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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2015-02-01
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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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1721402266432307200 |