Cargando…

Polyamine import and accumulation causes immunomodulation in macrophages engulfing apoptotic cells

Phagocytosis of apoptotic cells, termed efferocytosis, is critical for tissue homeostasis and drives anti-inflammatory programming in engulfing macrophages. Here, we assess metabolites in naive and inflammatory macrophages following engulfment of multiple cellular and non-cellular targets. Efferocyt...

Descripción completa

Detalles Bibliográficos
Autores principales: McCubbrey, Alexandra L., McManus, Shannon A., McClendon, Jazalle D., Thomas, Stacey M., Chatwin, Hope B., Reisz, Julie A., D’Alessandro, Angelo, Mould, Kara J., Bratton, Donna L., Henson, Peter M., Janssen, William J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8859864/
https://www.ncbi.nlm.nih.gov/pubmed/35021097
http://dx.doi.org/10.1016/j.celrep.2021.110222
_version_ 1784654547905413120
author McCubbrey, Alexandra L.
McManus, Shannon A.
McClendon, Jazalle D.
Thomas, Stacey M.
Chatwin, Hope B.
Reisz, Julie A.
D’Alessandro, Angelo
Mould, Kara J.
Bratton, Donna L.
Henson, Peter M.
Janssen, William J.
author_facet McCubbrey, Alexandra L.
McManus, Shannon A.
McClendon, Jazalle D.
Thomas, Stacey M.
Chatwin, Hope B.
Reisz, Julie A.
D’Alessandro, Angelo
Mould, Kara J.
Bratton, Donna L.
Henson, Peter M.
Janssen, William J.
author_sort McCubbrey, Alexandra L.
collection PubMed
description Phagocytosis of apoptotic cells, termed efferocytosis, is critical for tissue homeostasis and drives anti-inflammatory programming in engulfing macrophages. Here, we assess metabolites in naive and inflammatory macrophages following engulfment of multiple cellular and non-cellular targets. Efferocytosis leads to increases in the arginine-derived polyamines, spermidine and spermine, in vitro and in vivo. Surprisingly, polyamine accumulation after efferocytosis does not arise from retention of apoptotic cell metabolites or de novo synthesis but from enhanced polyamine import that is dependent on Rac1, actin, and PI3 kinase. Blocking polyamine import prevents efferocytosis from suppressing macrophage interleukin (IL)-1β or IL-6. This identifies efferocytosis as a trigger for polyamine import and accumulation, and imported polyamines as mediators of efferocytosis-induced immune reprogramming.
format Online
Article
Text
id pubmed-8859864
institution National Center for Biotechnology Information
language English
publishDate 2022
record_format MEDLINE/PubMed
spelling pubmed-88598642022-02-21 Polyamine import and accumulation causes immunomodulation in macrophages engulfing apoptotic cells McCubbrey, Alexandra L. McManus, Shannon A. McClendon, Jazalle D. Thomas, Stacey M. Chatwin, Hope B. Reisz, Julie A. D’Alessandro, Angelo Mould, Kara J. Bratton, Donna L. Henson, Peter M. Janssen, William J. Cell Rep Article Phagocytosis of apoptotic cells, termed efferocytosis, is critical for tissue homeostasis and drives anti-inflammatory programming in engulfing macrophages. Here, we assess metabolites in naive and inflammatory macrophages following engulfment of multiple cellular and non-cellular targets. Efferocytosis leads to increases in the arginine-derived polyamines, spermidine and spermine, in vitro and in vivo. Surprisingly, polyamine accumulation after efferocytosis does not arise from retention of apoptotic cell metabolites or de novo synthesis but from enhanced polyamine import that is dependent on Rac1, actin, and PI3 kinase. Blocking polyamine import prevents efferocytosis from suppressing macrophage interleukin (IL)-1β or IL-6. This identifies efferocytosis as a trigger for polyamine import and accumulation, and imported polyamines as mediators of efferocytosis-induced immune reprogramming. 2022-01-11 /pmc/articles/PMC8859864/ /pubmed/35021097 http://dx.doi.org/10.1016/j.celrep.2021.110222 Text en https://creativecommons.org/licenses/by-nc-nd/4.0/This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/ (https://creativecommons.org/licenses/by-nc-nd/4.0/) ).
spellingShingle Article
McCubbrey, Alexandra L.
McManus, Shannon A.
McClendon, Jazalle D.
Thomas, Stacey M.
Chatwin, Hope B.
Reisz, Julie A.
D’Alessandro, Angelo
Mould, Kara J.
Bratton, Donna L.
Henson, Peter M.
Janssen, William J.
Polyamine import and accumulation causes immunomodulation in macrophages engulfing apoptotic cells
title Polyamine import and accumulation causes immunomodulation in macrophages engulfing apoptotic cells
title_full Polyamine import and accumulation causes immunomodulation in macrophages engulfing apoptotic cells
title_fullStr Polyamine import and accumulation causes immunomodulation in macrophages engulfing apoptotic cells
title_full_unstemmed Polyamine import and accumulation causes immunomodulation in macrophages engulfing apoptotic cells
title_short Polyamine import and accumulation causes immunomodulation in macrophages engulfing apoptotic cells
title_sort polyamine import and accumulation causes immunomodulation in macrophages engulfing apoptotic cells
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8859864/
https://www.ncbi.nlm.nih.gov/pubmed/35021097
http://dx.doi.org/10.1016/j.celrep.2021.110222
work_keys_str_mv AT mccubbreyalexandral polyamineimportandaccumulationcausesimmunomodulationinmacrophagesengulfingapoptoticcells
AT mcmanusshannona polyamineimportandaccumulationcausesimmunomodulationinmacrophagesengulfingapoptoticcells
AT mcclendonjazalled polyamineimportandaccumulationcausesimmunomodulationinmacrophagesengulfingapoptoticcells
AT thomasstaceym polyamineimportandaccumulationcausesimmunomodulationinmacrophagesengulfingapoptoticcells
AT chatwinhopeb polyamineimportandaccumulationcausesimmunomodulationinmacrophagesengulfingapoptoticcells
AT reiszjuliea polyamineimportandaccumulationcausesimmunomodulationinmacrophagesengulfingapoptoticcells
AT dalessandroangelo polyamineimportandaccumulationcausesimmunomodulationinmacrophagesengulfingapoptoticcells
AT mouldkaraj polyamineimportandaccumulationcausesimmunomodulationinmacrophagesengulfingapoptoticcells
AT brattondonnal polyamineimportandaccumulationcausesimmunomodulationinmacrophagesengulfingapoptoticcells
AT hensonpeterm polyamineimportandaccumulationcausesimmunomodulationinmacrophagesengulfingapoptoticcells
AT janssenwilliamj polyamineimportandaccumulationcausesimmunomodulationinmacrophagesengulfingapoptoticcells