Heparan sulfate regulates amphiregulin programming of tissue reparative lung mesenchymal cells during influenza A virus infection in mice

Abstract Amphiregulin (Areg), a growth factor produced by regulatory T (Treg) cells to facilitate tissue repair, contains a heparan sulfate (HS) binding domain. How HS, a highly sulfated glycan subtype that alters growth factor signaling, influences Areg repair functions is unclear. Here we report t...

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Main Authors: Lucas F. Loffredo, Anmol Kustagi, Olivia R. Ringham, Fangda Li, Kenia de los Santos-Alexis, Anjali Saqi, Nicholas Arpaia
Format: Article
Language:English
Published: Nature Portfolio 2025-03-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-025-57362-z
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author Lucas F. Loffredo
Anmol Kustagi
Olivia R. Ringham
Fangda Li
Kenia de los Santos-Alexis
Anjali Saqi
Nicholas Arpaia
author_facet Lucas F. Loffredo
Anmol Kustagi
Olivia R. Ringham
Fangda Li
Kenia de los Santos-Alexis
Anjali Saqi
Nicholas Arpaia
author_sort Lucas F. Loffredo
collection DOAJ
description Abstract Amphiregulin (Areg), a growth factor produced by regulatory T (Treg) cells to facilitate tissue repair, contains a heparan sulfate (HS) binding domain. How HS, a highly sulfated glycan subtype that alters growth factor signaling, influences Areg repair functions is unclear. Here we report that inhibition of HS in various cell lines and primary lung mesenchymal cells (LMC) qualitatively alters Areg downstream signaling. Utilization of a panel of cell lines with targeted deletions in HS synthesis–related genes identifies the glypican family of HS proteoglycans as critical for Areg signaling. In the context of influenza A virus (IAV) infection in vivo, an Areg-responsive subset of reparative LMC upregulate glypican-4 and HS; conditional deletion of HS primarily within this LMC subset results in reduced repair characteristics following IAV infection. This study demonstrates that HS on a specific lung mesenchymal population is a mediator of Treg cell–derived Areg reparative signaling.
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publishDate 2025-03-01
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record_format Article
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spelling doaj-art-e5a09f9b04e34345afa2208728eb9abc2025-08-20T03:05:43ZengNature PortfolioNature Communications2041-17232025-03-0116111610.1038/s41467-025-57362-zHeparan sulfate regulates amphiregulin programming of tissue reparative lung mesenchymal cells during influenza A virus infection in miceLucas F. Loffredo0Anmol Kustagi1Olivia R. Ringham2Fangda Li3Kenia de los Santos-Alexis4Anjali Saqi5Nicholas Arpaia6Department of Microbiology & Immunology, Columbia UniversityDepartment of Microbiology & Immunology, Columbia UniversityDepartment of Microbiology & Immunology, Columbia UniversityDepartment of Microbiology & Immunology, Columbia UniversityDepartment of Microbiology & Immunology, Columbia UniversityDepartment of Pathology and Cell Biology, Columbia University Irving Medical CenterDepartment of Microbiology & Immunology, Columbia UniversityAbstract Amphiregulin (Areg), a growth factor produced by regulatory T (Treg) cells to facilitate tissue repair, contains a heparan sulfate (HS) binding domain. How HS, a highly sulfated glycan subtype that alters growth factor signaling, influences Areg repair functions is unclear. Here we report that inhibition of HS in various cell lines and primary lung mesenchymal cells (LMC) qualitatively alters Areg downstream signaling. Utilization of a panel of cell lines with targeted deletions in HS synthesis–related genes identifies the glypican family of HS proteoglycans as critical for Areg signaling. In the context of influenza A virus (IAV) infection in vivo, an Areg-responsive subset of reparative LMC upregulate glypican-4 and HS; conditional deletion of HS primarily within this LMC subset results in reduced repair characteristics following IAV infection. This study demonstrates that HS on a specific lung mesenchymal population is a mediator of Treg cell–derived Areg reparative signaling.https://doi.org/10.1038/s41467-025-57362-z
spellingShingle Lucas F. Loffredo
Anmol Kustagi
Olivia R. Ringham
Fangda Li
Kenia de los Santos-Alexis
Anjali Saqi
Nicholas Arpaia
Heparan sulfate regulates amphiregulin programming of tissue reparative lung mesenchymal cells during influenza A virus infection in mice
Nature Communications
title Heparan sulfate regulates amphiregulin programming of tissue reparative lung mesenchymal cells during influenza A virus infection in mice
title_full Heparan sulfate regulates amphiregulin programming of tissue reparative lung mesenchymal cells during influenza A virus infection in mice
title_fullStr Heparan sulfate regulates amphiregulin programming of tissue reparative lung mesenchymal cells during influenza A virus infection in mice
title_full_unstemmed Heparan sulfate regulates amphiregulin programming of tissue reparative lung mesenchymal cells during influenza A virus infection in mice
title_short Heparan sulfate regulates amphiregulin programming of tissue reparative lung mesenchymal cells during influenza A virus infection in mice
title_sort heparan sulfate regulates amphiregulin programming of tissue reparative lung mesenchymal cells during influenza a virus infection in mice
url https://doi.org/10.1038/s41467-025-57362-z
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