1. Developmental Biology

Cytoplasmic sharing through apical membrane remodeling

  1. Nora G Peterson
  2. Benjamin M Stormo
  3. Kevin P Schoenfelder
  4. Juliet S King
  5. Rayson RS Lee
  6. Donald T Fox  Is a corresponding author
  1. Duke University, United States
  2. Duke NUS, Singapore
https://doi.org/10.7554/eLife.58107
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  1. Nora G Peterson
  2. Benjamin M Stormo
  3. Kevin P Schoenfelder
  4. Juliet S King
  5. Rayson RS Lee
  6. Donald T Fox
(2020)
Cytoplasmic sharing through apical membrane remodeling
eLife 9:e58107.
https://doi.org/10.7554/eLife.58107
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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.

The following previously published data sets were used

Article and author information

Author details

  1. Nora G Peterson

    Cell Biology, Duke University, Durham, United States
    Competing interests
    The authors declare that no competing interests exist.

  2. Benjamin M Stormo

    Department of Cell Biology, Duke University, Durham, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6861-8451

  3. Kevin P Schoenfelder

    University Program in Genetics and Genomics, Duke University, Durham, United States
    Competing interests
    The authors declare that no competing interests exist.

  4. Juliet S King

    Department of Pharmacology & Cancer Biology, Duke University, Durham, United States
    Competing interests
    The authors declare that no competing interests exist.

  5. Rayson RS Lee

    Medical Scientist Training Program, Duke NUS, Singapore, Singapore
    Competing interests
    The authors declare that no competing interests exist.

  6. Donald T Fox

    Department of Pharmacology & Cancer Biology, Duke University, Durham, United States
    For correspondence
    don.fox@duke.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0436-179X

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

  1. Elaine Fuchs, Howard Hughes Medical Institute, The Rockefeller University, United States

Version history

  1. Received: April 21, 2020
  2. Accepted: October 13, 2020
  3. Accepted Manuscript published: October 14, 2020 (version 1)
  4. Version of Record published: November 10, 2020 (version 2)
  5. 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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  1. Nora G Peterson
  2. Benjamin M Stormo
  3. Kevin P Schoenfelder
  4. Juliet S King
  5. Rayson RS Lee
  6. Donald T Fox
(2020)
Cytoplasmic sharing through apical membrane remodeling
eLife 9:e58107.
https://doi.org/10.7554/eLife.58107

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