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The proneural wave in the Drosophila optic lobe is driven by an excitable reaction-diffusion mechanism

In living organisms, self-organised waves of signalling activity propagate spatiotemporal information within tissues. During the development of the largest component of the visual processing centre of the Drosophila brain, a travelling wave of proneural gene expression initiates neurogenesis in the...

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Autores principales: Jörg, David J, Caygill, Elizabeth E, Hakes, Anna E, Contreras, Esteban G, Brand, Andrea H, Simons, Benjamin D
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6386523/
https://www.ncbi.nlm.nih.gov/pubmed/30794154
http://dx.doi.org/10.7554/eLife.40919
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author Jörg, David J
Caygill, Elizabeth E
Hakes, Anna E
Contreras, Esteban G
Brand, Andrea H
Simons, Benjamin D
author_facet Jörg, David J
Caygill, Elizabeth E
Hakes, Anna E
Contreras, Esteban G
Brand, Andrea H
Simons, Benjamin D
author_sort Jörg, David J
collection PubMed
description In living organisms, self-organised waves of signalling activity propagate spatiotemporal information within tissues. During the development of the largest component of the visual processing centre of the Drosophila brain, a travelling wave of proneural gene expression initiates neurogenesis in the larval optic lobe primordium and drives the sequential transition of neuroepithelial cells into neuroblasts. Here, we propose that this ‘proneural wave’ is driven by an excitable reaction-diffusion system involving epidermal growth factor receptor (EGFR) signalling interacting with the proneural gene l’sc. Within this framework, a propagating transition zone emerges from molecular feedback and diffusion. Ectopic activation of EGFR signalling in clones within the neuroepithelium demonstrates that a transition wave can be excited anywhere in the tissue by inducing signalling activity, consistent with a key prediction of the model. Our model illuminates the physical and molecular underpinnings of proneural wave progression and suggests a generic mechanism for regulating the sequential differentiation of tissues.
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spelling pubmed-63865232019-02-25 The proneural wave in the Drosophila optic lobe is driven by an excitable reaction-diffusion mechanism Jörg, David J Caygill, Elizabeth E Hakes, Anna E Contreras, Esteban G Brand, Andrea H Simons, Benjamin D eLife Developmental Biology In living organisms, self-organised waves of signalling activity propagate spatiotemporal information within tissues. During the development of the largest component of the visual processing centre of the Drosophila brain, a travelling wave of proneural gene expression initiates neurogenesis in the larval optic lobe primordium and drives the sequential transition of neuroepithelial cells into neuroblasts. Here, we propose that this ‘proneural wave’ is driven by an excitable reaction-diffusion system involving epidermal growth factor receptor (EGFR) signalling interacting with the proneural gene l’sc. Within this framework, a propagating transition zone emerges from molecular feedback and diffusion. Ectopic activation of EGFR signalling in clones within the neuroepithelium demonstrates that a transition wave can be excited anywhere in the tissue by inducing signalling activity, consistent with a key prediction of the model. Our model illuminates the physical and molecular underpinnings of proneural wave progression and suggests a generic mechanism for regulating the sequential differentiation of tissues. eLife Sciences Publications, Ltd 2019-02-22 /pmc/articles/PMC6386523/ /pubmed/30794154 http://dx.doi.org/10.7554/eLife.40919 Text en © 2019, Jörg et al http://creativecommons.org/licenses/by/4.0/ http://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Developmental Biology
Jörg, David J
Caygill, Elizabeth E
Hakes, Anna E
Contreras, Esteban G
Brand, Andrea H
Simons, Benjamin D
The proneural wave in the Drosophila optic lobe is driven by an excitable reaction-diffusion mechanism
title The proneural wave in the Drosophila optic lobe is driven by an excitable reaction-diffusion mechanism
title_full The proneural wave in the Drosophila optic lobe is driven by an excitable reaction-diffusion mechanism
title_fullStr The proneural wave in the Drosophila optic lobe is driven by an excitable reaction-diffusion mechanism
title_full_unstemmed The proneural wave in the Drosophila optic lobe is driven by an excitable reaction-diffusion mechanism
title_short The proneural wave in the Drosophila optic lobe is driven by an excitable reaction-diffusion mechanism
title_sort proneural wave in the drosophila optic lobe is driven by an excitable reaction-diffusion mechanism
topic Developmental Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6386523/
https://www.ncbi.nlm.nih.gov/pubmed/30794154
http://dx.doi.org/10.7554/eLife.40919
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