Volume conservation principle involved in cell lengthening and nucleus movement during tissue morphogenesis
Tissue morphogenesis is the process in which coordinated movements and shape changes of large numbers of cells form tissues, organs, and the internal body structure. Understanding morphogenetic movements requires precise measurements of whole-cell shape changes over time. Tissue folding and invagina...
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National Academy of Sciences
2013
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| Online Access: | http://hdl.handle.net/1721.1/79590 https://orcid.org/0000-0001-8060-2607 |
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| author | Gelbart, Michael A. He, Bing Thiberge, Stephan Y. Wieschaus, Eric F. Kaschube, Matthias Martin, Adam C |
| author2 | Massachusetts Institute of Technology. Department of Biology |
| author_facet | Massachusetts Institute of Technology. Department of Biology Gelbart, Michael A. He, Bing Thiberge, Stephan Y. Wieschaus, Eric F. Kaschube, Matthias Martin, Adam C |
| author_sort | Gelbart, Michael A. |
| collection | MIT |
| description | Tissue morphogenesis is the process in which coordinated movements and shape changes of large numbers of cells form tissues, organs, and the internal body structure. Understanding morphogenetic movements requires precise measurements of whole-cell shape changes over time. Tissue folding and invagination are thought to be facilitated by apical constriction, but the mechanism by which changes near the apical cell surface affect changes along the entire apical–basal axis of the cell remains elusive. Here, we developed Embryo Development Geometry Explorer, an approach for quantifying rapid whole-cell shape changes over time, and we combined it with deep-tissue time-lapse imaging based on fast two-photon microscopy to study Drosophila ventral furrow formation. We found that both the cell lengthening along the apical–basal axis and the movement of the nucleus to the basal side proceeded stepwise and were correlated with apical constriction. Moreover, cell volume lost apically due to constriction largely balanced the volume gained basally by cell lengthening. The volume above the nucleus was conserved during its basal movement. Both apical volume loss and cell lengthening were absent in mutants showing deficits in the contractile cytoskeleton underlying apical constriction. We conclude that a single mechanical mechanism involving volume conservation and apical constriction-induced basal movement of cytoplasm accounts quantitatively for the cell shape changes and the nucleus movement in Drosophila ventral furrow formation. Our study provides a comprehensive quantitative analysis of the fast dynamics of whole-cell shape changes during tissue folding and points to a simplified model for Drosophila gastrulation. |
| first_indexed | 2024-09-23T16:37:38Z |
| format | Article |
| id | mit-1721.1/79590 |
| institution | Massachusetts Institute of Technology |
| language | en_US |
| last_indexed | 2024-09-23T16:37:38Z |
| publishDate | 2013 |
| publisher | National Academy of Sciences |
| record_format | dspace |
| spelling | mit-1721.1/795902022-09-29T20:24:49Z Volume conservation principle involved in cell lengthening and nucleus movement during tissue morphogenesis Gelbart, Michael A. He, Bing Thiberge, Stephan Y. Wieschaus, Eric F. Kaschube, Matthias Martin, Adam C Massachusetts Institute of Technology. Department of Biology Martin, Adam C. Tissue morphogenesis is the process in which coordinated movements and shape changes of large numbers of cells form tissues, organs, and the internal body structure. Understanding morphogenetic movements requires precise measurements of whole-cell shape changes over time. Tissue folding and invagination are thought to be facilitated by apical constriction, but the mechanism by which changes near the apical cell surface affect changes along the entire apical–basal axis of the cell remains elusive. Here, we developed Embryo Development Geometry Explorer, an approach for quantifying rapid whole-cell shape changes over time, and we combined it with deep-tissue time-lapse imaging based on fast two-photon microscopy to study Drosophila ventral furrow formation. We found that both the cell lengthening along the apical–basal axis and the movement of the nucleus to the basal side proceeded stepwise and were correlated with apical constriction. Moreover, cell volume lost apically due to constriction largely balanced the volume gained basally by cell lengthening. The volume above the nucleus was conserved during its basal movement. Both apical volume loss and cell lengthening were absent in mutants showing deficits in the contractile cytoskeleton underlying apical constriction. We conclude that a single mechanical mechanism involving volume conservation and apical constriction-induced basal movement of cytoplasm accounts quantitatively for the cell shape changes and the nucleus movement in Drosophila ventral furrow formation. Our study provides a comprehensive quantitative analysis of the fast dynamics of whole-cell shape changes during tissue folding and points to a simplified model for Drosophila gastrulation. 2013-07-12T14:55:20Z 2013-07-12T14:55:20Z 2012-11 2012-03 Article http://purl.org/eprint/type/JournalArticle 0027-8424 1091-6490 http://hdl.handle.net/1721.1/79590 Gelbart, M. A., B. He, A. C. Martin, S. Y. Thiberge, E. F. Wieschaus, and M. Kaschube. Volume Conservation Principle Involved in Cell Lengthening and Nucleus Movement During Tissue Morphogenesis. Proceedings of the National Academy of Sciences 109, no. 47 (November 20, 2012): 19298-19303. https://orcid.org/0000-0001-8060-2607 en_US http://dx.doi.org/10.1073/pnas.1205258109 Proceedings of the National Academy of Sciences Article is made available in accordance with the publisher's policy and may be subject to US copyright law. Please refer to the publisher's site for terms of use. application/pdf National Academy of Sciences PNAS |
| spellingShingle | Gelbart, Michael A. He, Bing Thiberge, Stephan Y. Wieschaus, Eric F. Kaschube, Matthias Martin, Adam C Volume conservation principle involved in cell lengthening and nucleus movement during tissue morphogenesis |
| title | Volume conservation principle involved in cell lengthening and nucleus movement during tissue morphogenesis |
| title_full | Volume conservation principle involved in cell lengthening and nucleus movement during tissue morphogenesis |
| title_fullStr | Volume conservation principle involved in cell lengthening and nucleus movement during tissue morphogenesis |
| title_full_unstemmed | Volume conservation principle involved in cell lengthening and nucleus movement during tissue morphogenesis |
| title_short | Volume conservation principle involved in cell lengthening and nucleus movement during tissue morphogenesis |
| title_sort | volume conservation principle involved in cell lengthening and nucleus movement during tissue morphogenesis |
| url | http://hdl.handle.net/1721.1/79590 https://orcid.org/0000-0001-8060-2607 |
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