TES-1/Tes and ZYX-1/Zyxin protect junctional actin networks under tension during epidermal morphogenesis in the C. elegans embryo

Allison M Lynch; Yuyun Zhu; Bethany G Lucas; Jonathan D Winkelman; Keliya Bai; Sterling C T Martin; Samuel Block; Mark M Slabodnick; Anjon Audhya; Bob Goldstein; Jonathan Pettitt; Margaret L Gardel; Jeff Hardin

doi:10.1016/j.cub.2022.10.045

TES-1/Tes and ZYX-1/Zyxin protect junctional actin networks under tension during epidermal morphogenesis in the C. elegans embryo

Curr Biol. 2022 Dec 5;32(23):5189-5199.e6. doi: 10.1016/j.cub.2022.10.045. Epub 2022 Nov 15.

Authors

Affiliations

¹ Program in Genetics, University of Wisconsin, Madison, WI 53706, USA.
² Department of Biology, Regis University, 3333 Regis Boulevard, Denver, CO 80221, USA.
³ Institute for Biophysical Dynamics, University of Chicago, Chicago, IL 60637, USA.
⁴ University of Aberdeen, Institute of Medical Sciences, Aberdeen AB25 2ZD, UK.
⁵ Biophysics Program, University of Wisconsin, Madison, WI 53706, USA.
⁶ Department of Biomolecular Chemistry, University of Wisconsin, Madison, WI 53706, USA.
⁷ Department of Biology, Knox University, Galesburg, IL 61401, USA; Department of Biology, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA.
⁸ Department of Biology, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA.
⁹ Institute for Biophysical Dynamics, University of Chicago, Chicago, IL 60637, USA; Department of Physics, James Franck Institute and Pritzker School of Molecular Engineering, University of Chicago, Chicago, IL 60637, USA.
¹⁰ Program in Genetics, University of Wisconsin, Madison, WI 53706, USA; Biophysics Program, University of Wisconsin, Madison, WI 53706, USA; Department of Integrative Biology, University of Wisconsin, Madison, WI 53706, USA. Electronic address: jdhardin@wisc.edu.

Abstract

LIM-domain-containing repeat (LCR) proteins are recruited to strained actin filaments within stress fibers in cultured cells,¹^,²^,³ but their roles at cell-cell junctions in living organisms have not been extensively studied. Here, we show that the Caenorhabditis elegans LCR proteins TES-1/Tes and ZYX-1/Zyxin are recruited to apical junctions during embryonic elongation when junctions are under tension. In genetic backgrounds in which embryonic elongation fails, junctional recruitment is severely compromised. The two proteins display complementary patterns of expression: TES-1 is expressed in lateral (seam) epidermal cells, whereas ZYX-1 is expressed in dorsal and ventral epidermal cells. tes-1 and zyx-1 mutant embryos display junctional F-actin defects. The loss of either protein strongly enhances morphogenetic defects in hypomorphic mutant backgrounds for cadherin/catenin complex (CCC) components. The LCR regions of TES-1 and ZYX-1 are recruited to stress fiber strain sites (SFSSs) in cultured vertebrate cells. Together, these data establish TES-1 and ZYX-1 as components of a multicellular, tension-sensitive system that stabilizes the junctional actin cytoskeleton during embryonic morphogenesis.

Keywords: C. elegans; F-actin; LIM-domain-containing protein; Tes; cadherin; cell-cell adhesion; mechanobiology; morphogenesis; zyxin; α-catenin.

Publication types

Research Support, N.I.H., Extramural

MeSH terms

Actins* / genetics
Animals
Caenorhabditis elegans* / genetics

Substances

Actins

Abstract

Publication types

MeSH terms

Substances

Grants and funding