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Dynamin regulates metaphase furrow formation and plasma membrane compartmentalization in the syncytial Drosophila embryo

The successive nuclear division cycles in the syncytial Drosophila embryo are accompanied by ingression and regression of plasma membrane furrows, which surround individual nuclei at the embryo periphery, playing a central role in embryo compartmentalization prior to cellularization. Here, we demons...

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Autores principales: Rikhy, Richa, Mavrakis, Manos, Lippincott-Schwartz, Jennifer
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Company of Biologists 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4359736/
https://www.ncbi.nlm.nih.gov/pubmed/25661871
http://dx.doi.org/10.1242/bio.20149936
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author Rikhy, Richa
Mavrakis, Manos
Lippincott-Schwartz, Jennifer
author_facet Rikhy, Richa
Mavrakis, Manos
Lippincott-Schwartz, Jennifer
author_sort Rikhy, Richa
collection PubMed
description The successive nuclear division cycles in the syncytial Drosophila embryo are accompanied by ingression and regression of plasma membrane furrows, which surround individual nuclei at the embryo periphery, playing a central role in embryo compartmentalization prior to cellularization. Here, we demonstrate that cell cycle changes in dynamin localization and activity at the plasma membrane (PM) regulate metaphase furrow formation and PM organization in the syncytial embryo. Dynamin was localized on short PM furrows during interphase, mediating endocytosis of PM components. Dynamin redistributed off ingressed PM furrows in metaphase, correlating with stabilized PM components and the associated actin regulatory machinery on long furrows. Acute inhibition of dynamin in the temperature sensitive shibire mutant embryo resulted in morphogenetic consequences in the syncytial division cycle. These included inhibition of metaphase furrow ingression, randomization of proteins normally polarized to intercap PM and disruption of the diffusion barrier separating PM domains above nuclei. Based on these findings, we propose that cell cycle changes in dynamin orchestrate recruitment of actin regulatory machinery for PM furrow dynamics during the early mitotic cycles in the Drosophila embryo.
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spelling pubmed-43597362015-04-02 Dynamin regulates metaphase furrow formation and plasma membrane compartmentalization in the syncytial Drosophila embryo Rikhy, Richa Mavrakis, Manos Lippincott-Schwartz, Jennifer Biol Open Research Article The successive nuclear division cycles in the syncytial Drosophila embryo are accompanied by ingression and regression of plasma membrane furrows, which surround individual nuclei at the embryo periphery, playing a central role in embryo compartmentalization prior to cellularization. Here, we demonstrate that cell cycle changes in dynamin localization and activity at the plasma membrane (PM) regulate metaphase furrow formation and PM organization in the syncytial embryo. Dynamin was localized on short PM furrows during interphase, mediating endocytosis of PM components. Dynamin redistributed off ingressed PM furrows in metaphase, correlating with stabilized PM components and the associated actin regulatory machinery on long furrows. Acute inhibition of dynamin in the temperature sensitive shibire mutant embryo resulted in morphogenetic consequences in the syncytial division cycle. These included inhibition of metaphase furrow ingression, randomization of proteins normally polarized to intercap PM and disruption of the diffusion barrier separating PM domains above nuclei. Based on these findings, we propose that cell cycle changes in dynamin orchestrate recruitment of actin regulatory machinery for PM furrow dynamics during the early mitotic cycles in the Drosophila embryo. The Company of Biologists 2015-02-06 /pmc/articles/PMC4359736/ /pubmed/25661871 http://dx.doi.org/10.1242/bio.20149936 Text en © 2015. Published by The Company of Biologists Ltd http://creativecommons.org/licenses/by/3.0 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
spellingShingle Research Article
Rikhy, Richa
Mavrakis, Manos
Lippincott-Schwartz, Jennifer
Dynamin regulates metaphase furrow formation and plasma membrane compartmentalization in the syncytial Drosophila embryo
title Dynamin regulates metaphase furrow formation and plasma membrane compartmentalization in the syncytial Drosophila embryo
title_full Dynamin regulates metaphase furrow formation and plasma membrane compartmentalization in the syncytial Drosophila embryo
title_fullStr Dynamin regulates metaphase furrow formation and plasma membrane compartmentalization in the syncytial Drosophila embryo
title_full_unstemmed Dynamin regulates metaphase furrow formation and plasma membrane compartmentalization in the syncytial Drosophila embryo
title_short Dynamin regulates metaphase furrow formation and plasma membrane compartmentalization in the syncytial Drosophila embryo
title_sort dynamin regulates metaphase furrow formation and plasma membrane compartmentalization in the syncytial drosophila embryo
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4359736/
https://www.ncbi.nlm.nih.gov/pubmed/25661871
http://dx.doi.org/10.1242/bio.20149936
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