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

Alison Lynch; Yuyun Zhu; Bethany Lucas; Jonathan Winkelman; Keliya Bai; Sterling Martin; Samuel Block; Mark Slabodnick; Anjon Audhya; Bob Goldstein; Jonathan Pettitt; Margaret 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

Alison Lynch, Yuyun Zhu, Bethany Lucas, Jonathan Winkelman, Keliya Bai, Sterling Martin, Samuel Block, Mark Slabodnick, Anjon Audhya, Bob Goldstein, Jonathan Pettitt, Margaret Gardel, Jeff Hardin

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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 associated with stress fibers in cultured cells ^1-3, and are therefore promising candidates for mediating self-healing of actin networks at cell-cell junctions, but their roles in living organisms have not been extensively studied. Here, we establish roles for the Caenorhabditis elegans LCR proteins TES-1/Tes and ZYX- 1/Zyxin at apical junctions during epithelial morphogenesis. TES-1 and ZYX-1 are recruited to apical junctions during embryonic elongation, when junctions are under tension; in genetic backgrounds in which embryonic elongation fails, junctional recruitment of both proteins is severely compromised. The two proteins display complementary patterns of expression: TES-1 is expressed mainly 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, and loss of TES-1 strongly enhances tension-dependent injury of junctional actin networks in hypomorphic mutant backgrounds for cadherin/catenin complex components. Consistent with a role in stabilizing junctional actin networks during rapid cell shape change, the LCR regions of TES-1 and ZYX-1 are both 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

Original language	English
Pages (from-to)	5189-5199
Number of pages	10
Journal	Current Biology
Volume	32
Issue number	23
Early online date	15 Nov 2022
DOIs	https://doi.org/10.1016/j.cub.2022.10.045
Publication status	Published - 5 Dec 2022

Bibliographical note

Acknowledgments
cDNA clones for hmr-1, ajm-1, zyx-1, zoo-1, hmp-1, and tes-1 (yk collection) were provided by Yuji Kohara (National Institute of Genetics). A.M.L., Y.Z., B.G.L., S.C.T.M., and J.H. were supported by NIH grant R01GM058038 and NIH MIRA R35GM145312 awarded to J.H.; S.C.T.M. was supported by a Gilliam Fellowship from the Howard Hughes Medical Institute and by an Advanced Opportunities Fellowship and a COVID-19 dissertation completion fellowship from the University of Wisconsin-Madison; S.B. and A.A. were supported by NIH MIRA R35GM134865 awarded to A.A.; J.D.W. was supported by NIH grant F32GM122372 and by NIH grant R01GM104032 and the Army Research Office Multidisciplinary University Research Initiative W911NF1410403 awarded to M.L.G.; and B.G. and M.M.S. were supported by NIH MIRA R35GM134838 awarded to B.G. and NIH grant F32GM119348 awarded to M.M.S. Some strains were provided by the Caenorhabditis Genetics Center (CGC; https://cbs.umn.edu/cgc/home), which is funded by the NIH Office of Research Infrastructure Programs (P40 OD010440).

Data Availability Statement

All data reported in this paper will be shared by the lead contact upon request.
This paper does not report original code.
Any additional information required to reanalyze the data reported in this paper is available from the lead contact upon request.

Keywords

C elegans
morphogenesis
zyxin
Tes
LIM domain containing protein
Cell cell adhesion
cadherin
F-actin
α-catenin
mechanobiology

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Lynch_etal_CB_TES1_Tes_And_AAM
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Lynch, A., Zhu, Y., Lucas, B., Winkelman, J., Bai, K., Martin, S., Block, S., Slabodnick, M., Audhya, A., Goldstein, B., Pettitt, J., Gardel, M., & Hardin, J. (2022). TES-1/Tes and ZYX-1/Zyxin protect junctional actin networks under tension during epidermal morphogenesis in the C. elegans embryo. Current Biology, 32(23), 5189-5199. https://doi.org/10.1016/j.cub.2022.10.045

Lynch, A, Zhu, Y, Lucas, B, Winkelman, J, Bai, K, Martin, S, Block, S, Slabodnick, M, Audhya, A, Goldstein, B, Pettitt, J, Gardel, M & Hardin, J 2022, 'TES-1/Tes and ZYX-1/Zyxin protect junctional actin networks under tension during epidermal morphogenesis in the C. elegans embryo', Current Biology, vol. 32, no. 23, pp. 5189-5199. https://doi.org/10.1016/j.cub.2022.10.045

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

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 associated with stress fibers in cultured cells 1-3, and are therefore promising candidates for mediating self-healing of actin networks at cell-cell junctions, but their roles in living organisms have not been extensively studied. Here, we establish roles for the Caenorhabditis elegans LCR proteins TES-1/Tes and ZYX- 1/Zyxin at apical junctions during epithelial morphogenesis. TES-1 and ZYX-1 are recruited to apical junctions during embryonic elongation, when junctions are under tension; in genetic backgrounds in which embryonic elongation fails, junctional recruitment of both proteins is severely compromised. The two proteins display complementary patterns of expression: TES-1 is expressed mainly 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, and loss of TES-1 strongly enhances tension-dependent injury of junctional actin networks in hypomorphic mutant backgrounds for cadherin/catenin complex components. Consistent with a role in stabilizing junctional actin networks during rapid cell shape change, the LCR regions of TES-1 and ZYX-1 are both 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, morphogenesis, zyxin, Tes, LIM domain containing protein, Cell cell adhesion, cadherin, F-actin, α-catenin, mechanobiology",

