Chiral cell sliding drives left-right asymmetric organ twisting
Polarized epithelial morphogenesis is an essential process in animal development. While this process is mostly attributed to directional cell intercalation, it can also be induced by other mechanisms. Using live-imaging analysis and a three-dimensional vertex model, we identified ‘cell sliding,’ a n...
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2018-06-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/32506 |
| _version_ | 1811252993724514304 |
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| author | Mikiko Inaki Ryo Hatori Naotaka Nakazawa Takashi Okumura Tomoki Ishibashi Junichi Kikuta Masaru Ishii Kenji Matsuno Hisao Honda |
| author_facet | Mikiko Inaki Ryo Hatori Naotaka Nakazawa Takashi Okumura Tomoki Ishibashi Junichi Kikuta Masaru Ishii Kenji Matsuno Hisao Honda |
| author_sort | Mikiko Inaki |
| collection | DOAJ |
| description | Polarized epithelial morphogenesis is an essential process in animal development. While this process is mostly attributed to directional cell intercalation, it can also be induced by other mechanisms. Using live-imaging analysis and a three-dimensional vertex model, we identified ‘cell sliding,’ a novel mechanism driving epithelial morphogenesis, in which cells directionally change their position relative to their subjacent (posterior) neighbors by sliding in one direction. In Drosophila embryonic hindgut, an initial left-right (LR) asymmetry of the cell shape (cell chirality in three dimensions), which occurs intrinsically before tissue deformation, is converted through LR asymmetric cell sliding into a directional axial twisting of the epithelial tube. In a Drosophila inversion mutant showing inverted cell chirality and hindgut rotation, cell sliding occurs in the opposite direction to that in wild-type. Unlike directional cell intercalation, cell sliding does not require junctional remodeling. Cell sliding may also be involved in other cases of LR-polarized epithelial morphogenesis. |
| first_indexed | 2024-04-12T16:43:03Z |
| format | Article |
| id | doaj.art-2c2433d324fb4edca16a6de7529ca89c |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-12T16:43:03Z |
| publishDate | 2018-06-01 |
| publisher | eLife Sciences Publications Ltd |
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| spelling | doaj.art-2c2433d324fb4edca16a6de7529ca89c2022-12-22T03:24:41ZengeLife Sciences Publications LtdeLife2050-084X2018-06-01710.7554/eLife.32506Chiral cell sliding drives left-right asymmetric organ twistingMikiko Inaki0Ryo Hatori1Naotaka Nakazawa2Takashi Okumura3Tomoki Ishibashi4Junichi Kikuta5Masaru Ishii6Kenji Matsuno7https://orcid.org/0000-0001-6140-8833Hisao Honda8Department of Biological Sciences, Graduate School of Science, Osaka University, Toyonaka, JapanDepartment of Biological Sciences, Graduate School of Science, Osaka University, Toyonaka, JapanDepartment of Biological Sciences, Graduate School of Science, Osaka University, Toyonaka, JapanDepartment of Biological Sciences, Graduate School of Science, Osaka University, Toyonaka, JapanDepartment of Biological Sciences, Graduate School of Science, Osaka University, Toyonaka, JapanDepartment of Immunology and Cell Biology, Graduate School of Medicine, Osaka University, Suita, JapanDepartment of Immunology and Cell Biology, Graduate School of Medicine, Osaka University, Suita, JapanDepartment of Biological Sciences, Graduate School of Science, Osaka University, Toyonaka, JapanDepartment of Physiology and Cell Biology, Graduate School of Medicine, Kobe University, Kobe, JapanPolarized epithelial morphogenesis is an essential process in animal development. While this process is mostly attributed to directional cell intercalation, it can also be induced by other mechanisms. Using live-imaging analysis and a three-dimensional vertex model, we identified ‘cell sliding,’ a novel mechanism driving epithelial morphogenesis, in which cells directionally change their position relative to their subjacent (posterior) neighbors by sliding in one direction. In Drosophila embryonic hindgut, an initial left-right (LR) asymmetry of the cell shape (cell chirality in three dimensions), which occurs intrinsically before tissue deformation, is converted through LR asymmetric cell sliding into a directional axial twisting of the epithelial tube. In a Drosophila inversion mutant showing inverted cell chirality and hindgut rotation, cell sliding occurs in the opposite direction to that in wild-type. Unlike directional cell intercalation, cell sliding does not require junctional remodeling. Cell sliding may also be involved in other cases of LR-polarized epithelial morphogenesis.https://elifesciences.org/articles/32506Left-right asymmetryCell chiralityCell slidingEpithelial morphogenesis |
| spellingShingle | Mikiko Inaki Ryo Hatori Naotaka Nakazawa Takashi Okumura Tomoki Ishibashi Junichi Kikuta Masaru Ishii Kenji Matsuno Hisao Honda Chiral cell sliding drives left-right asymmetric organ twisting eLife Left-right asymmetry Cell chirality Cell sliding Epithelial morphogenesis |
| title | Chiral cell sliding drives left-right asymmetric organ twisting |
| title_full | Chiral cell sliding drives left-right asymmetric organ twisting |
| title_fullStr | Chiral cell sliding drives left-right asymmetric organ twisting |
| title_full_unstemmed | Chiral cell sliding drives left-right asymmetric organ twisting |
| title_short | Chiral cell sliding drives left-right asymmetric organ twisting |
| title_sort | chiral cell sliding drives left right asymmetric organ twisting |
| topic | Left-right asymmetry Cell chirality Cell sliding Epithelial morphogenesis |
| url | https://elifesciences.org/articles/32506 |
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