Stored elastic bending tension as a mediator of embryonic body folding
Summary: During development, amniote vertebrate embryos transform from a flat sheet into a three-dimensional cylindrical form through ventral folding of the lateral sides of the sheet (the lateral plate [LP]) and their fusion in the ventral midline. Using a chick embryo slice system, we find that th...
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| Format: | Article |
| Language: | English |
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Elsevier
2025-01-01
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| Series: | Cell Reports |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S2211124724015511 |
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| author | Mira Zaher Ronit Yelin Alaa A. Arraf Julian Jadon Manar Abboud Asleh Sivan Goltzman Lihi Shaulov Dieter P. Reinhardt Thomas M. Schultheiss |
| author_facet | Mira Zaher Ronit Yelin Alaa A. Arraf Julian Jadon Manar Abboud Asleh Sivan Goltzman Lihi Shaulov Dieter P. Reinhardt Thomas M. Schultheiss |
| author_sort | Mira Zaher |
| collection | DOAJ |
| description | Summary: During development, amniote vertebrate embryos transform from a flat sheet into a three-dimensional cylindrical form through ventral folding of the lateral sides of the sheet (the lateral plate [LP]) and their fusion in the ventral midline. Using a chick embryo slice system, we find that the flat stage is actually a poised balance of opposing dorsal and ventral elastic bending tensions. An intact extracellular matrix (ECM) is required for generating tension, as localized digestion of ECM dissipates tension, while removal of endoderm or ectoderm layers has no significant effect. As development proceeds, dorsal bending tension dissipates coincident with epithelial-mesenchymal transition in the dorsal LP while ventral tension is maintained, changing the balance of forces to promote ventral folding. Interference with the elastic ECM component fibrillin reduces ventral bending tension and perturbs body folding in vivo. A model is presented for the accumulation and harnessing of LP bending tension to drive body folding. |
| format | Article |
| id | doaj-art-fcda0bddad67439caebed401a633897a |
| institution | Kabale University |
| issn | 2211-1247 |
| language | English |
| publishDate | 2025-01-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Cell Reports |
| spelling | doaj-art-fcda0bddad67439caebed401a633897a2025-01-12T05:24:52ZengElsevierCell Reports2211-12472025-01-01441115200Stored elastic bending tension as a mediator of embryonic body foldingMira Zaher0Ronit Yelin1Alaa A. Arraf2Julian Jadon3Manar Abboud Asleh4Sivan Goltzman5Lihi Shaulov6Dieter P. Reinhardt7Thomas M. Schultheiss8Department of Genetics and Developmental Biology, Rappaport Faculty of Medicine, Technion-Israel Institute of Technology, Haifa 31096, IsraelDepartment of Genetics and Developmental Biology, Rappaport Faculty of Medicine, Technion-Israel Institute of Technology, Haifa 31096, IsraelDepartment of Genetics and Developmental Biology, Rappaport Faculty of Medicine, Technion-Israel Institute of Technology, Haifa 31096, IsraelDepartment of Genetics and Developmental Biology, Rappaport Faculty of Medicine, Technion-Israel Institute of Technology, Haifa 31096, IsraelDepartment of Genetics and Developmental Biology, Rappaport Faculty of Medicine, Technion-Israel Institute of Technology, Haifa 31096, IsraelDepartment of Genetics and Developmental Biology, Rappaport Faculty of Medicine, Technion-Israel Institute of Technology, Haifa 31096, IsraelDepartment of Genetics and Developmental Biology, Rappaport Faculty of Medicine, Technion-Israel Institute of Technology, Haifa 31096, IsraelFaculty of Medicine and Health Sciences, McGill University, Montreal, QC H3A 0C7, Canada; Faculty of Dental Medicine and Oral Health Sciences, McGill University, Montreal, QC H3A 0C7, CanadaDepartment of Genetics and Developmental Biology, Rappaport Faculty of Medicine, Technion-Israel Institute of Technology, Haifa 31096, Israel; Corresponding authorSummary: During development, amniote vertebrate embryos transform from a flat sheet into a three-dimensional cylindrical form through ventral folding of the lateral sides of the sheet (the lateral plate [LP]) and their fusion in the ventral midline. Using a chick embryo slice system, we find that the flat stage is actually a poised balance of opposing dorsal and ventral elastic bending tensions. An intact extracellular matrix (ECM) is required for generating tension, as localized digestion of ECM dissipates tension, while removal of endoderm or ectoderm layers has no significant effect. As development proceeds, dorsal bending tension dissipates coincident with epithelial-mesenchymal transition in the dorsal LP while ventral tension is maintained, changing the balance of forces to promote ventral folding. Interference with the elastic ECM component fibrillin reduces ventral bending tension and perturbs body folding in vivo. A model is presented for the accumulation and harnessing of LP bending tension to drive body folding.http://www.sciencedirect.com/science/article/pii/S2211124724015511CP: Developmental biology |
| spellingShingle | Mira Zaher Ronit Yelin Alaa A. Arraf Julian Jadon Manar Abboud Asleh Sivan Goltzman Lihi Shaulov Dieter P. Reinhardt Thomas M. Schultheiss Stored elastic bending tension as a mediator of embryonic body folding Cell Reports CP: Developmental biology |
| title | Stored elastic bending tension as a mediator of embryonic body folding |
| title_full | Stored elastic bending tension as a mediator of embryonic body folding |
| title_fullStr | Stored elastic bending tension as a mediator of embryonic body folding |
| title_full_unstemmed | Stored elastic bending tension as a mediator of embryonic body folding |
| title_short | Stored elastic bending tension as a mediator of embryonic body folding |
| title_sort | stored elastic bending tension as a mediator of embryonic body folding |
| topic | CP: Developmental biology |
| url | http://www.sciencedirect.com/science/article/pii/S2211124724015511 |
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