1. Developmental Biology
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Antagonistic control of C. elegans germline stem cell proliferation and differentiation by PUF proteins FBF-1 and FBF-2

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Cite this article as: eLife 2020;9:e52788 doi: 10.7554/eLife.52788

Abstract

Stem cells support tissue maintenance, but the mechanisms that coordinate the rate of stem cell self-renewal with differentiation at a population level remain uncharacterized. We find that two PUF family RNA-binding proteins FBF-1 and FBF-2 have opposite effects on C. elegans germline stem cell dynamics: FBF-1 restricts the rate of meiotic entry, while FBF-2 promotes both cell division and meiotic entry rates. Antagonistic effects of FBFs are mediated by their distinct activities towards the shared set of target mRNAs, where FBF-1-mediated post-transcriptional control requires the activity of CCR4-NOT deadenylase, while FBF-2 is deadenylase-independent and might protect the targets from deadenylation. These regulatory differences depend on protein sequences outside of the conserved PUF family RNA-binding domain. We propose that the opposing FBF-1 and FBF-2 activities serve to modulate stem cell division rate simultaneously with the rate of meiotic entry.

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All data generated or analysed during this study are included in the manuscript and supporting files.

Article and author information

Author details

  1. Xiaobo Wang

    Division of Biological Sciences, University of Montana, Missoula, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Mary Ellenbecker

    Division of Biological Sciences, University of Montana, Missoula, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Benjamin Hickey

    Division of Biological Sciences, University of Montana, Missoula, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Nicholas J Day

    Division of Biological Sciences, University of Montana, Missoula, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Emily Osterli

    Division of Biological Sciences, University of Montana, Missoula, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Mikaya Terzo

    Division of Biological Sciences, University of Montana, Missoula, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Ekaterina Voronina

    Division of Biological Sciences, University of Montana, Missoula, United States
    For correspondence
    ekaterina.voronina@mso.umt.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0194-4260

Funding

National Institute of General Medical Sciences (GM109053)

  • Ekaterina Voronina

National Institute of General Medical Sciences (P20GM103546)

  • Ekaterina Voronina

American Heart Association (18PRE34070028)

  • Xiaobo Wang

Montana Academy of Sciences

  • Xiaobo Wang

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

Reviewing Editor

  1. Yukiko M Yamashita, University of Michigan, United States

Publication history

  1. Received: October 16, 2019
  2. Accepted: August 14, 2020
  3. Accepted Manuscript published: August 17, 2020 (version 1)
  4. Version of Record published: September 2, 2020 (version 2)

Copyright

© 2020, Wang 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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