Dynamics of BMP signaling and distribution during zebrafish dorsal-ventral patterning

During vertebrate embryogenesis, dorsal-ventral patterning is controlled by the BMP/Chordin activator/inhibitor system. BMP induces ventral fates, whereas Chordin inhibits BMP signaling on the dorsal side. Several theories can explain how the distributions of BMP and Chordin are regulated to achieve...

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Main Authors: Autumn P Pomreinke, Gary H Soh, Katherine W Rogers, Jennifer K Bergmann, Alexander J Bläßle, Patrick Müller
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2017-08-01
Series:eLife
Subjects:
BMP
Online Access:https://elifesciences.org/articles/25861
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spelling doaj-91fee3c1ae4f4193a7cf619c90aaf7912021-05-05T13:43:35ZengeLife Sciences Publications LtdeLife2050-084X2017-08-01610.7554/eLife.25861Dynamics of BMP signaling and distribution during zebrafish dorsal-ventral patterningAutumn P Pomreinke0Gary H Soh1Katherine W Rogers2https://orcid.org/0000-0001-5700-2662Jennifer K Bergmann3Alexander J Bläßle4Patrick Müller5https://orcid.org/0000-0002-0702-6209Systems Biology of Development Group, Friedrich Miescher Laboratory of the Max Planck Society, Tübingen, GermanySystems Biology of Development Group, Friedrich Miescher Laboratory of the Max Planck Society, Tübingen, GermanySystems Biology of Development Group, Friedrich Miescher Laboratory of the Max Planck Society, Tübingen, GermanySystems Biology of Development Group, Friedrich Miescher Laboratory of the Max Planck Society, Tübingen, GermanySystems Biology of Development Group, Friedrich Miescher Laboratory of the Max Planck Society, Tübingen, GermanySystems Biology of Development Group, Friedrich Miescher Laboratory of the Max Planck Society, Tübingen, GermanyDuring vertebrate embryogenesis, dorsal-ventral patterning is controlled by the BMP/Chordin activator/inhibitor system. BMP induces ventral fates, whereas Chordin inhibits BMP signaling on the dorsal side. Several theories can explain how the distributions of BMP and Chordin are regulated to achieve patterning, but the assumptions regarding activator/inhibitor diffusion and stability differ between models. Notably, ‘shuttling’ models in which the BMP distribution is modulated by a Chordin-mediated increase in BMP diffusivity have gained recent prominence. Here, we directly test five major models by measuring the biophysical properties of fluorescently tagged BMP2b and Chordin in zebrafish embryos. We found that BMP2b and Chordin diffuse and rapidly form extracellular protein gradients, Chordin does not modulate the diffusivity or distribution of BMP2b, and Chordin is not required to establish peak levels of BMP signaling. Our findings challenge current self-regulating reaction-diffusion and shuttling models and provide support for a graded source-sink mechanism underlying zebrafish dorsal-ventral patterning.https://elifesciences.org/articles/25861BMPChordindorsal-ventral patterninggradient formationdiffusionshuttling
collection DOAJ
language English
format Article
sources DOAJ
author Autumn P Pomreinke
Gary H Soh
Katherine W Rogers
Jennifer K Bergmann
Alexander J Bläßle
Patrick Müller
spellingShingle Autumn P Pomreinke
Gary H Soh
Katherine W Rogers
Jennifer K Bergmann
Alexander J Bläßle
Patrick Müller
Dynamics of BMP signaling and distribution during zebrafish dorsal-ventral patterning
eLife
BMP
Chordin
dorsal-ventral patterning
gradient formation
diffusion
shuttling
author_facet Autumn P Pomreinke
Gary H Soh
Katherine W Rogers
Jennifer K Bergmann
Alexander J Bläßle
Patrick Müller
author_sort Autumn P Pomreinke
title Dynamics of BMP signaling and distribution during zebrafish dorsal-ventral patterning
title_short Dynamics of BMP signaling and distribution during zebrafish dorsal-ventral patterning
title_full Dynamics of BMP signaling and distribution during zebrafish dorsal-ventral patterning
title_fullStr Dynamics of BMP signaling and distribution during zebrafish dorsal-ventral patterning
title_full_unstemmed Dynamics of BMP signaling and distribution during zebrafish dorsal-ventral patterning
title_sort dynamics of bmp signaling and distribution during zebrafish dorsal-ventral patterning
publisher eLife Sciences Publications Ltd
series eLife
issn 2050-084X
publishDate 2017-08-01
description During vertebrate embryogenesis, dorsal-ventral patterning is controlled by the BMP/Chordin activator/inhibitor system. BMP induces ventral fates, whereas Chordin inhibits BMP signaling on the dorsal side. Several theories can explain how the distributions of BMP and Chordin are regulated to achieve patterning, but the assumptions regarding activator/inhibitor diffusion and stability differ between models. Notably, ‘shuttling’ models in which the BMP distribution is modulated by a Chordin-mediated increase in BMP diffusivity have gained recent prominence. Here, we directly test five major models by measuring the biophysical properties of fluorescently tagged BMP2b and Chordin in zebrafish embryos. We found that BMP2b and Chordin diffuse and rapidly form extracellular protein gradients, Chordin does not modulate the diffusivity or distribution of BMP2b, and Chordin is not required to establish peak levels of BMP signaling. Our findings challenge current self-regulating reaction-diffusion and shuttling models and provide support for a graded source-sink mechanism underlying zebrafish dorsal-ventral patterning.
topic BMP
Chordin
dorsal-ventral patterning
gradient formation
diffusion
shuttling
url https://elifesciences.org/articles/25861
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