Embryogenesis requires cells to change shape and move without disrupting epithelial integrity. This requires robust, responsive linkage between adherens junctions and the actomyosin cytoskeleton. Using Drosophila morphogenesis, we define molecular mechanisms mediating junction–cytoskeletal linkage and explore the role of mechanosensing. We focus on the junction–cytoskeletal linker Canoe, a multidomain protein. We engineered the canoe locus to define how its domains mediate its mechanism of action. To our surprise, the PDZ and FAB domains, which we thought connected junctions and F-actin, are not required for viability or mechanosensitive recruitment to junctions under tension. The FAB domain stabilizes junctions experiencing elevated force, but in its absence, most cells recover, suggesting redundant interactions. In contrast, the Rap1-binding RA domains are critical for all Cno functions and enrichment at junctions under tension. This supports a model in which junctional robustness derives from a large protein network assembled via multivalent interactions, with proteins at network nodes and some node connections more critical than others.
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6 December 2021
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November 11 2021
Multivalent interactions make adherens junction–cytoskeletal linkage robust during morphogenesis
Kia Z. Perez-Vale
,
Kia Z. Perez-Vale
1
Curriculum in Genetics and Molecular Biology, University of North Carolina at Chapel Hill, Chapel Hill, NC
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Kristi D. Yow
,
Kristi D. Yow
2
Department of Biology, University of North Carolina at Chapel Hill, Chapel Hill, NC
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Ruth I. Johnson
,
Ruth I. Johnson
3
Department of Biology, Wesleyan University, Middletown, CT
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Amy E. Byrnes
,
Amy E. Byrnes
4
Program in Molecular and Cellular Biophysics, University of North Carolina at Chapel Hill, Chapel Hill, NC
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Tara M. Finegan
,
Tara M. Finegan
5
Department of Physics and BioInspired Syracuse, Syracuse University, Syracuse, NY
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Kevin C. Slep
,
Kevin C. Slep
2
Department of Biology, University of North Carolina at Chapel Hill, Chapel Hill, NC
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Mark Peifer
1
Curriculum in Genetics and Molecular Biology, University of North Carolina at Chapel Hill, Chapel Hill, NC
2
Department of Biology, University of North Carolina at Chapel Hill, Chapel Hill, NC
6
Lineberger Comprehensive Cancer Center, University of North Carolina at Chapel Hill, Chapel Hill, NC
Correspondence to Mark Peifer: peifer@unc.edu
Search for other works by this author on:
Kia Z. Perez-Vale
1
Curriculum in Genetics and Molecular Biology, University of North Carolina at Chapel Hill, Chapel Hill, NC
Kristi D. Yow
2
Department of Biology, University of North Carolina at Chapel Hill, Chapel Hill, NC
Ruth I. Johnson
3
Department of Biology, Wesleyan University, Middletown, CT
Amy E. Byrnes
4
Program in Molecular and Cellular Biophysics, University of North Carolina at Chapel Hill, Chapel Hill, NC
Tara M. Finegan
5
Department of Physics and BioInspired Syracuse, Syracuse University, Syracuse, NY
Kevin C. Slep
2
Department of Biology, University of North Carolina at Chapel Hill, Chapel Hill, NC
1
Curriculum in Genetics and Molecular Biology, University of North Carolina at Chapel Hill, Chapel Hill, NC
2
Department of Biology, University of North Carolina at Chapel Hill, Chapel Hill, NC
6
Lineberger Comprehensive Cancer Center, University of North Carolina at Chapel Hill, Chapel Hill, NC
Correspondence to Mark Peifer: peifer@unc.edu
Received:
April 19 2021
Revision Received:
September 15 2021
Accepted:
October 04 2021
Online Issn: 1540-8140
Print Issn: 0021-9525
Funding
Funder(s):
National Institutes of Health
- Award Id(s): R35 GM118096
Funder(s):
National Institutes of Health
- Award Id(s): GM008570
Funder(s):
National Institutes of Health
- Award Id(s): F31 GM131521,T32 GM007092
Funder(s):
Burroughs Wellcome Fund
© 2021 Perez-Vale et al.
2021
This article is distributed under the terms of an Attribution–Noncommercial–Share Alike–No Mirror Sites license for the first six months after the publication date (see http://www.rupress.org/terms/). After six months it is available under a Creative Commons License (Attribution–Noncommercial–Share Alike 4.0 International license, as described at https://creativecommons.org/licenses/by-nc-sa/4.0/).
J Cell Biol (2021) 220 (12): e202104087.
Article history
Received:
April 19 2021
Revision Received:
September 15 2021
Accepted:
October 04 2021
Citation
Kia Z. Perez-Vale, Kristi D. Yow, Ruth I. Johnson, Amy E. Byrnes, Tara M. Finegan, Kevin C. Slep, Mark Peifer; Multivalent interactions make adherens junction–cytoskeletal linkage robust during morphogenesis. J Cell Biol 6 December 2021; 220 (12): e202104087. doi: https://doi.org/10.1083/jcb.202104087
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