStr	Immunometabolic adaptation in monocytes underpins functional changes during pregnancy
title_full_unstemmed	Immunometabolic adaptation in monocytes underpins functional changes during pregnancy
title_sort	Immunometabolic adaptation in monocytes underpins functional changes during pregnancy
author_id_str_mv	ae088f7f8609d2b2ea4666f9b52b3c15 90f7cfd66781feba615436189178a528 6405b7880498750d41c93c6ff89cff96 ff080296775381560053d5e3a6e81745 9cfd17551c0d1f7438895121e4fbb6e8 0fce0f7ddbdbfeb968f4e2f1e3f86744 c71a7a4be7361094d046d312202bce0c
author_id_fullname_str_mv	ae088f7f8609d2b2ea4666f9b52b3c15_*_April Rees 90f7cfd66781feba615436189178a528__Benjamin Jenkins 6405b7880498750d41c93c6ff89cff96__Roberto Angelini ff080296775381560053d5e3a6e81745__Luke Davies 9cfd17551c0d1f7438895121e4fbb6e8__James Cronin 0fce0f7ddbdbfeb968f4e2f1e3f86744__Nick Jones c71a7a4be7361094d046d312202bce0c_**_Cathy Thornton
author	April Rees Benjamin Jenkins Roberto Angelini Luke Davies James Cronin Nick Jones Cathy Thornton
author2	April Rees Benjamin Jenkins Roberto Angelini Luke Davies James Cronin Nick Jones Cathy Thornton
format	Journal article
container_title	iScience
container_volume	27
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publishDate	2024
institution	Swansea University
issn	2589-0042
doi_str_mv	10.1016/j.isci.2024.109779
publisher	Elsevier BV
college_str	Faculty of Medicine, Health and Life Sciences
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hierarchy_top_title	Faculty of Medicine, Health and Life Sciences
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hierarchy_parent_title	Faculty of Medicine, Health and Life Sciences
department_str	Swansea University Medical School - Biomedical Science{{{_:::_}}}Faculty of Medicine, Health and Life Sciences{{{_:::_}}}Swansea University Medical School - Biomedical Science
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description	Metabolic heterogeneity is a determinant of immune cell function. The normal physiological metabolic reprogramming of pregnancy that ensures the fuel requirements of mother and baby are met, might also underpin changes in immunity that occur with pregnancy and manifest as altered responses to pathogens and changes to autoimmune disease symptoms. Using peripheral blood from pregnant women at term, we reveal that monocytes lose M2-like and gain M1-like properties accompanied by reductions in mitochondrial mass, maximal respiration and cardiolipin content in pregnancy; glycolysis is unperturbed. We establish that muramyl dipeptide (MDP)-stimulated cytokine production relies on oxidative metabolism, then show in pregnancy reduced cytokine production in response to MDP but not LPS. Overall, mitochondrially centred metabolic capabilities of late gestation monocytes are downregulated revealing natural plasticity in monocyte phenotype and function that could reveal targets for improving pregnancy outcomes but also yield alternative therapeutic approaches to diverse metabolic and/or immune-mediated diseases beyond pregnancy.
published_date	2024-05-17T08:23:51Z
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Immunometabolic adaptation in monocytes underpins functional changes during pregnancy

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