Cytoplasmic sharing through apical membrane remodeling
Abstract
Multiple nuclei sharing a common cytoplasm are found in diverse tissues, organisms, and diseases. Yet, multinucleation remains a poorly understood biological property. Cytoplasm sharing invariably involves plasma membrane breaches. In contrast, we discovered cytoplasm sharing without membrane breaching in highly resorptive Drosophila rectal papillae. During a six-hour developmental window, 100 individual papillar cells assemble a multinucleate cytoplasm, allowing passage of proteins of at least 62kDa throughout papillar tissue. Papillar cytoplasm sharing does not employ canonical mechanisms such as incomplete cytokinesis or muscle fusion pore regulators. Instead, sharing requires gap junction proteins (normally associated with transport of molecules <1kDa), which are positioned by membrane remodeling GTPases. Our work reveals a new role for apical membrane remodeling in converting a multicellular epithelium into a giant multinucleate cytoplasm.
Data availability
All data generated or analysed during this study are included in the manuscript and supporting files.
Article and author information
Author details
Funding
National Institutes of Health (GM118447)
- Donald T Fox
National Institutes of Health (HL140811)
- Nora G Peterson
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Elaine Fuchs, Howard Hughes Medical Institute, The Rockefeller University, United States
Version history
- Received: April 21, 2020
- Accepted: October 13, 2020
- Accepted Manuscript published: October 14, 2020 (version 1)
- Version of Record published: November 10, 2020 (version 2)
- Version of Record updated: November 11, 2020 (version 3)
Copyright
© 2020, Peterson et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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