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The E3 ubiquitin ligase mindbomb1 controls planar cell polarity-dependent convergent extension movements during zebrafish gastrulation

Vertebrate Delta/Notch signaling involves multiple ligands, receptors and transcription factors. Delta endocytosis – a critical event for Notch activation – is however essentially controlled by the E3 Ubiquitin ligase Mindbomb1 (Mib1). Mib1 inactivation is therefore often used to inhibit Notch signa...

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Autores principales: Saraswathy, Vishnu Muraleedharan, Kurup, Akshai Janardhana, Sharma, Priyanka, Polès, Sophie, Poulain, Morgane, Fürthauer, Maximilian
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8937233/
https://www.ncbi.nlm.nih.gov/pubmed/35142609
http://dx.doi.org/10.7554/eLife.71928
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author Saraswathy, Vishnu Muraleedharan
Kurup, Akshai Janardhana
Sharma, Priyanka
Polès, Sophie
Poulain, Morgane
Fürthauer, Maximilian
author_facet Saraswathy, Vishnu Muraleedharan
Kurup, Akshai Janardhana
Sharma, Priyanka
Polès, Sophie
Poulain, Morgane
Fürthauer, Maximilian
author_sort Saraswathy, Vishnu Muraleedharan
collection PubMed
description Vertebrate Delta/Notch signaling involves multiple ligands, receptors and transcription factors. Delta endocytosis – a critical event for Notch activation – is however essentially controlled by the E3 Ubiquitin ligase Mindbomb1 (Mib1). Mib1 inactivation is therefore often used to inhibit Notch signaling. However, recent findings indicate that Mib1 function extends beyond the Notch pathway. We report a novel Notch-independent role of Mib1 in zebrafish gastrulation. mib1 null mutants and morphants display impaired Convergence Extension (CE) movements. Comparison of different mib1 mutants and functional rescue experiments indicate that Mib1 controls CE independently of Notch. Mib1-dependent CE defects can be rescued using the Planar Cell Polarity (PCP) downstream mediator RhoA, or enhanced through knock-down of the PCP ligand Wnt5b. Mib1 regulates CE through its RING Finger domains that have been implicated in substrate ubiquitination, suggesting that Mib1 may control PCP protein trafficking. Accordingly, we show that Mib1 controls the endocytosis of the PCP component Ryk and that Ryk internalization is required for CE. Numerous morphogenetic processes involve both Notch and PCP signaling. Our observation that during zebrafish gastrulation Mib1 exerts a Notch-independent control of PCP-dependent CE movements suggest that Mib1 loss-of-function phenotypes should be cautiously interpreted depending on the biological context.
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spelling pubmed-89372332022-03-22 The E3 ubiquitin ligase mindbomb1 controls planar cell polarity-dependent convergent extension movements during zebrafish gastrulation Saraswathy, Vishnu Muraleedharan Kurup, Akshai Janardhana Sharma, Priyanka Polès, Sophie Poulain, Morgane Fürthauer, Maximilian eLife Developmental Biology Vertebrate Delta/Notch signaling involves multiple ligands, receptors and transcription factors. Delta endocytosis – a critical event for Notch activation – is however essentially controlled by the E3 Ubiquitin ligase Mindbomb1 (Mib1). Mib1 inactivation is therefore often used to inhibit Notch signaling. However, recent findings indicate that Mib1 function extends beyond the Notch pathway. We report a novel Notch-independent role of Mib1 in zebrafish gastrulation. mib1 null mutants and morphants display impaired Convergence Extension (CE) movements. Comparison of different mib1 mutants and functional rescue experiments indicate that Mib1 controls CE independently of Notch. Mib1-dependent CE defects can be rescued using the Planar Cell Polarity (PCP) downstream mediator RhoA, or enhanced through knock-down of the PCP ligand Wnt5b. Mib1 regulates CE through its RING Finger domains that have been implicated in substrate ubiquitination, suggesting that Mib1 may control PCP protein trafficking. Accordingly, we show that Mib1 controls the endocytosis of the PCP component Ryk and that Ryk internalization is required for CE. Numerous morphogenetic processes involve both Notch and PCP signaling. Our observation that during zebrafish gastrulation Mib1 exerts a Notch-independent control of PCP-dependent CE movements suggest that Mib1 loss-of-function phenotypes should be cautiously interpreted depending on the biological context. eLife Sciences Publications, Ltd 2022-02-10 /pmc/articles/PMC8937233/ /pubmed/35142609 http://dx.doi.org/10.7554/eLife.71928 Text en © 2022, Saraswathy et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Developmental Biology
Saraswathy, Vishnu Muraleedharan
Kurup, Akshai Janardhana
Sharma, Priyanka
Polès, Sophie
Poulain, Morgane
Fürthauer, Maximilian
The E3 ubiquitin ligase mindbomb1 controls planar cell polarity-dependent convergent extension movements during zebrafish gastrulation
title The E3 ubiquitin ligase mindbomb1 controls planar cell polarity-dependent convergent extension movements during zebrafish gastrulation
title_full The E3 ubiquitin ligase mindbomb1 controls planar cell polarity-dependent convergent extension movements during zebrafish gastrulation
title_fullStr The E3 ubiquitin ligase mindbomb1 controls planar cell polarity-dependent convergent extension movements during zebrafish gastrulation
title_full_unstemmed The E3 ubiquitin ligase mindbomb1 controls planar cell polarity-dependent convergent extension movements during zebrafish gastrulation
title_short The E3 ubiquitin ligase mindbomb1 controls planar cell polarity-dependent convergent extension movements during zebrafish gastrulation
title_sort e3 ubiquitin ligase mindbomb1 controls planar cell polarity-dependent convergent extension movements during zebrafish gastrulation
topic Developmental Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8937233/
https://www.ncbi.nlm.nih.gov/pubmed/35142609
http://dx.doi.org/10.7554/eLife.71928
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