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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Main Authors: Richa Rikhy, Manos Mavrakis, Jennifer Lippincott-Schwartz
Format: Article
Language:English
Published: The Company of Biologists 2015-02-01
Series:Biology Open
Subjects:
Online Access:http://bio.biologists.org/content/4/3/301
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spelling doaj-274dd43b30af47f097e3c9ec37ff67932021-06-02T18:12:30ZengThe Company of BiologistsBiology Open2046-63902015-02-014330131110.1242/bio.2014993620149936Dynamin regulates metaphase furrow formation and plasma membrane compartmentalization in the syncytial Drosophila embryoRicha Rikhy0Manos Mavrakis1Jennifer Lippincott-Schwartz2 Cell Biology and Metabolism Program, NICHD, NIH, Building 18T, 101, 18 Library Drive, Bethesda, MD, USA. Institut de Biologie du Développement de Marseille, CNRS UMR7288, Aix-Marseille Université, 13288 Marseille, France. Cell Biology and Metabolism Program, NICHD, NIH, Building 18T, 101, 18 Library Drive, Bethesda, MD, USA. 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.http://bio.biologists.org/content/4/3/301DynaminEndocytosisDrosophilaPolarityActinCompartmentalizationSyncytium
collection DOAJ
language English
format Article
sources DOAJ
author Richa Rikhy
Manos Mavrakis
Jennifer Lippincott-Schwartz
spellingShingle Richa Rikhy
Manos Mavrakis
Jennifer Lippincott-Schwartz
Dynamin regulates metaphase furrow formation and plasma membrane compartmentalization in the syncytial Drosophila embryo
Biology Open
Dynamin
Endocytosis
Drosophila
Polarity
Actin
Compartmentalization
Syncytium
author_facet Richa Rikhy
Manos Mavrakis
Jennifer Lippincott-Schwartz
author_sort Richa Rikhy
title 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_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_sort dynamin regulates metaphase furrow formation and plasma membrane compartmentalization in the syncytial drosophila embryo
publisher The Company of Biologists
series Biology Open
issn 2046-6390
publishDate 2015-02-01
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.
topic Dynamin
Endocytosis
Drosophila
Polarity
Actin
Compartmentalization
Syncytium
url http://bio.biologists.org/content/4/3/301
work_keys_str_mv AT richarikhy dynaminregulatesmetaphasefurrowformationandplasmamembranecompartmentalizationinthesyncytialdrosophilaembryo
AT manosmavrakis dynaminregulatesmetaphasefurrowformationandplasmamembranecompartmentalizationinthesyncytialdrosophilaembryo
AT jenniferlippincottschwartz dynaminregulatesmetaphasefurrowformationandplasmamembranecompartmentalizationinthesyncytialdrosophilaembryo
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