IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-29723-5.html
   My bibliography  Save this article

Cooperative interaction between ERα and the EMT-inducer ZEB1 reprograms breast cancer cells for bone metastasis

Author

Listed:
  • Nastaran Mohammadi Ghahhari

    (Université de Genève, Sciences III)

  • Magdalena K. Sznurkowska

    (Institute of Molecular Health Sciences, ETH Zurich)

  • Nicolas Hulo

    (Université de Genève)

  • Lilia Bernasconi

    (Université de Genève, Sciences III)

  • Nicola Aceto

    (Institute of Molecular Health Sciences, ETH Zurich)

  • Didier Picard

    (Université de Genève, Sciences III)

Abstract

The epithelial to mesenchymal transition (EMT) has been proposed to contribute to the metastatic spread of breast cancer cells. EMT-promoting transcription factors determine a continuum of different EMT states. In contrast, estrogen receptor α (ERα) helps to maintain the epithelial phenotype of breast cancer cells and its expression is crucial for effective endocrine therapies. Determining whether and how EMT-associated transcription factors such as ZEB1 modulate ERα signaling during early stages of EMT could promote the discovery of therapeutic approaches to suppress metastasis. Here we show that, shortly after induction of EMT and while cells are still epithelial, ZEB1 modulates ERα-mediated transcription induced by estrogen or cAMP signaling in breast cancer cells. Based on these findings and our ex vivo and xenograft results, we suggest that the functional interaction between ZEB1 and ERα may alter the tissue tropism of metastatic breast cancer cells towards bone.

