IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v16y2025i1d10.1038_s41467-025-58175-w.html
   My bibliography  Save this article

Ferroptosis spreads to neighboring cells via plasma membrane contacts

Author

Listed:
  • Bernhard F. Roeck

    (University of Cologne
    University of Cologne)

  • Sara Lotfipour Nasudivar

    (University of Cologne
    University of Cologne)

  • Michael R. H. Vorndran

    (University of Cologne
    University of Cologne)

  • Lena Schueller

    (University of Cologne
    University of Cologne)

  • F. Isil Yapici

    (University of Cologne
    University of Cologne
    University Hospital of Cologne)

  • Matthias Rübsam

    (University of Cologne
    University Hospital of Cologne
    University of Cologne)

  • Silvia Karstedt

    (University of Cologne
    University of Cologne
    University Hospital of Cologne)

  • Carien M. Niessen

    (University of Cologne
    University Hospital of Cologne
    University of Cologne)

  • Ana J. Garcia-Saez

    (University of Cologne
    University of Cologne
    Max Planck Institute of Biophysics)

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.

Suggested Citation

  • Bernhard F. Roeck & Sara Lotfipour Nasudivar & Michael R. H. Vorndran & Lena Schueller & F. Isil Yapici & Matthias Rübsam & Silvia Karstedt & Carien M. Niessen & Ana J. Garcia-Saez, 2025. "Ferroptosis spreads to neighboring cells via plasma membrane contacts," Nature Communications, Nature, vol. 16(1), pages 1-18, December.
  • Handle: RePEc:nat:natcom:v:16:y:2025:i:1:d:10.1038_s41467-025-58175-w
    DOI: 10.1038/s41467-025-58175-w
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-025-58175-w
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-025-58175-w?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Christina M. Bebber & Emily S. Thomas & Jenny Stroh & Zhiyi Chen & Ariadne Androulidaki & Anna Schmitt & Michaela N. Höhne & Lukas Stüker & Cleidson Pádua Alves & Armin Khonsari & Marcel A. Dammert & , 2021. "Ferroptosis response segregates small cell lung cancer (SCLC) neuroendocrine subtypes," Nature Communications, Nature, vol. 12(1), pages 1-19, December.
    2. Eikan Mishima & Toshitaka Nakamura & Jiashuo Zheng & Weijia Zhang & André Santos Dias Mourão & Peter Sennhenn & Marcus Conrad, 2023. "DHODH inhibitors sensitize to ferroptosis by FSP1 inhibition," Nature, Nature, vol. 619(7968), pages 9-18, July.
    3. Florencio Porto Freitas & Hamed Alborzinia & Ancély Ferreira dos Santos & Palina Nepachalovich & Lohans Pedrera & Omkar Zilka & Alex Inague & Corinna Klein & Nesrine Aroua & Kamini Kaushal & Bettina K, 2024. "7-Dehydrocholesterol is an endogenous suppressor of ferroptosis," Nature, Nature, vol. 626(7998), pages 401-410, February.
    4. Jiao Wu & Alexander M. Minikes & Minghui Gao & Huijie Bian & Yong Li & Brent R. Stockwell & Zhi-Nan Chen & Xuejun Jiang, 2019. "Publisher Correction: Intercellular interaction dictates cancer cell ferroptosis via NF2–YAP signalling," Nature, Nature, vol. 572(7770), pages 20-20, August.
    5. Jiao Wu & Alexander M. Minikes & Minghui Gao & Huijie Bian & Yong Li & Brent R. Stockwell & Zhi-Nan Chen & Xuejun Jiang, 2019. "Intercellular interaction dictates cancer cell ferroptosis via NF2–YAP signalling," Nature, Nature, vol. 572(7769), pages 402-406, August.
    6. Sebastian Doll & Florencio Porto Freitas & Ron Shah & Maceler Aldrovandi & Milene Costa Silva & Irina Ingold & Andrea Goya Grocin & Thamara Nishida Xavier da Silva & Elena Panzilius & Christina H. Sch, 2019. "FSP1 is a glutathione-independent ferroptosis suppressor," Nature, Nature, vol. 575(7784), pages 693-698, November.
