Intracellular signalling and intercellular coupling coordinate heterogeneous contractile events to facilitate tissue folding
Cellular forces generated in the apical domain of epithelial cells reshape tissues. Recent studies highlighted an important role for dynamic actomyosin contractions, called pulses, that change cell and tissue shape. Net cell shape change depends on whether cell shape is stabilized, or ratcheted, bet...
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| Format: | Article |
| Language: | en_US |
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Nature Publishing Group
2015
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| Online Access: | http://hdl.handle.net/1721.1/98473 https://orcid.org/0000-0001-8060-2607 https://orcid.org/0000-0002-3283-3248 |
| _version_ | 1826212246174302208 |
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| author | Xie, Shicong Martin, Adam C |
| author2 | Massachusetts Institute of Technology. Computational and Systems Biology Program |
| author_facet | Massachusetts Institute of Technology. Computational and Systems Biology Program Xie, Shicong Martin, Adam C |
| author_sort | Xie, Shicong |
| collection | MIT |
| description | Cellular forces generated in the apical domain of epithelial cells reshape tissues. Recent studies highlighted an important role for dynamic actomyosin contractions, called pulses, that change cell and tissue shape. Net cell shape change depends on whether cell shape is stabilized, or ratcheted, between pulses. Whether there are different classes of contractile pulses in wild-type embryos and how pulses are spatiotemporally coordinated is unknown. Here we develop a computational framework to identify and classify pulses and determine how pulses are coordinated during invagination of the Drosophila ventral furrow. We demonstrate biased transitions in pulse behaviour, where weak or unratcheted pulses transition to ratcheted pulses. The transcription factor Twist directs this transition, with cells in Twist-depleted embryos exhibiting abnormal reversed transitions in pulse behaviour. We demonstrate that ratcheted pulses have higher probability of having neighbouring contractions, and that ratcheting of pulses prevents competition between neighbouring contractions, allowing collective behaviour. |
| first_indexed | 2024-09-23T15:18:39Z |
| format | Article |
| id | mit-1721.1/98473 |
| institution | Massachusetts Institute of Technology |
| language | en_US |
| last_indexed | 2024-09-23T15:18:39Z |
| publishDate | 2015 |
| publisher | Nature Publishing Group |
| record_format | dspace |
| spelling | mit-1721.1/984732022-10-02T02:03:43Z Intracellular signalling and intercellular coupling coordinate heterogeneous contractile events to facilitate tissue folding Xie, Shicong Martin, Adam C Massachusetts Institute of Technology. Computational and Systems Biology Program Massachusetts Institute of Technology. Department of Biology Xie, Shicong Martin, Adam C. Cellular forces generated in the apical domain of epithelial cells reshape tissues. Recent studies highlighted an important role for dynamic actomyosin contractions, called pulses, that change cell and tissue shape. Net cell shape change depends on whether cell shape is stabilized, or ratcheted, between pulses. Whether there are different classes of contractile pulses in wild-type embryos and how pulses are spatiotemporally coordinated is unknown. Here we develop a computational framework to identify and classify pulses and determine how pulses are coordinated during invagination of the Drosophila ventral furrow. We demonstrate biased transitions in pulse behaviour, where weak or unratcheted pulses transition to ratcheted pulses. The transcription factor Twist directs this transition, with cells in Twist-depleted embryos exhibiting abnormal reversed transitions in pulse behaviour. We demonstrate that ratcheted pulses have higher probability of having neighbouring contractions, and that ratcheting of pulses prevents competition between neighbouring contractions, allowing collective behaviour. National Institute of General Medical Sciences (U.S.) (Grant R00GM089826) National Institute of General Medical Sciences (U.S.) (Grant R01GM105984) 2015-09-14T13:06:37Z 2015-09-14T13:06:37Z 2015-05 2014-11 Article http://purl.org/eprint/type/JournalArticle 2041-1723 http://hdl.handle.net/1721.1/98473 Xie, Shicong, and Adam C. Martin. “Intracellular Signalling and Intercellular Coupling Coordinate Heterogeneous Contractile Events to Facilitate Tissue Folding.” Nat Comms 6 (May 26, 2015): 7161. © 2015 Macmillan Publishers Limited https://orcid.org/0000-0001-8060-2607 https://orcid.org/0000-0002-3283-3248 en_US http://dx.doi.org/10.1038/ncomms8161 Nature Communications Creative Commons Attribution http://creativecommons.org/licenses/by/4.0/ application/pdf Nature Publishing Group Nature Publishing Group |
| spellingShingle | Xie, Shicong Martin, Adam C Intracellular signalling and intercellular coupling coordinate heterogeneous contractile events to facilitate tissue folding |
| title | Intracellular signalling and intercellular coupling coordinate heterogeneous contractile events to facilitate tissue folding |
| title_full | Intracellular signalling and intercellular coupling coordinate heterogeneous contractile events to facilitate tissue folding |
| title_fullStr | Intracellular signalling and intercellular coupling coordinate heterogeneous contractile events to facilitate tissue folding |
| title_full_unstemmed | Intracellular signalling and intercellular coupling coordinate heterogeneous contractile events to facilitate tissue folding |
| title_short | Intracellular signalling and intercellular coupling coordinate heterogeneous contractile events to facilitate tissue folding |
| title_sort | intracellular signalling and intercellular coupling coordinate heterogeneous contractile events to facilitate tissue folding |
| url | http://hdl.handle.net/1721.1/98473 https://orcid.org/0000-0001-8060-2607 https://orcid.org/0000-0002-3283-3248 |
| work_keys_str_mv | AT xieshicong intracellularsignallingandintercellularcouplingcoordinateheterogeneouscontractileeventstofacilitatetissuefolding AT martinadamc intracellularsignallingandintercellularcouplingcoordinateheterogeneouscontractileeventstofacilitatetissuefolding |