Abstract
ABSTRACTThe 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.
Highlights
Drosophila embryo development occurs in a syncytium where the nuclei divide without plasma membrane (PM) boundaries
We propose a model in which changes in dynamin localization and activity during the mitotic cycle help coordinate actin and PM remodeling to form metaphase furrows in the syncytial Drosophila embryo
The establishment of PM furrows as discrete compartments surrounding individual nuclei and their mitotic ingression/ regression dynamics is an essential mechanism for Drosophila embryo compartmentalization before cellularization (Mavrakis et al, 2009)
Summary
Drosophila embryo development occurs in a syncytium where the nuclei divide without PM boundaries. Ingressed furrows (6–9 mm in length) in metaphase possibly keep mitotic spindles isolated so they remain bipolar, enabling proper segregation of daughter nuclei during mitosis. Shortened furrows (1–3 mm) in interphase, found in the intercap region, surround individual nuclei, helping to position nuclei uniformly across the embryo cortex. Restricted diffusion of PM components across the furrow gives rise to barriers within the syncytial PM that may help shape morphogen gradients in the embryo (Mavrakis et al, 2009)
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