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Nanotopography enhances dynamic remodeling of tight junction proteins through cytosolic complexes

View ORCID ProfileXiao Huang, Xiaoyu Shi, Mollie Eva Hansen, Cameron L. Nemeth, Anna Ceili, Bo Huang, Theodora Mauro, Michael Koval, Tejal A. Desai
doi: https://doi.org/10.1101/858118
Xiao Huang
1Department of Bioengineering and Therapeutic Sciences, University of California, San Francisco, San Francisco, California, USA
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  • ORCID record for Xiao Huang
Xiaoyu Shi
2Department of Pharmaceutical Chemistry, University of California, San Francisco, San Francisco, California, USA
3Department of Developmental and Cell Biology, University of California, Irvine, Irvine, California, USA
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Mollie Eva Hansen
4UC Berkeley-UCSF Graduate Program in Bioengineering, University of California, San Francisco, San Francisco, California, USA
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Cameron L. Nemeth
4UC Berkeley-UCSF Graduate Program in Bioengineering, University of California, San Francisco, San Francisco, California, USA
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Anna Ceili
5Department of Dermatology, University of California, San Francisco, San Francisco, California, USA
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Bo Huang
2Department of Pharmaceutical Chemistry, University of California, San Francisco, San Francisco, California, USA
6Department of Biochemistry and Biophysics, University of California, San Francisco, San Francisco, California, USA
7Chan Zuckerberg Biohub, San Francisco, California, USA
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Theodora Mauro
5Department of Dermatology, University of California, San Francisco, San Francisco, California, USA
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Michael Koval
8Division of Pulmonary, Allergy, and Critical Care Medicine and Department of Cell Biology, Emory University School of Medicine, Atlanta, Georgia, USA
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Tejal A. Desai
1Department of Bioengineering and Therapeutic Sciences, University of California, San Francisco, San Francisco, California, USA
4UC Berkeley-UCSF Graduate Program in Bioengineering, University of California, San Francisco, San Francisco, California, USA
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  • For correspondence: tejal.desai@ucsf.edu
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Abstract

The epithelial tight junction regulates barrier function and is responsive to extracellular stimuli. Here we demonstrated that contact of synthetic surfaces with defined nanotopography at the apical surface of epithelial monolayers increased paracellular permeability of macromolecules. To monitor changes in tight junction morphology in live cells, we fluorescently tagged the scaffold protein zonula occludens-1 (ZO-1) through CRISPR/Cas9-based gene editing. Contact between cells and nanostructured surfaces destabilized junction-associated ZO-1 and promoted its arrangement into highly dynamic non-junctional cytosolic complexes that averaged ∼2 μm in diameter. Junction-associated ZO-1 rapidly remodeled, and we also observed the direct transformation of cytosolic complexes into junction-like structures. Claudin-family tight junction transmembrane proteins and F-actin also were associated with these ZO-1 containing cytosolic complexes. These data suggest that the cytosolic structures are novel intermediates formed in response to nanotopographic cues that facilitate rapid tight junction remodeling in order to regulate paracellular permeability.

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Posted November 28, 2019.
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Nanotopography enhances dynamic remodeling of tight junction proteins through cytosolic complexes
Xiao Huang, Xiaoyu Shi, Mollie Eva Hansen, Cameron L. Nemeth, Anna Ceili, Bo Huang, Theodora Mauro, Michael Koval, Tejal A. Desai
bioRxiv 858118; doi: https://doi.org/10.1101/858118
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Nanotopography enhances dynamic remodeling of tight junction proteins through cytosolic complexes
Xiao Huang, Xiaoyu Shi, Mollie Eva Hansen, Cameron L. Nemeth, Anna Ceili, Bo Huang, Theodora Mauro, Michael Koval, Tejal A. Desai
bioRxiv 858118; doi: https://doi.org/10.1101/858118

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