    7. Hannah K. C. Co & Chia-Chou Wu & Yi-Chen Lee & Sheng-hong Chen, 2024. "Emergence of large-scale cell death through ferroptotic trigger waves," Nature, Nature, vol. 631(8021), pages 654-662, July.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Haibin Deng & Liang Zhao & Huixiang Ge & Yanyun Gao & Yan Fu & Yantang Lin & Mojgan Masoodi & Tereza Losmanova & Michaela Medová & Julien Ott & Min Su & Wenxiang Wang & Ren-Wang Peng & Patrick Dorn & , 2025. "Ubiquinol-mediated suppression of mitochondria-associated ferroptosis is a targetable function of lactate dehydrogenase B in cancer," Nature Communications, Nature, vol. 16(1), pages 1-17, December.
    2. Pranavi Koppula & Guang Lei & Yilei Zhang & Yuelong Yan & Chao Mao & Lavanya Kondiparthi & Jiejun Shi & Xiaoguang Liu & Amber Horbath & Molina Das & Wei Li & Masha V. Poyurovsky & Kellen Olszewski & B, 2022. "A targetable CoQ-FSP1 axis drives ferroptosis- and radiation-resistance in KEAP1 inactive lung cancers," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    3. Hui Yang & Qingqing Li & Xingxing Chen & Mingzhe Weng & Yakai Huang & Qiwen Chen & Xiaocen Liu & Haoyu Huang & Yanhuizhi Feng & Hanyu Zhou & Mengying Zhang & Weiya Pei & Xueqin Li & Qingsheng Fu & Lia, 2024. "Targeting SOX13 inhibits assembly of respiratory chain supercomplexes to overcome ferroptosis resistance in gastric cancer," Nature Communications, Nature, vol. 15(1), pages 1-21, December.
    4. André Gollowitzer & Helmut Pein & Zhigang Rao & Lorenz Waltl & Leonhard Bereuter & Konstantin Loeser & Tobias Meyer & Vajiheh Jafari & Finja Witt & René Winkler & Fengting Su & Silke Große & Maria Thü, 2025. "Attenuated growth factor signaling during cell death initiation sensitizes membranes towards peroxidation," Nature Communications, Nature, vol. 16(1), pages 1-31, December.
    5. Xin-yu He & Xiao Fan & Lei Qu & Xiang Wang & Li Jiang & Ling-jie Sang & Cheng-yu Shi & Siyi Lin & Jie-cheng Yang & Zuo-zhen Yang & Kai Lei & Jun-hong Li & Huai-qiang Ju & Qingfeng Yan & Jian Liu & Fud, 2023. "LncRNA modulates Hippo-YAP signaling to reprogram iron metabolism," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    6. Athena Kyrkou & Robert Valla & Yao Zhang & Giulia Ambrosi & Stephanie Laier & Karin Müller-Decker & Michael Boutros & Aurelio A. Teleman, 2024. "G6PD and ACSL3 are synthetic lethal partners of NF2 in Schwann cells," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    7. Yuma Saimoto & Daiki Kusakabe & Kazushi Morimoto & Yuta Matsuoka & Eisho Kozakura & Nao Kato & Kayoko Tsunematsu & Tomohiro Umeno & Tamiko Kiyotani & Shota Matsumoto & Mieko Tsuji & Tasuku Hirayama & , 2025. "Lysosomal lipid peroxidation contributes to ferroptosis induction via lysosomal membrane permeabilization," Nature Communications, Nature, vol. 16(1), pages 1-13, December.
    8. Feixia Wang & Yifeng Liu & Feida Ni & Jiani Jin & Yiqing Wu & Yun Huang & Xiaohang Ye & Xilin Shen & Yue Ying & Jianhua Chen & Ruixue Chen & Yanye Zhang & Xiao Sun & Siwen Wang & Xiao Xu & Chuan Chen , 2022. "BNC1 deficiency-triggered ferroptosis through the NF2-YAP pathway induces primary ovarian insufficiency," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    9. Bin Huang & Hui Wang & Shuo Liu & Meng Hao & Dan Luo & Yi Zhou & Ying Huang & Yong Nian & Lei Zhang & Bo Chu & Chengqian Yin, 2025. "Palmitoylation-dependent regulation of GPX4 suppresses ferroptosis," Nature Communications, Nature, vol. 16(1), pages 1-19, December.
