A DPP-mediated feed-forward loop canalizes morphogenesis during Drosophila dorsal closure
Development is robust because nature has selected various mechanisms to buffer the deleterious effects of environmental and genetic variations to deliver phenotypic stability. Robustness relies on smart network motifs such as feed-forward loops (FFLs) that ensure the reliable interpretation of devel...
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Rockefeller University Press
2015
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Online Access: | http://hdl.handle.net/1721.1/94532 |
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author | Keeley, Charlotte N. Ducuing, Antoine Mollereau, Bertrand Vincent, Stephane |
author2 | Massachusetts Institute of Technology. Department of Biological Engineering |
author_facet | Massachusetts Institute of Technology. Department of Biological Engineering Keeley, Charlotte N. Ducuing, Antoine Mollereau, Bertrand Vincent, Stephane |
author_sort | Keeley, Charlotte N. |
collection | MIT |
description | Development is robust because nature has selected various mechanisms to buffer the deleterious effects of environmental and genetic variations to deliver phenotypic stability. Robustness relies on smart network motifs such as feed-forward loops (FFLs) that ensure the reliable interpretation of developmental signals. In this paper, we show that Decapentaplegic (DPP) and JNK form a coherent FFL that controls the specification and differentiation of leading edge cells during Drosophila melanogaster dorsal closure (DC). We provide molecular evidence that through repression by Brinker (Brk), the DPP branch of the FFL filters unwanted JNK activity. High-throughput live imaging revealed that this DPP/Brk branch is dispensable for DC under normal conditions but is required when embryos are subjected to thermal stress. Our results indicate that the wiring of DPP signaling buffers against environmental challenges and canalizes cell identity. We propose that the main function of DPP pathway during Drosophila DC is to ensure robust morphogenesis, a distinct function from its well-established ability to spread spatial information. |
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format | Article |
id | mit-1721.1/94532 |
institution | Massachusetts Institute of Technology |
language | en_US |
last_indexed | 2024-09-23T12:53:19Z |
publishDate | 2015 |
publisher | Rockefeller University Press |
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spelling | mit-1721.1/945322022-09-28T10:41:19Z A DPP-mediated feed-forward loop canalizes morphogenesis during Drosophila dorsal closure Keeley, Charlotte N. Ducuing, Antoine Mollereau, Bertrand Vincent, Stephane Massachusetts Institute of Technology. Department of Biological Engineering Keeley, Charlotte N. Development is robust because nature has selected various mechanisms to buffer the deleterious effects of environmental and genetic variations to deliver phenotypic stability. Robustness relies on smart network motifs such as feed-forward loops (FFLs) that ensure the reliable interpretation of developmental signals. In this paper, we show that Decapentaplegic (DPP) and JNK form a coherent FFL that controls the specification and differentiation of leading edge cells during Drosophila melanogaster dorsal closure (DC). We provide molecular evidence that through repression by Brinker (Brk), the DPP branch of the FFL filters unwanted JNK activity. High-throughput live imaging revealed that this DPP/Brk branch is dispensable for DC under normal conditions but is required when embryos are subjected to thermal stress. Our results indicate that the wiring of DPP signaling buffers against environmental challenges and canalizes cell identity. We propose that the main function of DPP pathway during Drosophila DC is to ensure robust morphogenesis, a distinct function from its well-established ability to spread spatial information. 2015-02-13T19:13:31Z 2015-02-13T19:13:31Z 2015-01 2014-10 Article http://purl.org/eprint/type/JournalArticle 0021-9525 1540-8140 http://hdl.handle.net/1721.1/94532 Ducuing, A., C. Keeley, B. Mollereau, and S. Vincent. “A DPP-Mediated Feed-Forward Loop Canalizes Morphogenesis During Drosophila Dorsal Closure.” The Journal of Cell Biology 208, no. 2 (January 19, 2015): 239–248. en_US http://dx.doi.org/10.1083/jcb.201410042 The Journal of Cell Biology Creative Commons Attribution http://creativecommons.org/licenses/by-nc-sa/3.0/ application/pdf Rockefeller University Press Rockefeller University Press |
spellingShingle | Keeley, Charlotte N. Ducuing, Antoine Mollereau, Bertrand Vincent, Stephane A DPP-mediated feed-forward loop canalizes morphogenesis during Drosophila dorsal closure |
title | A DPP-mediated feed-forward loop canalizes morphogenesis during Drosophila dorsal closure |
title_full | A DPP-mediated feed-forward loop canalizes morphogenesis during Drosophila dorsal closure |
title_fullStr | A DPP-mediated feed-forward loop canalizes morphogenesis during Drosophila dorsal closure |
title_full_unstemmed | A DPP-mediated feed-forward loop canalizes morphogenesis during Drosophila dorsal closure |
title_short | A DPP-mediated feed-forward loop canalizes morphogenesis during Drosophila dorsal closure |
title_sort | dpp mediated feed forward loop canalizes morphogenesis during drosophila dorsal closure |
url | http://hdl.handle.net/1721.1/94532 |
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