Ferroptosis spreads to neighboring cells via plasma membrane contacts

Abstract Ferroptosis is a lytic, iron-dependent form of regulated cell death characterized by excessive lipid peroxidation and associated with necrosis spread in diseased tissues through unknown mechanisms. Using a novel optogenetic system for light-driven ferroptosis induction via degradation of th...

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Main Authors: Bernhard F. Roeck, Sara Lotfipour Nasudivar, Michael R. H. Vorndran, Lena Schueller, F. Isil Yapici, Matthias Rübsam, Silvia von Karstedt, Carien M. Niessen, Ana J. Garcia-Saez
Format: Article
Language:English
Published: Nature Portfolio 2025-03-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-025-58175-w
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author Bernhard F. Roeck
Sara Lotfipour Nasudivar
Michael R. H. Vorndran
Lena Schueller
F. Isil Yapici
Matthias Rübsam
Silvia von Karstedt
Carien M. Niessen
Ana J. Garcia-Saez
author_facet Bernhard F. Roeck
Sara Lotfipour Nasudivar
Michael R. H. Vorndran
Lena Schueller
F. Isil Yapici
Matthias Rübsam
Silvia von Karstedt
Carien M. Niessen
Ana J. Garcia-Saez
author_sort Bernhard F. Roeck
collection DOAJ
description Abstract Ferroptosis is a lytic, iron-dependent form of regulated cell death characterized by excessive lipid peroxidation and associated with necrosis spread in diseased tissues through unknown mechanisms. Using a novel optogenetic system for light-driven ferroptosis induction via degradation of the anti-ferroptotic protein GPX4, we show that lipid peroxidation and ferroptotic death can spread to neighboring cells through their closely adjacent plasma membranes. Ferroptosis propagation is dependent on cell distance and completely abolished by disruption of α-catenin-dependent intercellular contacts or by chelation of extracellular iron. Remarkably, bridging cells with a lipid bilayer or increasing contacts between neighboring cells enhances ferroptosis spread. Reconstitution of iron-dependent spread of lipid peroxidation between pure lipid, contacting liposomes provides evidence for the physicochemical mechanism involved. Our findings support a model in which iron-dependent lipid peroxidation propagates across proximal plasma membranes of neighboring cells, thereby promoting the transmission of ferroptotic cell death with consequences for pathological tissue necrosis spread.
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spelling doaj-art-192407955e544abcbc15bef4eca2e0b62025-08-20T02:10:10ZengNature PortfolioNature Communications2041-17232025-03-0116111810.1038/s41467-025-58175-wFerroptosis spreads to neighboring cells via plasma membrane contactsBernhard F. Roeck0Sara Lotfipour Nasudivar1Michael R. H. Vorndran2Lena Schueller3F. Isil Yapici4Matthias Rübsam5Silvia von Karstedt6Carien M. Niessen7Ana J. Garcia-Saez8Institute for Genetics, University of CologneInstitute for Genetics, University of CologneInstitute for Genetics, University of CologneInstitute for Genetics, University of CologneCECAD Cluster of Excellence, University of CologneCECAD Cluster of Excellence, University of CologneCECAD Cluster of Excellence, University of CologneCECAD Cluster of Excellence, University of CologneInstitute for Genetics, University of CologneAbstract Ferroptosis is a lytic, iron-dependent form of regulated cell death characterized by excessive lipid peroxidation and associated with necrosis spread in diseased tissues through unknown mechanisms. Using a novel optogenetic system for light-driven ferroptosis induction via degradation of the anti-ferroptotic protein GPX4, we show that lipid peroxidation and ferroptotic death can spread to neighboring cells through their closely adjacent plasma membranes. Ferroptosis propagation is dependent on cell distance and completely abolished by disruption of α-catenin-dependent intercellular contacts or by chelation of extracellular iron. Remarkably, bridging cells with a lipid bilayer or increasing contacts between neighboring cells enhances ferroptosis spread. Reconstitution of iron-dependent spread of lipid peroxidation between pure lipid, contacting liposomes provides evidence for the physicochemical mechanism involved. Our findings support a model in which iron-dependent lipid peroxidation propagates across proximal plasma membranes of neighboring cells, thereby promoting the transmission of ferroptotic cell death with consequences for pathological tissue necrosis spread.https://doi.org/10.1038/s41467-025-58175-w
spellingShingle Bernhard F. Roeck
Sara Lotfipour Nasudivar
Michael R. H. Vorndran
Lena Schueller
F. Isil Yapici
Matthias Rübsam
Silvia von Karstedt
Carien M. Niessen
Ana J. Garcia-Saez
Ferroptosis spreads to neighboring cells via plasma membrane contacts
Nature Communications
title Ferroptosis spreads to neighboring cells via plasma membrane contacts
title_full Ferroptosis spreads to neighboring cells via plasma membrane contacts
title_fullStr Ferroptosis spreads to neighboring cells via plasma membrane contacts
title_full_unstemmed Ferroptosis spreads to neighboring cells via plasma membrane contacts
title_short Ferroptosis spreads to neighboring cells via plasma membrane contacts
title_sort ferroptosis spreads to neighboring cells via plasma membrane contacts
url https://doi.org/10.1038/s41467-025-58175-w
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