Optogenetic inhibition of actomyosin reveals mechanical bistability of the mesoderm epithelium during Drosophila mesoderm invagination
Apical constriction driven by actin and non-muscle myosin II (actomyosin) provides a well-conserved mechanism to mediate epithelial folding. It remains unclear how contractile forces near the apical surface of a cell sheet drive out-of-the-plane bending of the sheet and whether myosin contractility...
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2022-02-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/69082 |
| _version_ | 1828195314683609088 |
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| author | Hanqing Guo Michael Swan Bing He |
| author_facet | Hanqing Guo Michael Swan Bing He |
| author_sort | Hanqing Guo |
| collection | DOAJ |
| description | Apical constriction driven by actin and non-muscle myosin II (actomyosin) provides a well-conserved mechanism to mediate epithelial folding. It remains unclear how contractile forces near the apical surface of a cell sheet drive out-of-the-plane bending of the sheet and whether myosin contractility is required throughout folding. By optogenetic-mediated acute inhibition of actomyosin, we find that during Drosophila mesoderm invagination, actomyosin contractility is critical to prevent tissue relaxation during the early, ‘priming’ stage of folding but is dispensable for the actual folding step after the tissue passes through a stereotyped transitional configuration. This binary response suggests that Drosophila mesoderm is mechanically bistable during gastrulation. Computer modeling analysis demonstrates that the binary tissue response to actomyosin inhibition can be recapitulated in the simulated epithelium that undergoes buckling-like deformation jointly mediated by apical constriction in the mesoderm and in-plane compression generated by apicobasal shrinkage of the surrounding ectoderm. Interestingly, comparison between wild-type and snail mutants that fail to specify the mesoderm demonstrates that the lateral ectoderm undergoes apicobasal shrinkage during gastrulation independently of mesoderm invagination. We propose that Drosophila mesoderm invagination is achieved through an interplay between local apical constriction and mechanical bistability of the epithelium that facilitates epithelial buckling. |
| first_indexed | 2024-04-12T09:41:33Z |
| format | Article |
| id | doaj.art-db2f4de4dda24dc2be41831b4901b18e |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-12T09:41:33Z |
| publishDate | 2022-02-01 |
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| series | eLife |
| spelling | doaj.art-db2f4de4dda24dc2be41831b4901b18e2022-12-22T03:38:04ZengeLife Sciences Publications LtdeLife2050-084X2022-02-011110.7554/eLife.69082Optogenetic inhibition of actomyosin reveals mechanical bistability of the mesoderm epithelium during Drosophila mesoderm invaginationHanqing Guo0https://orcid.org/0000-0001-8722-6253Michael Swan1Bing He2https://orcid.org/0000-0002-8564-0933Department of Biological Sciences, Dartmouth College, Hanover, United StatesDepartment of Molecular Biology, Princeton University, Princeton, United StatesDepartment of Biological Sciences, Dartmouth College, Hanover, United StatesApical constriction driven by actin and non-muscle myosin II (actomyosin) provides a well-conserved mechanism to mediate epithelial folding. It remains unclear how contractile forces near the apical surface of a cell sheet drive out-of-the-plane bending of the sheet and whether myosin contractility is required throughout folding. By optogenetic-mediated acute inhibition of actomyosin, we find that during Drosophila mesoderm invagination, actomyosin contractility is critical to prevent tissue relaxation during the early, ‘priming’ stage of folding but is dispensable for the actual folding step after the tissue passes through a stereotyped transitional configuration. This binary response suggests that Drosophila mesoderm is mechanically bistable during gastrulation. Computer modeling analysis demonstrates that the binary tissue response to actomyosin inhibition can be recapitulated in the simulated epithelium that undergoes buckling-like deformation jointly mediated by apical constriction in the mesoderm and in-plane compression generated by apicobasal shrinkage of the surrounding ectoderm. Interestingly, comparison between wild-type and snail mutants that fail to specify the mesoderm demonstrates that the lateral ectoderm undergoes apicobasal shrinkage during gastrulation independently of mesoderm invagination. We propose that Drosophila mesoderm invagination is achieved through an interplay between local apical constriction and mechanical bistability of the epithelium that facilitates epithelial buckling.https://elifesciences.org/articles/69082epithelial foldinggastrulationventral furrowapical constrictionmechanical bistabilitycompression |
| spellingShingle | Hanqing Guo Michael Swan Bing He Optogenetic inhibition of actomyosin reveals mechanical bistability of the mesoderm epithelium during Drosophila mesoderm invagination eLife epithelial folding gastrulation ventral furrow apical constriction mechanical bistability compression |
| title | Optogenetic inhibition of actomyosin reveals mechanical bistability of the mesoderm epithelium during Drosophila mesoderm invagination |
| title_full | Optogenetic inhibition of actomyosin reveals mechanical bistability of the mesoderm epithelium during Drosophila mesoderm invagination |
| title_fullStr | Optogenetic inhibition of actomyosin reveals mechanical bistability of the mesoderm epithelium during Drosophila mesoderm invagination |
| title_full_unstemmed | Optogenetic inhibition of actomyosin reveals mechanical bistability of the mesoderm epithelium during Drosophila mesoderm invagination |
| title_short | Optogenetic inhibition of actomyosin reveals mechanical bistability of the mesoderm epithelium during Drosophila mesoderm invagination |
| title_sort | optogenetic inhibition of actomyosin reveals mechanical bistability of the mesoderm epithelium during drosophila mesoderm invagination |
| topic | epithelial folding gastrulation ventral furrow apical constriction mechanical bistability compression |
| url | https://elifesciences.org/articles/69082 |
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