Staphylococcus epidermidis alters macrophage polarization and phagocytic uptake by extracellular DNA release in vitro

Abstract Biofilm formation shields Staphylococcus epidermidis from host defense mechanisms, contributing to chronic implant infections. Using wild-type S. epidermidis 1457, a PIA-negative mutant (1457-M10), and an eDNA-negative mutant (1457ΔatlE), this study examined the influence of biofilm matrix...

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Main Authors: Samira Weißelberg, Anna Both, Antonio Virgilio Failla, Jiabin Huang, Stefan Linder, Denise Ohnezeit, Patricia Bartsch, Martin Aepfelbacher, Holger Rohde
Format: Article
Language:English
Published: Nature Portfolio 2024-11-01
Series:npj Biofilms and Microbiomes
Online Access:https://doi.org/10.1038/s41522-024-00604-7
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author Samira Weißelberg
Anna Both
Antonio Virgilio Failla
Jiabin Huang
Stefan Linder
Denise Ohnezeit
Patricia Bartsch
Martin Aepfelbacher
Holger Rohde
author_facet Samira Weißelberg
Anna Both
Antonio Virgilio Failla
Jiabin Huang
Stefan Linder
Denise Ohnezeit
Patricia Bartsch
Martin Aepfelbacher
Holger Rohde
author_sort Samira Weißelberg
collection DOAJ
description Abstract Biofilm formation shields Staphylococcus epidermidis from host defense mechanisms, contributing to chronic implant infections. Using wild-type S. epidermidis 1457, a PIA-negative mutant (1457-M10), and an eDNA-negative mutant (1457ΔatlE), this study examined the influence of biofilm matrix components on human monocyte-derived macrophage (hMDM) interactions. The wild-type strain was resistant to phagocytosis and induced an anti-inflammatory response in hMDMs, while both mutants were more susceptible to phagocytosis and triggered a pro-inflammatory response. Removing eDNA from the 1457 biofilm matrix increased hMDM uptake and a pro-inflammatory reaction, whereas adding eDNA to the 1457ΔatlE mutant reduced phagocytosis and promoted an anti-inflammatory response. Inhibiting TLR9 enhanced bacterial uptake and induced a pro-inflammatory response in hMDMs exposed to wild-type S. epidermidis. This study highlights the critical role of eDNA in immune evasion and the central role of TLR9 in modulating macrophage responses, advancing the understanding of implant infections.
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spelling doaj-art-a980c3bd6ec94de8bd644b1975e3519f2025-08-20T02:32:56ZengNature Portfolionpj Biofilms and Microbiomes2055-50082024-11-0110111510.1038/s41522-024-00604-7Staphylococcus epidermidis alters macrophage polarization and phagocytic uptake by extracellular DNA release in vitroSamira Weißelberg0Anna Both1Antonio Virgilio Failla2Jiabin Huang3Stefan Linder4Denise Ohnezeit5Patricia Bartsch6Martin Aepfelbacher7Holger Rohde8Institut für Medizinische Mikrobiologie, Virologie und Hygiene, Universitätsklinikum Hamburg-Eppendorf (UKE)Institut für Medizinische Mikrobiologie, Virologie und Hygiene, Universitätsklinikum Hamburg-Eppendorf (UKE)UKE Microscopy Imaging Facility (Umif), Universitätsklinikum Hamburg-Eppendorf (UKE)Institut für Medizinische Mikrobiologie, Virologie und Hygiene, Universitätsklinikum Hamburg-Eppendorf (UKE)Institut für Medizinische Mikrobiologie, Virologie und Hygiene, Universitätsklinikum Hamburg-Eppendorf (UKE)Institut für Medizinische Mikrobiologie, Virologie und Hygiene, Universitätsklinikum Hamburg-Eppendorf (UKE)Institut für Medizinische Mikrobiologie, Virologie und Hygiene, Universitätsklinikum Hamburg-Eppendorf (UKE)Institut für Medizinische Mikrobiologie, Virologie und Hygiene, Universitätsklinikum Hamburg-Eppendorf (UKE)Institut für Medizinische Mikrobiologie, Virologie und Hygiene, Universitätsklinikum Hamburg-Eppendorf (UKE)Abstract Biofilm formation shields Staphylococcus epidermidis from host defense mechanisms, contributing to chronic implant infections. Using wild-type S. epidermidis 1457, a PIA-negative mutant (1457-M10), and an eDNA-negative mutant (1457ΔatlE), this study examined the influence of biofilm matrix components on human monocyte-derived macrophage (hMDM) interactions. The wild-type strain was resistant to phagocytosis and induced an anti-inflammatory response in hMDMs, while both mutants were more susceptible to phagocytosis and triggered a pro-inflammatory response. Removing eDNA from the 1457 biofilm matrix increased hMDM uptake and a pro-inflammatory reaction, whereas adding eDNA to the 1457ΔatlE mutant reduced phagocytosis and promoted an anti-inflammatory response. Inhibiting TLR9 enhanced bacterial uptake and induced a pro-inflammatory response in hMDMs exposed to wild-type S. epidermidis. This study highlights the critical role of eDNA in immune evasion and the central role of TLR9 in modulating macrophage responses, advancing the understanding of implant infections.https://doi.org/10.1038/s41522-024-00604-7
spellingShingle Samira Weißelberg
Anna Both
Antonio Virgilio Failla
Jiabin Huang
Stefan Linder
Denise Ohnezeit
Patricia Bartsch
Martin Aepfelbacher
Holger Rohde
Staphylococcus epidermidis alters macrophage polarization and phagocytic uptake by extracellular DNA release in vitro
npj Biofilms and Microbiomes
title Staphylococcus epidermidis alters macrophage polarization and phagocytic uptake by extracellular DNA release in vitro
title_full Staphylococcus epidermidis alters macrophage polarization and phagocytic uptake by extracellular DNA release in vitro
title_fullStr Staphylococcus epidermidis alters macrophage polarization and phagocytic uptake by extracellular DNA release in vitro
title_full_unstemmed Staphylococcus epidermidis alters macrophage polarization and phagocytic uptake by extracellular DNA release in vitro
title_short Staphylococcus epidermidis alters macrophage polarization and phagocytic uptake by extracellular DNA release in vitro
title_sort staphylococcus epidermidis alters macrophage polarization and phagocytic uptake by extracellular dna release in vitro
url https://doi.org/10.1038/s41522-024-00604-7
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