    10. Yandi Wu & Tongsheng Huang & Xinghui Li & Conghui Shen & Honglin Ren & Haiping Wang & Teng Wu & Xinlu Fu & Shijie Deng & Ziqi Feng & Shijie Xiong & Hui Li & Saifei Gao & Zhenyu Yang & Fei Gao & Lele D, 2023. "Retinol dehydrogenase 10 reduction mediated retinol metabolism disorder promotes diabetic cardiomyopathy in male mice," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    11. Wei Yang & Bo Mu & Jing You & Chenyu Tian & Huachao Bin & Zhiqiang Xu & Liting Zhang & Ronggang Ma & Ming Wu & Guo Zhang & Chong Huang & Linli Li & Zhenhua Shao & Lunzhi Dai & Laurent Désaubry & Sheng, 2022. "Non-classical ferroptosis inhibition by a small molecule targeting PHB2," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    12. Nathan P. Ward & Sang Jun Yoon & Tyce Flynn & Amanda M. Sherwood & Maddison A. Olley & Juliana Madej & Gina M. DeNicola, 2024. "Mitochondrial respiratory function is preserved under cysteine starvation via glutathione catabolism in NSCLC," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    13. Yun Lv & Chunhui Liang & Qichao Sun & Jing Zhu & Haiyan Xu & Xiaoqing Li & Yao-yao Li & Qihai Wang & Huiqing Yuan & Bo Chu & Deyu Zhu, 2023. "Structural insights into FSP1 catalysis and ferroptosis inhibition," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    14. Jun Jiang & Lili Yang & Qianqian Xie & Xi Liu & Jie Jiang & Jie Zhang & Shuping Zhang & Huizhen Zheng & Wenjie Li & Xiaoming Cai & Sijin Liu & Ruibin Li, 2024. "Synthetic vectors for activating the driving axis of ferroptosis," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    15. Zifan Ye & Lei Fu & Shuangyu Li & Ziying Chen & Jianhong Ouyang & Xinci Shang & Yanli Liu & Lianghui Gao & Yipeng Wang, 2024. "Synergistic collaboration between AMPs and non-direct antimicrobial cationic peptides," Nature Communications, Nature, vol. 15(1), pages 1-26, December.
    16. Da Teng & Kenneth D. Swanson & Ruiheng Wang & Aojia Zhuang & Haofeng Wu & Zhixin Niu & Li Cai & Faith R. Avritt & Lei Gu & John M. Asara & Yaqing Zhang & Bin Zheng, 2025. "DHODH modulates immune evasion of cancer cells via CDP-Choline dependent regulation of phospholipid metabolism and ferroptosis," Nature Communications, Nature, vol. 16(1), pages 1-16, December.
    17. Samya Van Coillie & Emily Van San & Ines Goetschalckx & Bartosz Wiernicki & Banibrata Mukhopadhyay & Wulf Tonnus & Sze Men Choi & Ria Roelandt & Catalina Dumitrascu & Ludwig Lamberts & Geert Dams & Wa, 2022. "Targeting ferroptosis protects against experimental (multi)organ dysfunction and death," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    18. Zhe Wang & Xin Yang & Delin Chen & Yanqing Liu & Zhiming Li & Shoufu Duan & Zhiguo Zhang & Xuejun Jiang & Brent R. Stockwell & Wei Gu, 2024. "GAS41 modulates ferroptosis by anchoring NRF2 on chromatin," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    19. Dadi Jiang & Youming Guo & Tianyu Wang & Liang Wang & Yuelong Yan & Ling Xia & Rakesh Bam & Zhifen Yang & Hyemin Lee & Takao Iwawaki & Boyi Gan & Albert C. Koong, 2024. "IRE1α determines ferroptosis sensitivity through regulation of glutathione synthesis," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    20. Giovanni Tosi & Alessandro Paoli & Gaia Zuccolotto & Emilia Turco & Manuela Simonato & Daniela Tosoni & Francesco Tucci & Pietro Lugato & Monica Giomo & Nicola Elvassore & Antonio Rosato & Paola Cogo , 2024. "Cancer cell stiffening via CoQ10 and UBIAD1 regulates ECM signaling and ferroptosis in breast cancer," Nature Communications, Nature, vol. 15(1), pages 1-24, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:16:y:2025:i:1:d:10.1038_s41467-025-58175-w. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.