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E-cadherin integrates mechanotransduction and EGFR signaling to control junctional tissue polarization and tight junction positioning

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  • Matthias Rübsam

    (Department of Dermatology, University of Cologne
    Cologne Excellence Cluster for Stress Responses in Ageing-associated diseases (CECAD)
    Center for Molecular Medicine Cologne (CMMC) University of Cologne)

  • Aaron F. Mertz

    (Yale University
    The Rockefeller University)

  • Akiharu Kubo

    (Keio University School of Medicine)

  • Susanna Marg

    (Hannover Medical School)

  • Christian Jüngst

    (Cologne Excellence Cluster for Stress Responses in Ageing-associated diseases (CECAD))

  • Gladiola Goranci-Buzhala

    (Department of Dermatology, University of Cologne
    Cologne Excellence Cluster for Stress Responses in Ageing-associated diseases (CECAD)
    Center for Molecular Medicine Cologne (CMMC) University of Cologne)

  • Astrid C. Schauss

    (Cologne Excellence Cluster for Stress Responses in Ageing-associated diseases (CECAD))

  • Valerie Horsley

    (Yale University)

  • Eric R. Dufresne

    (Yale University
    Yale University)

  • Markus Moser

    (Max Planck Institute for Biochemistry)

  • Wolfgang Ziegler

    (Hannover Medical School)

  • Masayuki Amagai

    (Keio University School of Medicine)

  • Sara A. Wickström

    (Cologne Excellence Cluster for Stress Responses in Ageing-associated diseases (CECAD)
    Max Planck Institute for Biology of Ageing)

  • Carien M. Niessen

    (Department of Dermatology, University of Cologne
    Cologne Excellence Cluster for Stress Responses in Ageing-associated diseases (CECAD)
    Center for Molecular Medicine Cologne (CMMC) University of Cologne)

Abstract

Generation of a barrier in multi-layered epithelia like the epidermis requires restricted positioning of functional tight junctions (TJ) to the most suprabasal viable layer. This positioning necessitates tissue-level polarization of junctions and the cytoskeleton through unknown mechanisms. Using quantitative whole-mount imaging, genetic ablation, and traction force microscopy and atomic force microscopy, we find that ubiquitously localized E-cadherin coordinates tissue polarization of tension-bearing adherens junction (AJ) and F-actin organization to allow formation of an apical TJ network only in the uppermost viable layer. Molecularly, E-cadherin localizes and tunes EGFR activity and junctional tension to inhibit premature TJ complex formation in lower layers while promoting increased tension and TJ stability in the granular layer 2. In conclusion, our data identify an E-cadherin-dependent mechanical circuit that integrates adhesion, contractile forces and biochemical signaling to drive the polarized organization of junctional tension necessary to build an in vivo epithelial barrier.

Suggested Citation

  • Matthias Rübsam & Aaron F. Mertz & Akiharu Kubo & Susanna Marg & Christian Jüngst & Gladiola Goranci-Buzhala & Astrid C. Schauss & Valerie Horsley & Eric R. Dufresne & Markus Moser & Wolfgang Ziegler , 2017. "E-cadherin integrates mechanotransduction and EGFR signaling to control junctional tissue polarization and tight junction positioning," Nature Communications, Nature, vol. 8(1), pages 1-16, December.
    • Handle: RePEc:nat:natcom:v:8:y:2017:i:1:d:10.1038_s41467-017-01170-7
    DOI: 10.1038/s41467-017-01170-7
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    Cited by:

    1. John Fadul & Teresa Zulueta-Coarasa & Gloria M. Slattum & Nadja M. Redd & Mauricio Franco Jin & Michael J. Redd & Stephan Daetwyler & Danielle Hedeen & Jan Huisken & Jody Rosenblatt, 2021. "KRas-transformed epithelia cells invade and partially dedifferentiate by basal cell extrusion," Nature Communications, Nature, vol. 12(1), pages 1-9, December.

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