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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Main Authors: Keeley, Charlotte N., Ducuing, Antoine, Mollereau, Bertrand, Vincent, Stephane
Other Authors: Massachusetts Institute of Technology. Department of Biological Engineering
Format: Article
Language:en_US
Published: Rockefeller University Press 2015
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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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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