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The Drosophila Actin Regulator ENABLED Regulates Cell Shape and Orientation during Gonad Morphogenesis

Organs develop distinctive morphologies to fulfill their unique functions. We used Drosophila embryonic gonads as a model to study how two different cell lineages, primordial germ cells (PGCs) and somatic gonadal precursors (SGPs), combine to form one organ. We developed a membrane GFP marker to ima...

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Autores principales: Sano, Hiroko, Kunwar, Prabhat S., Renault, Andrew D., Barbosa, Vitor, Clark, Ivan B. N., Ishihara, Shuji, Sugimura, Kaoru, Lehmann, Ruth
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2012
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3530444/
https://www.ncbi.nlm.nih.gov/pubmed/23300733
http://dx.doi.org/10.1371/journal.pone.0052649
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author Sano, Hiroko
Kunwar, Prabhat S.
Renault, Andrew D.
Barbosa, Vitor
Clark, Ivan B. N.
Ishihara, Shuji
Sugimura, Kaoru
Lehmann, Ruth
author_facet Sano, Hiroko
Kunwar, Prabhat S.
Renault, Andrew D.
Barbosa, Vitor
Clark, Ivan B. N.
Ishihara, Shuji
Sugimura, Kaoru
Lehmann, Ruth
author_sort Sano, Hiroko
collection PubMed
description Organs develop distinctive morphologies to fulfill their unique functions. We used Drosophila embryonic gonads as a model to study how two different cell lineages, primordial germ cells (PGCs) and somatic gonadal precursors (SGPs), combine to form one organ. We developed a membrane GFP marker to image SGP behaviors live. These studies show that a combination of SGP cell shape changes and inward movement of anterior and posterior SGPs leads to the compaction of the spherical gonad. This process is disrupted in mutants of the actin regulator, enabled (ena). We show that Ena coordinates these cell shape changes and the inward movement of the SGPs, and Ena affects the intracellular localization of DE-cadherin (DE-cad). Mathematical simulation based on these observations suggests that changes in DE-cad localization can generate the forces needed to compact an elongated structure into a sphere. We propose that Ena regulates force balance in the SGPs by sequestering DE-cad, leading to the morphogenetic movement required for gonad compaction.
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spelling pubmed-35304442013-01-08 The Drosophila Actin Regulator ENABLED Regulates Cell Shape and Orientation during Gonad Morphogenesis Sano, Hiroko Kunwar, Prabhat S. Renault, Andrew D. Barbosa, Vitor Clark, Ivan B. N. Ishihara, Shuji Sugimura, Kaoru Lehmann, Ruth PLoS One Research Article Organs develop distinctive morphologies to fulfill their unique functions. We used Drosophila embryonic gonads as a model to study how two different cell lineages, primordial germ cells (PGCs) and somatic gonadal precursors (SGPs), combine to form one organ. We developed a membrane GFP marker to image SGP behaviors live. These studies show that a combination of SGP cell shape changes and inward movement of anterior and posterior SGPs leads to the compaction of the spherical gonad. This process is disrupted in mutants of the actin regulator, enabled (ena). We show that Ena coordinates these cell shape changes and the inward movement of the SGPs, and Ena affects the intracellular localization of DE-cadherin (DE-cad). Mathematical simulation based on these observations suggests that changes in DE-cad localization can generate the forces needed to compact an elongated structure into a sphere. We propose that Ena regulates force balance in the SGPs by sequestering DE-cad, leading to the morphogenetic movement required for gonad compaction. Public Library of Science 2012-12-26 /pmc/articles/PMC3530444/ /pubmed/23300733 http://dx.doi.org/10.1371/journal.pone.0052649 Text en © 2012 Sano et al http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Sano, Hiroko
Kunwar, Prabhat S.
Renault, Andrew D.
Barbosa, Vitor
Clark, Ivan B. N.
Ishihara, Shuji
Sugimura, Kaoru
Lehmann, Ruth
The Drosophila Actin Regulator ENABLED Regulates Cell Shape and Orientation during Gonad Morphogenesis
title The Drosophila Actin Regulator ENABLED Regulates Cell Shape and Orientation during Gonad Morphogenesis
title_full The Drosophila Actin Regulator ENABLED Regulates Cell Shape and Orientation during Gonad Morphogenesis
title_fullStr The Drosophila Actin Regulator ENABLED Regulates Cell Shape and Orientation during Gonad Morphogenesis
title_full_unstemmed The Drosophila Actin Regulator ENABLED Regulates Cell Shape and Orientation during Gonad Morphogenesis
title_short The Drosophila Actin Regulator ENABLED Regulates Cell Shape and Orientation during Gonad Morphogenesis
title_sort drosophila actin regulator enabled regulates cell shape and orientation during gonad morphogenesis
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3530444/
https://www.ncbi.nlm.nih.gov/pubmed/23300733
http://dx.doi.org/10.1371/journal.pone.0052649
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