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TES-1/Tes protects junctional actin networks under tension from self-injury during epidermal morphogenesis in the C. elegans embryo

Allison M. Lynch, Bethany G. Lucas, Jonathan D. Winkelman, Sterling C.T. Martin, Samuel D. Block, Anjon Audhya, Margaret L. Gardel, View ORCID ProfileJeff Hardin
doi: https://doi.org/10.1101/2021.09.30.462556
Allison M. Lynch
1Program in Biophysics, University of Wisconsin, Madison, WI 53706 USA
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Bethany G. Lucas
4Department of Biology, Regis University, 3333 Regis Boulevard, Denver, Colorado 80221 USA
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Jonathan D. Winkelman
5Institute for Biophysical Dynamics, University of Chicago, Chicago, IL 60637
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Sterling C.T. Martin
1Program in Biophysics, University of Wisconsin, Madison, WI 53706 USA
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Samuel D. Block
3Department of Biomolecular Chemistry, University of Wisconsin, Madison, WI 53706 USA
6Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, 77 Massachusetts Ave. Building 76-511, Cambridge, MA 02139 USA
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Anjon Audhya
3Department of Biomolecular Chemistry, University of Wisconsin, Madison, WI 53706 USA
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Margaret L. Gardel
5Institute for Biophysical Dynamics, University of Chicago, Chicago, IL 60637
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Jeff Hardin
1Program in Biophysics, University of Wisconsin, Madison, WI 53706 USA
2Department of Integrative Biology, University of Wisconsin, Madison, WI 53706 USA
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  • ORCID record for Jeff Hardin
  • For correspondence: jdhardin@wisc.edu
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Abstract

During embryonic morphogenesis, the integrity of epithelial tissues depends on the ability of cells in tissue sheets to undergo rapid changes in cell shape while preventing self-injury to junctional actin networks. LIM domain-containing repeat (LCR) proteins are recruited to sites of strained actin filaments in cultured cells [1–3], and are therefore promising candidates for mediating self-healing of actin networks, but whether they play similar roles in living organisms has not been determined. Here, we establish roles for Caenorhabditis elegans TES-1/Tes, an actin-binding LCR protein present at apical junctions, during epithelial morphogenesis. TES-1::GFP is recruited to apical junctions during embryonic elongation, when junctions are under tension; in embryos in which stochastic failure of cell elongation occurs, TES-1 is only strongly recruited to junctions in cells that successfully elongate, and recruitment is severely compromised in genetic backgrounds in which cell shape changes do not successfully occur. tes-1 mutant embryos display junctional F-actin defects, and loss of TES-1 strongly enhances tension-dependent injury of junctional actin networks in hypomorphic mutant backgrounds for CCC components, suggesting that TES-1 helps to prevent self-injury of junctional actin networks during rapid cell shape change. Consistent with such role, a fragment of TES-1 containing its LIM domains localizes to stress fiber strain sites (SFSS) in cultured vertebrate cells. Together, these data establish TES-1 as a tension-sensitive stabilizer of the junctional actin cytoskeleton during embryonic morphogenesis.

Competing Interest Statement

The authors have declared no competing interest.

  • Abbreviations used in this study

    AJ
    adherens junction
    CCC
    cadherin-catenin complex
    CFB
    circumferential filament bundle
    DIC
    differential interference contrast
    LIM
    Lin-l1, Isl-1, Mec-3
    PET
    Prickle, Espinas, Testin
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    Posted October 01, 2021.
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    TES-1/Tes protects junctional actin networks under tension from self-injury during epidermal morphogenesis in the C. elegans embryo
    Allison M. Lynch, Bethany G. Lucas, Jonathan D. Winkelman, Sterling C.T. Martin, Samuel D. Block, Anjon Audhya, Margaret L. Gardel, Jeff Hardin
    bioRxiv 2021.09.30.462556; doi: https://doi.org/10.1101/2021.09.30.462556
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    TES-1/Tes protects junctional actin networks under tension from self-injury during epidermal morphogenesis in the C. elegans embryo
    Allison M. Lynch, Bethany G. Lucas, Jonathan D. Winkelman, Sterling C.T. Martin, Samuel D. Block, Anjon Audhya, Margaret L. Gardel, Jeff Hardin
    bioRxiv 2021.09.30.462556; doi: https://doi.org/10.1101/2021.09.30.462556

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