Phase transitioned nuclear Oskar promotes cell division of Drosophila primordial germ cells

  1. Kathryn E Kistler
  2. Tatjana Trcek  Is a corresponding author
  3. Thomas R Hurd
  4. Ruoyu Chen
  5. Feng-Xia Liang
  6. Joseph Sall
  7. Masato Kato
  8. Ruth Lehmann  Is a corresponding author
  1. New York University School of Medicine, United States
  2. NYU Langone Health, United States
  3. University of Texas Southwestern Medical Center, United States

Abstract

Germ granules are non-membranous ribonucleoprotein granules deemed the hubs for post-transcriptional gene regulation and functionally linked to germ cell fate across species. Little is known about the physical properties of germ granules and how these relate to germ cell function. Here we study two types of germ granules in the Drosophila embryo: cytoplasmic germ granules that instruct primordial germ cells (PGCs) formation and nuclear germ granules within early PGCs with unknown function. We show that cytoplasmic and nuclear germ granules are phase transitioned condensates nucleated by Oskar protein that display liquid as well as hydrogel-like properties. Focusing on nuclear granules, we find that Oskar drives their formation in heterologous cell systems. Multiple, independent Oskar protein domains synergize to promote granule phase separation. Deletion of Oskar's nuclear localization sequence specifically ablates nuclear granules in cell systems. In the embryo, nuclear germ granules promote germ cell divisions thereby increasing PGC number for the next generation.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files. Source data has been provided for Figure 3 and Figure 3-figure supplement 1 (Supplementary file 1).

Article and author information

Author details

  1. Kathryn E Kistler

    Department of Cell Biology, New York University School of Medicine, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Tatjana Trcek

    Department of Cell Biology, New York University School of Medicine, New York, United States
    For correspondence
    Tatjana.TrcekPulisic@med.nyu.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4405-8733
  3. Thomas R Hurd

    Department of Cell Biology, New York University School of Medicine, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Ruoyu Chen

    Department of Cell Biology, New York University School of Medicine, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Feng-Xia Liang

    DART Microscopy Laboratory, NYU Langone Health, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Joseph Sall

    DART Microscopy Laboratory, NYU Langone Health, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Masato Kato

    Department of Biochemistry, University of Texas Southwestern Medical Center, Dallas, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Ruth Lehmann

    Department of Cell Biology, New York University School of Medicine, New York, United States
    For correspondence
    lehmann@saturn.med.nyu.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8454-5651

Funding

Howard Hughes Medical Institute

  • Ruth Lehmann

Eunice Kennedy Shriver National Institute of Child Health and Human Development (K99HD088675)

  • Tatjana Trcek

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Copyright

© 2018, Kistler 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. Kathryn E Kistler
  2. Tatjana Trcek
  3. Thomas R Hurd
  4. Ruoyu Chen
  5. Feng-Xia Liang
  6. Joseph Sall
  7. Masato Kato
  8. Ruth Lehmann
(2018)
Phase transitioned nuclear Oskar promotes cell division of Drosophila primordial germ cells
eLife 7:e37949.
https://doi.org/10.7554/eLife.37949

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https://doi.org/10.7554/eLife.37949