Planar Differential Growth Rates Initiate Precise Fold Positions in Complex Epithelia
Tissue folding is a fundamental process that shapes epithelia into complex 3D organs. The initial positioning of folds is the foundation for the emergence of correct tissue morphology. Mechanisms forming individual folds have been studied, but the precise positioning of folds in complex, multi-folde...
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| Vydáno v: | Developmental cell Ročník 51; číslo 3; s. 299 |
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| Hlavní autoři: | , , , , , , |
| Médium: | Journal Article |
| Jazyk: | angličtina |
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United States
04.11.2019
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| ISSN: | 1878-1551, 1878-1551 |
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| Abstract | Tissue folding is a fundamental process that shapes epithelia into complex 3D organs. The initial positioning of folds is the foundation for the emergence of correct tissue morphology. Mechanisms forming individual folds have been studied, but the precise positioning of folds in complex, multi-folded epithelia is less well-understood. We present a computational model of morphogenesis, encompassing local differential growth and tissue mechanics, to investigate tissue fold positioning. We use the Drosophila wing disc as our model system and show that there is spatial-temporal heterogeneity in its planar growth rates. This differential growth, especially at the early stages of development, is the main driver for fold positioning. Increased apical layer stiffness and confinement by the basement membrane drive fold formation but influence positioning to a lesser degree. The model successfully predicts the in vivo morphology of overgrowth clones and wingless mutants via perturbations solely on planar differential growth in silico. |
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| AbstractList | Tissue folding is a fundamental process that shapes epithelia into complex 3D organs. The initial positioning of folds is the foundation for the emergence of correct tissue morphology. Mechanisms forming individual folds have been studied, but the precise positioning of folds in complex, multi-folded epithelia is less well-understood. We present a computational model of morphogenesis, encompassing local differential growth and tissue mechanics, to investigate tissue fold positioning. We use the Drosophila wing disc as our model system and show that there is spatial-temporal heterogeneity in its planar growth rates. This differential growth, especially at the early stages of development, is the main driver for fold positioning. Increased apical layer stiffness and confinement by the basement membrane drive fold formation but influence positioning to a lesser degree. The model successfully predicts the in vivo morphology of overgrowth clones and wingless mutants via perturbations solely on planar differential growth in silico. Tissue folding is a fundamental process that shapes epithelia into complex 3D organs. The initial positioning of folds is the foundation for the emergence of correct tissue morphology. Mechanisms forming individual folds have been studied, but the precise positioning of folds in complex, multi-folded epithelia is less well-understood. We present a computational model of morphogenesis, encompassing local differential growth and tissue mechanics, to investigate tissue fold positioning. We use the Drosophila wing disc as our model system and show that there is spatial-temporal heterogeneity in its planar growth rates. This differential growth, especially at the early stages of development, is the main driver for fold positioning. Increased apical layer stiffness and confinement by the basement membrane drive fold formation but influence positioning to a lesser degree. The model successfully predicts the in vivo morphology of overgrowth clones and wingless mutants via perturbations solely on planar differential growth in silico.Tissue folding is a fundamental process that shapes epithelia into complex 3D organs. The initial positioning of folds is the foundation for the emergence of correct tissue morphology. Mechanisms forming individual folds have been studied, but the precise positioning of folds in complex, multi-folded epithelia is less well-understood. We present a computational model of morphogenesis, encompassing local differential growth and tissue mechanics, to investigate tissue fold positioning. We use the Drosophila wing disc as our model system and show that there is spatial-temporal heterogeneity in its planar growth rates. This differential growth, especially at the early stages of development, is the main driver for fold positioning. Increased apical layer stiffness and confinement by the basement membrane drive fold formation but influence positioning to a lesser degree. The model successfully predicts the in vivo morphology of overgrowth clones and wingless mutants via perturbations solely on planar differential growth in silico. |
| Author | Duda, Maria Kirkland, Natalie J Burden, Jemima J Barrientos, Ricardo Mao, Yanlan Muñoz, José J Tozluoǧlu, Melda |
| Author_xml | – sequence: 1 givenname: Melda surname: Tozluoǧlu fullname: Tozluoǧlu, Melda organization: MRC Laboratory for Molecular Cell Biology, University College London, London WC1E 6BT, UK – sequence: 2 givenname: Maria surname: Duda fullname: Duda, Maria organization: MRC Laboratory for Molecular Cell Biology, University College London, London WC1E 6BT, UK – sequence: 3 givenname: Natalie J surname: Kirkland fullname: Kirkland, Natalie J organization: MRC Laboratory for Molecular Cell Biology, University College London, London WC1E 6BT, UK – sequence: 4 givenname: Ricardo surname: Barrientos fullname: Barrientos, Ricardo organization: MRC Laboratory for Molecular Cell Biology, University College London, London WC1E 6BT, UK – sequence: 5 givenname: Jemima J surname: Burden fullname: Burden, Jemima J organization: MRC Laboratory for Molecular Cell Biology, University College London, London WC1E 6BT, UK – sequence: 6 givenname: José J surname: Muñoz fullname: Muñoz, José J organization: Mathematical and Computational Modeling (LaCàN), Universitat Politècnica de Catalunya, Barcelona, Spain – sequence: 7 givenname: Yanlan surname: Mao fullname: Mao, Yanlan email: y.mao@ucl.ac.uk organization: MRC Laboratory for Molecular Cell Biology, University College London, London WC1E 6BT, UK; Institute for the Physics of Living Systems, University College London, London WC1E 6BT, UK; College of Information and Control, Nanjing University of Information Science and Technology, Nanjing, Jiangsu 210044, China. Electronic address: y.mao@ucl.ac.uk |
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| SubjectTerms | Animals Basement Membrane - ultrastructure Clone Cells Computer Simulation Drosophila melanogaster - growth & development Drosophila melanogaster - metabolism Drosophila Proteins - genetics Epithelium - anatomy & histology Epithelium - growth & development Epithelium - ultrastructure Imaginal Discs - anatomy & histology Imaginal Discs - ultrastructure Models, Biological Morphogenesis Mutation - genetics Time Factors Wings, Animal - anatomy & histology Wings, Animal - ultrastructure Wnt1 Protein - genetics |
| Title | Planar Differential Growth Rates Initiate Precise Fold Positions in Complex Epithelia |
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