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.

Reviewing Editor

  1. Anthony A Hyman, Max Planck Institute of Molecular Cell Biology and Genetics, Germany

Version history

  1. Received: April 28, 2018
  2. Accepted: September 9, 2018
  3. Accepted Manuscript published: September 27, 2018 (version 1)
  4. Version of Record published: October 16, 2018 (version 2)

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.

Metrics

  • 5,095
    Page views
  • 852
    Downloads
  • 62
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, Scopus, PubMed Central.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  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

Share this article

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

Further reading

    1. Cell Biology
    Kazuki Hanaoka, Kensuke Nishikawa ... Kouichi Funato
    Research Article

    Membrane contact sites (MCSs) are junctures that perform important roles including coordinating lipid metabolism. Previous studies have indicated that vacuolar fission/fusion processes are coupled with modifications in the membrane lipid composition. However, it has been still unclear whether MCS-mediated lipid metabolism controls the vacuolar morphology. Here, we report that deletion of tricalbins (Tcb1, Tcb2, and Tcb3), tethering proteins at endoplasmic reticulum (ER)–plasma membrane (PM) and ER–Golgi contact sites, alters fusion/fission dynamics and causes vacuolar fragmentation in the yeast Saccharomyces cerevisiae. In addition, we show that the sphingolipid precursor phytosphingosine (PHS) accumulates in tricalbin-deleted cells, triggering the vacuolar division. Detachment of the nucleus–vacuole junction (NVJ), an important contact site between the vacuole and the perinuclear ER, restored vacuolar morphology in both cells subjected to high exogenous PHS and Tcb3-deleted cells, supporting that PHS transport across the NVJ induces vacuole division. Thus, our results suggest that vacuolar morphology is maintained by MCSs through the metabolism of sphingolipids.

    1. Cell Biology
    2. Chromosomes and Gene Expression
    Monica Salinas-Pena, Elena Rebollo, Albert Jordan
    Research Article

    Histone H1 participates in chromatin condensation and regulates nuclear processes. Human somatic cells may contain up to seven histone H1 variants, although their functional heterogeneity is not fully understood. Here, we have profiled the differential nuclear distribution of the somatic H1 repertoire in human cells through imaging techniques including super-resolution microscopy. H1 variants exhibit characteristic distribution patterns in both interphase and mitosis. H1.2, H1.3, and H1.5 are universally enriched at the nuclear periphery in all cell lines analyzed and co-localize with compacted DNA. H1.0 shows a less pronounced peripheral localization, with apparent variability among different cell lines. On the other hand, H1.4 and H1X are distributed throughout the nucleus, being H1X universally enriched in high-GC regions and abundant in the nucleoli. Interestingly, H1.4 and H1.0 show a more peripheral distribution in cell lines lacking H1.3 and H1.5. The differential distribution patterns of H1 suggest specific functionalities in organizing lamina-associated domains or nucleolar activity, which is further supported by a distinct response of H1X or phosphorylated H1.4 to the inhibition of ribosomal DNA transcription. Moreover, H1 variants depletion affects chromatin structure in a variant-specific manner. Concretely, H1.2 knock-down, either alone or combined, triggers a global chromatin decompaction. Overall, imaging has allowed us to distinguish H1 variants distribution beyond the segregation in two groups denoted by previous ChIP-Seq determinations. Our results support H1 variants heterogeneity and suggest that variant-specific functionality can be shared between different cell types.