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Peritoneal tissue-resident macrophages are metabolically poised to engage microbes using tissue-niche fuels

Luke Davies Orcid Logo, Christopher M. Rice, Erika M. Palmieri, Philip R. Taylor Orcid Logo, Douglas B. Kuhns, Daniel W. McVicar

Nature Communications, Volume: 8, Issue: 1

Swansea University Author: Luke Davies Orcid Logo

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DOI (Published version): 10.1038/s41467-017-02092-0

Abstract

The importance of metabolism in macrophage function has been reported, but the in vivo relevance of the in vitro observations is still unclear. Here we show that macrophage metabolites are defined in a specific tissue context, and these metabolites are crucially linked to tissue-resident macrophage...

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Published in: Nature Communications
ISSN: 2041-1723
Published: Springer Science and Business Media LLC 2017
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URI: https://cronfa.swan.ac.uk/Record/cronfa61702
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last_indexed 2023-01-13T19:22:37Z
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spelling 2022-11-07T11:30:04.8406451 v2 61702 2022-10-31 Peritoneal tissue-resident macrophages are metabolically poised to engage microbes using tissue-niche fuels ff080296775381560053d5e3a6e81745 0000-0001-7767-4060 Luke Davies Luke Davies true false 2022-10-31 BMS The importance of metabolism in macrophage function has been reported, but the in vivo relevance of the in vitro observations is still unclear. Here we show that macrophage metabolites are defined in a specific tissue context, and these metabolites are crucially linked to tissue-resident macrophage functions. We find the peritoneum to be rich in glutamate, a glutaminolysis-fuel that is exploited by peritoneal-resident macrophages to maintain respiratory burst during phagocytosis via enhancing mitochondrial complex-II metabolism. This niche-supported, inducible mitochondrial function is dependent on protein kinase C activity, and is required to fine-tune the cytokine responses that control inflammation. In addition, we find that peritoneal-resident macrophage mitochondria are recruited to phagosomes and produce mitochondrially derived reactive oxygen species, which are necessary for microbial killing. We propose that tissue-resident macrophages are metabolically poised in situ to protect and exploit their tissue-niche by utilising locally available fuels to implement specific metabolic programmes upon microbial sensing. Journal Article Nature Communications 8 1 Springer Science and Business Media LLC 2041-1723 12 12 2017 2017-12-12 10.1038/s41467-017-02092-0 COLLEGE NANME Biomedical Sciences COLLEGE CODE BMS Swansea University This work has been funded in part with federal funds from the National Cancer Institute, National Institutes of Health, Intramural Research Program, USA and the Henry Wellcome Trust, UK (WT103973MA). P.R.T. is funded by the Wellcome Trust (107964/Z/15/Z). D.B.K. is under Contract No. HHSN261200800001E. 2022-11-07T11:30:04.8406451 2022-10-31T12:39:26.6851288 Faculty of Medicine, Health and Life Sciences Swansea University Medical School - Medicine Luke Davies 0000-0001-7767-4060 1 Christopher M. Rice 2 Erika M. Palmieri 3 Philip R. Taylor 0000-0003-0163-1421 4 Douglas B. Kuhns 5 Daniel W. McVicar 6 61702__25666__f1910de8be4647bd850c05394f9fb20d.pdf 61702.pdf 2022-11-07T11:28:50.0727279 Output 2207882 application/pdf Version of Record true © The Author(s) 2017. This article is licensed under a Creative Commons Attribution 4.0 International License true eng http://creativecommons.org/licenses/by/4.0/
title Peritoneal tissue-resident macrophages are metabolically poised to engage microbes using tissue-niche fuels
spellingShingle Peritoneal tissue-resident macrophages are metabolically poised to engage microbes using tissue-niche fuels
Luke Davies
title_short Peritoneal tissue-resident macrophages are metabolically poised to engage microbes using tissue-niche fuels
title_full Peritoneal tissue-resident macrophages are metabolically poised to engage microbes using tissue-niche fuels
title_fullStr Peritoneal tissue-resident macrophages are metabolically poised to engage microbes using tissue-niche fuels
title_full_unstemmed Peritoneal tissue-resident macrophages are metabolically poised to engage microbes using tissue-niche fuels
title_sort Peritoneal tissue-resident macrophages are metabolically poised to engage microbes using tissue-niche fuels
author_id_str_mv ff080296775381560053d5e3a6e81745
author_id_fullname_str_mv ff080296775381560053d5e3a6e81745_***_Luke Davies
author Luke Davies
author2 Luke Davies
Christopher M. Rice
Erika M. Palmieri
Philip R. Taylor
Douglas B. Kuhns
Daniel W. McVicar
format Journal article
container_title Nature Communications
container_volume 8
container_issue 1
publishDate 2017
institution Swansea University
issn 2041-1723
doi_str_mv 10.1038/s41467-017-02092-0
publisher Springer Science and Business Media LLC
college_str Faculty of Medicine, Health and Life Sciences
hierarchytype
hierarchy_top_id facultyofmedicinehealthandlifesciences
hierarchy_top_title Faculty of Medicine, Health and Life Sciences
hierarchy_parent_id facultyofmedicinehealthandlifesciences
hierarchy_parent_title Faculty of Medicine, Health and Life Sciences
department_str Swansea University Medical School - Medicine{{{_:::_}}}Faculty of Medicine, Health and Life Sciences{{{_:::_}}}Swansea University Medical School - Medicine
document_store_str 1
active_str 0
description The importance of metabolism in macrophage function has been reported, but the in vivo relevance of the in vitro observations is still unclear. Here we show that macrophage metabolites are defined in a specific tissue context, and these metabolites are crucially linked to tissue-resident macrophage functions. We find the peritoneum to be rich in glutamate, a glutaminolysis-fuel that is exploited by peritoneal-resident macrophages to maintain respiratory burst during phagocytosis via enhancing mitochondrial complex-II metabolism. This niche-supported, inducible mitochondrial function is dependent on protein kinase C activity, and is required to fine-tune the cytokine responses that control inflammation. In addition, we find that peritoneal-resident macrophage mitochondria are recruited to phagosomes and produce mitochondrially derived reactive oxygen species, which are necessary for microbial killing. We propose that tissue-resident macrophages are metabolically poised in situ to protect and exploit their tissue-niche by utilising locally available fuels to implement specific metabolic programmes upon microbial sensing.
published_date 2017-12-12T04:20:43Z
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score 10.999207

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