author = "Alison Lynch and Yuyun Zhu and Bethany Lucas and Jonathan Winkelman and Keliya Bai and Sterling Martin and Samuel Block and Mark Slabodnick and Anjon Audhya and Bob Goldstein and Jonathan Pettitt and Margaret Gardel and Jeff Hardin",

note = "Acknowledgments cDNA clones for hmr-1, ajm-1, zyx-1, zoo-1, hmp-1, and tes-1 (yk collection) were provided by Yuji Kohara (National Institute of Genetics). A.M.L., Y.Z., B.G.L., S.C.T.M., and J.H. were supported by NIH grant R01GM058038 and NIH MIRA R35GM145312 awarded to J.H.; S.C.T.M. was supported by a Gilliam Fellowship from the Howard Hughes Medical Institute and by an Advanced Opportunities Fellowship and a COVID-19 dissertation completion fellowship from the University of Wisconsin-Madison; S.B. and A.A. were supported by NIH MIRA R35GM134865 awarded to A.A.; J.D.W. was supported by NIH grant F32GM122372 and by NIH grant R01GM104032 and the Army Research Office Multidisciplinary University Research Initiative W911NF1410403 awarded to M.L.G.; and B.G. and M.M.S. were supported by NIH MIRA R35GM134838 awarded to B.G. and NIH grant F32GM119348 awarded to M.M.S. Some strains were provided by the Caenorhabditis Genetics Center (CGC; https://cbs.umn.edu/cgc/home), which is funded by the NIH Office of Research Infrastructure Programs (P40 OD010440).",

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T1 - TES-1/Tes and ZYX-1/Zyxin protect junctional actin networks under tension during epidermal morphogenesis in the C. elegans embryo

AU - Lynch, Alison

AU - Zhu, Yuyun

AU - Lucas, Bethany

AU - Winkelman, Jonathan

AU - Bai, Keliya

AU - Martin, Sterling

AU - Block, Samuel

AU - Slabodnick, Mark

AU - Audhya, Anjon

AU - Goldstein, Bob

AU - Pettitt, Jonathan

AU - Gardel, Margaret

AU - Hardin, Jeff

N1 - Acknowledgments cDNA clones for hmr-1, ajm-1, zyx-1, zoo-1, hmp-1, and tes-1 (yk collection) were provided by Yuji Kohara (National Institute of Genetics). A.M.L., Y.Z., B.G.L., S.C.T.M., and J.H. were supported by NIH grant R01GM058038 and NIH MIRA R35GM145312 awarded to J.H.; S.C.T.M. was supported by a Gilliam Fellowship from the Howard Hughes Medical Institute and by an Advanced Opportunities Fellowship and a COVID-19 dissertation completion fellowship from the University of Wisconsin-Madison; S.B. and A.A. were supported by NIH MIRA R35GM134865 awarded to A.A.; J.D.W. was supported by NIH grant F32GM122372 and by NIH grant R01GM104032 and the Army Research Office Multidisciplinary University Research Initiative W911NF1410403 awarded to M.L.G.; and B.G. and M.M.S. were supported by NIH MIRA R35GM134838 awarded to B.G. and NIH grant F32GM119348 awarded to M.M.S. Some strains were provided by the Caenorhabditis Genetics Center (CGC; https://cbs.umn.edu/cgc/home), which is funded by the NIH Office of Research Infrastructure Programs (P40 OD010440).

PY - 2022/12/5

Y1 - 2022/12/5

N2 - 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 associated with stress fibers in cultured cells 1-3, and are therefore promising candidates for mediating self-healing of actin networks at cell-cell junctions, but their roles in living organisms have not been extensively studied. Here, we establish roles for the Caenorhabditis elegans LCR proteins TES-1/Tes and ZYX- 1/Zyxin at apical junctions during epithelial morphogenesis. TES-1 and ZYX-1 are recruited to apical junctions during embryonic elongation, when junctions are under tension; in genetic backgrounds in which embryonic elongation fails, junctional recruitment of both proteins is severely compromised. The two proteins display complementary patterns of expression: TES-1 is expressed mainly 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, and loss of TES-1 strongly enhances tension-dependent injury of junctional actin networks in hypomorphic mutant backgrounds for cadherin/catenin complex components. Consistent with a role in stabilizing junctional actin networks during rapid cell shape change, the LCR regions of TES-1 and ZYX-1 are both 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

AB - 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 associated with stress fibers in cultured cells 1-3, and are therefore promising candidates for mediating self-healing of actin networks at cell-cell junctions, but their roles in living organisms have not been extensively studied. Here, we establish roles for the Caenorhabditis elegans LCR proteins TES-1/Tes and ZYX- 1/Zyxin at apical junctions during epithelial morphogenesis. TES-1 and ZYX-1 are recruited to apical junctions during embryonic elongation, when junctions are under tension; in genetic backgrounds in which embryonic elongation fails, junctional recruitment of both proteins is severely compromised. The two proteins display complementary patterns of expression: TES-1 is expressed mainly 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, and loss of TES-1 strongly enhances tension-dependent injury of junctional actin networks in hypomorphic mutant backgrounds for cadherin/catenin complex components. Consistent with a role in stabilizing junctional actin networks during rapid cell shape change, the LCR regions of TES-1 and ZYX-1 are both 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

KW - C elegans

KW - morphogenesis

KW - zyxin

KW - Tes

KW - LIM domain containing protein

KW - Cell cell adhesion

KW - cadherin

KW - F-actin

KW - α-catenin

KW - mechanobiology

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DO - 10.1016/j.cub.2022.10.045

M3 - Article

SN - 0960-9822

VL - 32

SP - 5189

EP - 5199

JO - Current Biology

JF - Current Biology

IS - 23

ER -

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

Abstract

Bibliographical note

Data Availability Statement

Keywords

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