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Reciprocal regulation between cell mechanics and ZO-1 guides tight junction assembly and epithelial morphogenesis

Alexis J. Haas, Ceniz Zihni, Susanne M. Krug, Riccardo Maraspini, Tetsuhisa Otani, Mikio Furuse, Alf Honigmann, View ORCID ProfileMaria Balda, Karl Matter
doi: https://doi.org/10.1101/2022.07.17.500023
Alexis J. Haas
1UCL Institute of Ophthalmology, University College London, London EC1V 9EL, UK
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Ceniz Zihni
1UCL Institute of Ophthalmology, University College London, London EC1V 9EL, UK
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Susanne M. Krug
2Clinical Physiology / Nutritional Medicine, Charité - Universitätsmedizin Berlin, Campus Benjamin Franklin,12203 Berlin, Germany
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Riccardo Maraspini
4Max Planck Institute of Molecular Cell Biology and Genetics, 01309 Dresden, Germany
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Tetsuhisa Otani
3Division of Cell Structure, National Institute for Physiological Sciences, Okazaki, Aichi 444-8787, Japan
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Mikio Furuse
3Division of Cell Structure, National Institute for Physiological Sciences, Okazaki, Aichi 444-8787, Japan
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Alf Honigmann
4Max Planck Institute of Molecular Cell Biology and Genetics, 01309 Dresden, Germany
5Biotechnologisches Zentrum (BIOTEC), Center for Molecular and Cellular Bioengineering (CMCB), Technische Universität Dresden, 01307 Dresden, Germany
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Maria Balda
1UCL Institute of Ophthalmology, University College London, London EC1V 9EL, UK
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  • For correspondence: k.matter@ucl.ac.uk
Karl Matter
1UCL Institute of Ophthalmology, University College London, London EC1V 9EL, UK
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ABSTRACT

Formation and maintenance of tissue barriers require the coordination of cell mechanics and cell-cell junction assembly. Here, we combined methods to modulate ECM stiffness and to measure mechanical forces on adhesion complexes to investigate how tight junctions regulate cell mechanics and epithelial morphogenesis. We found that depletion of the tight junction adaptor ZO-1 regulates cytoskeletal tension at cell-matrix and cell-cell interfaces in an ECM stiffness-regulated manner, possibly via differential organisation of the actin cytoskeleton. ZO-1 depletion inhibited junction assembly and disrupted morphogenesis in an ECM stiffness-dependent manner. Both processes were rescued by inhibition of cell contractility. Although ZO-1-deficient cells could assemble functional barriers at low tension, their tight junctions remained corrupted with strongly reduced and discontinuous recruitment of junctional components. Our results thus reveal that reciprocal regulation between ZO-1 and cell mechanics controls tight junction assembly and epithelial morphogenesis, and that tension-independent roles of ZO-1 control proper junction organisation.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • ↵* Address for Communications UCL Institute of Ophthalmology, University College London, Bath Street, London EC1V 9EL, UK, T: 44/20 76084014/6861, k.matter{at}ucl.ac.uk/m.balda{at}ucl.ac.uk

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Posted July 18, 2022.
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Reciprocal regulation between cell mechanics and ZO-1 guides tight junction assembly and epithelial morphogenesis
Alexis J. Haas, Ceniz Zihni, Susanne M. Krug, Riccardo Maraspini, Tetsuhisa Otani, Mikio Furuse, Alf Honigmann, Maria Balda, Karl Matter
bioRxiv 2022.07.17.500023; doi: https://doi.org/10.1101/2022.07.17.500023
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Reciprocal regulation between cell mechanics and ZO-1 guides tight junction assembly and epithelial morphogenesis
Alexis J. Haas, Ceniz Zihni, Susanne M. Krug, Riccardo Maraspini, Tetsuhisa Otani, Mikio Furuse, Alf Honigmann, Maria Balda, Karl Matter
bioRxiv 2022.07.17.500023; doi: https://doi.org/10.1101/2022.07.17.500023

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