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Prickle isoform participation in distinct polarization events in the Drosophila eye

Planar cell polarity (PCP) signaling regulates several polarization events during development of ommatidia in the Drosophila eye, including directing chirality by polarizing a cell fate choice and determining the direction and extent of ommatidial rotation. The pk(sple) isoform of the PCP protein Pr...

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Autores principales: Cho, Bomsoo, Song, Song, Wan, Joy Y., Axelrod, Jeffrey D.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8836327/
https://www.ncbi.nlm.nih.gov/pubmed/35148314
http://dx.doi.org/10.1371/journal.pone.0262328
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author Cho, Bomsoo
Song, Song
Wan, Joy Y.
Axelrod, Jeffrey D.
author_facet Cho, Bomsoo
Song, Song
Wan, Joy Y.
Axelrod, Jeffrey D.
author_sort Cho, Bomsoo
collection PubMed
description Planar cell polarity (PCP) signaling regulates several polarization events during development of ommatidia in the Drosophila eye, including directing chirality by polarizing a cell fate choice and determining the direction and extent of ommatidial rotation. The pk(sple) isoform of the PCP protein Prickle is known to participate in the R3/R4 cell fate decision, but the control of other polarization events and the potential contributions of the three Pk isoforms have not been clarified. Here, by characterizing expression and subcellular localization of individual isoforms together with re-analyzing isoform specific phenotypes, we show that the R3/R4 fate decision, its coordination with rotation direction, and completion of rotation to a final ±90° rotation angle are separable polarization decisions with distinct Pk isoform requirements and contributions. Both pk(sple) and pk(pk) can enforce robust R3/R4 fate decisions, but only pk(sple) can correctly orient them along the dorsal-ventral axis. In contrast, pk(sple) and pk(pk) can fully and interchangeably sustain coordination of rotation direction and rotation to completion. We propose that expression dynamics and competitive interactions determine isoform participation in these processes. We propose that the selective requirement for pk(sple) to orient the R3/R4 decision and their interchangeability for coordination and completion of rotation reflects their previously described differential interaction with the Fat/Dachsous system which is known to be required for orientation of R3/R4 decisions but not for coordination or completion of rotation.
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spelling pubmed-88363272022-02-12 Prickle isoform participation in distinct polarization events in the Drosophila eye Cho, Bomsoo Song, Song Wan, Joy Y. Axelrod, Jeffrey D. PLoS One Research Article Planar cell polarity (PCP) signaling regulates several polarization events during development of ommatidia in the Drosophila eye, including directing chirality by polarizing a cell fate choice and determining the direction and extent of ommatidial rotation. The pk(sple) isoform of the PCP protein Prickle is known to participate in the R3/R4 cell fate decision, but the control of other polarization events and the potential contributions of the three Pk isoforms have not been clarified. Here, by characterizing expression and subcellular localization of individual isoforms together with re-analyzing isoform specific phenotypes, we show that the R3/R4 fate decision, its coordination with rotation direction, and completion of rotation to a final ±90° rotation angle are separable polarization decisions with distinct Pk isoform requirements and contributions. Both pk(sple) and pk(pk) can enforce robust R3/R4 fate decisions, but only pk(sple) can correctly orient them along the dorsal-ventral axis. In contrast, pk(sple) and pk(pk) can fully and interchangeably sustain coordination of rotation direction and rotation to completion. We propose that expression dynamics and competitive interactions determine isoform participation in these processes. We propose that the selective requirement for pk(sple) to orient the R3/R4 decision and their interchangeability for coordination and completion of rotation reflects their previously described differential interaction with the Fat/Dachsous system which is known to be required for orientation of R3/R4 decisions but not for coordination or completion of rotation. Public Library of Science 2022-02-11 /pmc/articles/PMC8836327/ /pubmed/35148314 http://dx.doi.org/10.1371/journal.pone.0262328 Text en © 2022 Cho et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Cho, Bomsoo
Song, Song
Wan, Joy Y.
Axelrod, Jeffrey D.
Prickle isoform participation in distinct polarization events in the Drosophila eye
title Prickle isoform participation in distinct polarization events in the Drosophila eye
title_full Prickle isoform participation in distinct polarization events in the Drosophila eye
title_fullStr Prickle isoform participation in distinct polarization events in the Drosophila eye
title_full_unstemmed Prickle isoform participation in distinct polarization events in the Drosophila eye
title_short Prickle isoform participation in distinct polarization events in the Drosophila eye
title_sort prickle isoform participation in distinct polarization events in the drosophila eye
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8836327/
https://www.ncbi.nlm.nih.gov/pubmed/35148314
http://dx.doi.org/10.1371/journal.pone.0262328
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