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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 62 kDa 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 < 1 kDa), 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.

SUBMITTER: Peterson NG 

PROVIDER: S-EPMC7655102 | biostudies-literature | 2020 Oct

REPOSITORIES: biostudies-literature

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Cytoplasmic sharing through apical membrane remodeling.

Peterson Nora G NG   Stormo Benjamin M BM   Schoenfelder Kevin P KP   King Juliet S JS   Lee Rayson Rs RR   Fox Donald T DT  

eLife 20201014


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 <i>Drosophila</i> rectal papillae. During a six-hour developmental window, 100 individual papillar cells assemble a multinucleate cytoplasm, allowing passage of proteins of at  ...[more]

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