Mechanical heterogeneity along single cell-cell junctions is driven by lateral clustering of cadherins during vertebrate axis elongation
Morphogenesis is governed by the interplay of molecular signals and mechanical forces across multiple length scales. The last decade has seen tremendous advances in our understanding of the dynamics of protein localization and turnover at subcellular length scales, and at the other end of the spectr...
| Main Authors: | , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
eLife Sciences Publications Ltd
2021-05-01
|
| Series: | eLife |
| Subjects: | |
| Online Access: | https://elifesciences.org/articles/65390 |
| _version_ | 1818018176765526016 |
|---|---|
| author | Robert J Huebner Abdul Naseer Malmi-Kakkada Sena Sarıkaya Shinuo Weng D Thirumalai John B Wallingford |
| author_facet | Robert J Huebner Abdul Naseer Malmi-Kakkada Sena Sarıkaya Shinuo Weng D Thirumalai John B Wallingford |
| author_sort | Robert J Huebner |
| collection | DOAJ |
| description | Morphogenesis is governed by the interplay of molecular signals and mechanical forces across multiple length scales. The last decade has seen tremendous advances in our understanding of the dynamics of protein localization and turnover at subcellular length scales, and at the other end of the spectrum, of mechanics at tissue-level length scales. Integrating the two remains a challenge, however, because we lack a detailed understanding of the subcellular patterns of mechanical properties of cells within tissues. Here, in the context of the elongating body axis of Xenopus embryos, we combine tools from cell biology and physics to demonstrate that individual cell-cell junctions display finely-patterned local mechanical heterogeneity along their length. We show that such local mechanical patterning is essential for the cell movements of convergent extension and is imparted by locally patterned clustering of a classical cadherin. Finally, the patterning of cadherins and thus local mechanics along cell-cell junctions are controlled by Planar Cell Polarity signaling, a key genetic module for CE that is mutated in diverse human birth defects. |
| first_indexed | 2024-04-14T07:35:47Z |
| format | Article |
| id | doaj.art-47545ae2776d49158e731d02407c7e69 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-14T07:35:47Z |
| publishDate | 2021-05-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-47545ae2776d49158e731d02407c7e692022-12-22T02:05:41ZengeLife Sciences Publications LtdeLife2050-084X2021-05-011010.7554/eLife.65390Mechanical heterogeneity along single cell-cell junctions is driven by lateral clustering of cadherins during vertebrate axis elongationRobert J Huebner0https://orcid.org/0000-0001-8778-9689Abdul Naseer Malmi-Kakkada1https://orcid.org/0000-0002-5429-4652Sena Sarıkaya2https://orcid.org/0000-0001-5008-2065Shinuo Weng3https://orcid.org/0000-0001-7932-913XD Thirumalai4https://orcid.org/0000-0003-1801-5924John B Wallingford5https://orcid.org/0000-0002-6280-8625Department of Molecular Biosciences, University of Texas, Austin, United StatesDepartment of Chemistry, University of Texas, Austin, United States; Department of Chemistry and Physics, Augusta University, Augusta, GeorgiaDepartment of Molecular Biosciences, University of Texas, Austin, United StatesDepartment of Molecular Biosciences, University of Texas, Austin, United StatesDepartment of Chemistry, University of Texas, Austin, United StatesDepartment of Molecular Biosciences, University of Texas, Austin, United StatesMorphogenesis is governed by the interplay of molecular signals and mechanical forces across multiple length scales. The last decade has seen tremendous advances in our understanding of the dynamics of protein localization and turnover at subcellular length scales, and at the other end of the spectrum, of mechanics at tissue-level length scales. Integrating the two remains a challenge, however, because we lack a detailed understanding of the subcellular patterns of mechanical properties of cells within tissues. Here, in the context of the elongating body axis of Xenopus embryos, we combine tools from cell biology and physics to demonstrate that individual cell-cell junctions display finely-patterned local mechanical heterogeneity along their length. We show that such local mechanical patterning is essential for the cell movements of convergent extension and is imparted by locally patterned clustering of a classical cadherin. Finally, the patterning of cadherins and thus local mechanics along cell-cell junctions are controlled by Planar Cell Polarity signaling, a key genetic module for CE that is mutated in diverse human birth defects.https://elifesciences.org/articles/65390cadherinheterogeneityaxis elongationplanar cell polarity |
| spellingShingle | Robert J Huebner Abdul Naseer Malmi-Kakkada Sena Sarıkaya Shinuo Weng D Thirumalai John B Wallingford Mechanical heterogeneity along single cell-cell junctions is driven by lateral clustering of cadherins during vertebrate axis elongation eLife cadherin heterogeneity axis elongation planar cell polarity |
| title | Mechanical heterogeneity along single cell-cell junctions is driven by lateral clustering of cadherins during vertebrate axis elongation |
| title_full | Mechanical heterogeneity along single cell-cell junctions is driven by lateral clustering of cadherins during vertebrate axis elongation |
| title_fullStr | Mechanical heterogeneity along single cell-cell junctions is driven by lateral clustering of cadherins during vertebrate axis elongation |
| title_full_unstemmed | Mechanical heterogeneity along single cell-cell junctions is driven by lateral clustering of cadherins during vertebrate axis elongation |
| title_short | Mechanical heterogeneity along single cell-cell junctions is driven by lateral clustering of cadherins during vertebrate axis elongation |
| title_sort | mechanical heterogeneity along single cell cell junctions is driven by lateral clustering of cadherins during vertebrate axis elongation |
| topic | cadherin heterogeneity axis elongation planar cell polarity |
| url | https://elifesciences.org/articles/65390 |
| work_keys_str_mv | AT robertjhuebner mechanicalheterogeneityalongsinglecellcelljunctionsisdrivenbylateralclusteringofcadherinsduringvertebrateaxiselongation AT abdulnaseermalmikakkada mechanicalheterogeneityalongsinglecellcelljunctionsisdrivenbylateralclusteringofcadherinsduringvertebrateaxiselongation AT senasarıkaya mechanicalheterogeneityalongsinglecellcelljunctionsisdrivenbylateralclusteringofcadherinsduringvertebrateaxiselongation AT shinuoweng mechanicalheterogeneityalongsinglecellcelljunctionsisdrivenbylateralclusteringofcadherinsduringvertebrateaxiselongation AT dthirumalai mechanicalheterogeneityalongsinglecellcelljunctionsisdrivenbylateralclusteringofcadherinsduringvertebrateaxiselongation AT johnbwallingford mechanicalheterogeneityalongsinglecellcelljunctionsisdrivenbylateralclusteringofcadherinsduringvertebrateaxiselongation |