Suggested Citation

  • Nastaran Mohammadi Ghahhari & Magdalena K. Sznurkowska & Nicolas Hulo & Lilia Bernasconi & Nicola Aceto & Didier Picard, 2022. "Cooperative interaction between ERα and the EMT-inducer ZEB1 reprograms breast cancer cells for bone metastasis," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-29723-5
    DOI: 10.1038/s41467-022-29723-5
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-29723-5
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-022-29723-5?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. Xin Ye & Wai Leong Tam & Tsukasa Shibue & Yasemin Kaygusuz & Ferenc Reinhardt & Elinor Ng Eaton & Robert A. Weinberg, 2015. "Distinct EMT programs control normal mammary stem cells and tumour-initiating cells," Nature, Nature, vol. 525(7568), pages 256-260, September.
    2. Waltraut Lehmann & Dirk Mossmann & Julia Kleemann & Kerstin Mock & Chris Meisinger & Tilman Brummer & Ricarda Herr & Simone Brabletz & Marc P. Stemmler & Thomas Brabletz, 2016. "ZEB1 turns into a transcriptional activator by interacting with YAP1 in aggressive cancer types," Nature Communications, Nature, vol. 7(1), pages 1-15, April.
    3. Hartland W. Jackson & Jana R. Fischer & Vito R. T. Zanotelli & H. Raza Ali & Robert Mechera & Savas D. Soysal & Holger Moch & Simone Muenst & Zsuzsanna Varga & Walter P. Weber & Bernd Bodenmiller, 2020. "The single-cell pathology landscape of breast cancer," Nature, Nature, vol. 578(7796), pages 615-620, February.
    4. Ievgenia Pastushenko & Federico Mauri & Yura Song & Florian Cock & Bob Meeusen & Benjamin Swedlund & Francis Impens & Delphi Haver & Matthieu Opitz & Manuel Thery & Yacine Bareche & Gaelle Lapouge & M, 2021. "Fat1 deletion promotes hybrid EMT state, tumour stemness and metastasis," Nature, Nature, vol. 589(7842), pages 448-455, January.
    5. Ievgenia Pastushenko & Audrey Brisebarre & Alejandro Sifrim & Marco Fioramonti & Tatiana Revenco & Soufiane Boumahdi & Alexandra Van Keymeulen & Daniel Brown & Virginie Moers & Sophie Lemaire & Sarah , 2018. "Identification of the tumour transition states occurring during EMT," Nature, Nature, vol. 556(7702), pages 463-468, April.
    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. Peter Bailey & Rachel A. Ridgway & Patrizia Cammareri & Mairi Treanor-Taylor & Ulla-Maja Bailey & Christina Schoenherr & Max Bone & Daniel Schreyer & Karin Purdie & Jason Thomson & William Rickaby & R, 2023. "Driver gene combinations dictate cutaneous squamous cell carcinoma disease continuum progression," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    2. Juan Du & Junlei Zhang & Lin Wang & Xun Wang & Yaxing Zhao & Jiaoying Lu & Tingmin Fan & Meng Niu & Jie Zhang & Fei Cheng & Jun Li & Qi Zhu & Daoqiang Zhang & Hao Pei & Guang Li & Xingguang Liang & He, 2023. "Selective oxidative protection leads to tissue topological changes orchestrated by macrophage during ulcerative colitis," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    3. Yunhao Bai & Bokai Zhu & John-Paul Oliveria & Bryan J. Cannon & Dorien Feyaerts & Marc Bosse & Kausalia Vijayaragavan & Noah F. Greenwald & Darci Phillips & Christian M. Schürch & Samuel M. Naik & Edw, 2023. "Expanded vacuum-stable gels for multiplexed high-resolution spatial histopathology," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    4. C. Megan Young & Laurent Beziaud & Pierre Dessen & Angela Madurga Alonso & Albert Santamaria-Martínez & Joerg Huelsken, 2023. "Metabolic dependencies of metastasis-initiating cells in female breast cancer," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    5. Rui Chen & Jiasu Xu & Boqian Wang & Yi Ding & Aynur Abdulla & Yiyang Li & Lai Jiang & Xianting Ding, 2024. "SpiDe-Sr: blind super-resolution network for precise cell segmentation and clustering in spatial proteomics imaging," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    6. Kaiwen Wang & Yuqiu Yang & Fangjiang Wu & Bing Song & Xinlei Wang & Tao Wang, 2023. "Comparative analysis of dimension reduction methods for cytometry by time-of-flight data," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    7. Patrick Aouad & Yueyun Zhang & Fabio Martino & Céline Stibolt & Simak Ali & Giovanna Ambrosini & Sendurai A. Mani & Kelly Maggs & Hazel M. Quinn & George Sflomos & Cathrin Brisken, 2022. "Epithelial-mesenchymal plasticity determines estrogen receptor positive breast cancer dormancy and epithelial reconversion drives recurrence," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    8. Anat Kreimer & Tal Ashuach & Fumitaka Inoue & Alex Khodaverdian & Chengyu Deng & Nir Yosef & Nadav Ahituv, 2022. "Massively parallel reporter perturbation assays uncover temporal regulatory architecture during neural differentiation," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    9. Zhiyuan Yuan & Yisi Li & Minglei Shi & Fan Yang & Juntao Gao & Jianhua Yao & Michael Q. Zhang, 2022. "SOTIP is a versatile method for microenvironment modeling with spatial omics data," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    10. Stefanie Hiltbrunner & Lena Cords & Sabrina Kasser & Sandra N. Freiberger & Susanne Kreutzer & Nora C. Toussaint & Linda Grob & Isabelle Opitz & Michael Messerli & Martin Zoche & Alex Soltermann & Mar, 2023. "Acquired resistance to anti-PD1 therapy in patients with NSCLC associates with immunosuppressive T cell phenotype," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    11. Guidantonio Malagoli Tagliazucchi & Anna J. Wiecek & Eloise Withnell & Maria Secrier, 2023. "Genomic and microenvironmental heterogeneity shaping epithelial-to-mesenchymal trajectories in cancer," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    12. Mariel C. Paul & Christian Schneeweis & Chiara Falcomatà & Chuan Shan & Daniel Rossmeisl & Stella Koutsouli & Christine Klement & Magdalena Zukowska & Sebastian A. Widholz & Moritz Jesinghaus & Konsta, 2023. "Non-canonical functions of SNAIL drive context-specific cancer progression," Nature Communications, Nature, vol. 14(1), pages 1-21, December.
    13. Darci Phillips & Magdalena Matusiak & Belén Rivero Gutierrez & Salil S. Bhate & Graham L. Barlow & Sizun Jiang & Janos Demeter & Kimberly S. Smythe & Robert H. Pierce & Steven P. Fling & Nirasha Ramch, 2021. "Immune cell topography predicts response to PD-1 blockade in cutaneous T cell lymphoma," Nature Communications, Nature, vol. 12(1), pages 1-18, December.
    14. Jiawen Bu & Yixiao Zhang & Sijin Wu & Haonan Li & Lisha Sun & Yang Liu & Xudong Zhu & Xinbo Qiao & Qingtian Ma & Chao Liu & Nan Niu & Jinqi Xue & Guanglei Chen & Yongliang Yang & Caigang Liu, 2023. "KK-LC-1 as a therapeutic target to eliminate ALDH+ stem cells in triple negative breast cancer," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    15. Thomas Hu & Mayar Allam & Shuangyi Cai & Walter Henderson & Brian Yueh & Aybuke Garipcan & Anton V. Ievlev & Maryam Afkarian & Semir Beyaz & Ahmet F. Coskun, 2023. "Single-cell spatial metabolomics with cell-type specific protein profiling for tissue systems biology," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    16. Hugo Croizer & Rana Mhaidly & Yann Kieffer & Geraldine Gentric & Lounes Djerroudi & Renaud Leclere & Floriane Pelon & Catherine Robley & Mylene Bohec & Arnaud Meng & Didier Meseure & Emanuela Romano &, 2024. "Deciphering the spatial landscape and plasticity of immunosuppressive fibroblasts in breast cancer," Nature Communications, Nature, vol. 15(1), pages 1-28, December.
    17. Michele Bortolomeazzi & Lucia Montorsi & Damjan Temelkovski & Mohamed Reda Keddar & Amelia Acha-Sagredo & Michael J. Pitcher & Gianluca Basso & Luigi Laghi & Manuel Rodriguez-Justo & Jo Spencer & Fran, 2022. "A SIMPLI (Single-cell Identification from MultiPLexed Images) approach for spatially-resolved tissue phenotyping at single-cell resolution," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    18. Lining Liang & Hao Sun & Wei Zhang & Mengdan Zhang & Xiao Yang & Rui Kuang & Hui Zheng, 2016. "Meta-Analysis of EMT Datasets Reveals Different Types of EMT," PLOS ONE, Public Library of Science, vol. 11(6), pages 1-22, June.
    19. Yael Amitay & Yuval Bussi & Ben Feinstein & Shai Bagon & Idan Milo & Leeat Keren, 2023. "CellSighter: a neural network to classify cells in highly multiplexed images," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    20. Peng Lu & Karolyn A. Oetjen & Diane E. Bender & Marianna B. Ruzinova & Daniel A. C. Fisher & Kevin G. Shim & Russell K. Pachynski & W. Nathaniel Brennen & Stephen T. Oh & Daniel C. Link & Daniel L. J., 2023. "IMC-Denoise: a content aware denoising pipeline to enhance Imaging Mass Cytometry," Nature Communications, Nature, vol. 14(1), pages 1-16, 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:13:y:2022:i:1:d:10.1038_s41467-022-29723-5. 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.