Post-meiotic DNA double-strand breaks occur in Tetrahymena, and require Topoisomerase II and Spo11

  1. Takahiko Akematsu  Is a corresponding author
  2. Yasuhiro Fukuda
  3. Jyoti Garg
  4. Jeffrey S Fillingham
  5. Ronald E Pearlman
  6. Josef Loidl
  1. University of Vienna, Austria
  2. Tohoku University, Japan
  3. York University, Canada
  4. Ryerson University, Canada

Abstract

Based on observations of markers for DNA lesions, such as phosphorylated histone H2AX (γH2AX) and open DNA ends, it has been suggested that post-meiotic DNA double-strand breaks (PM-DSBs) enable chromatin remodeling during animal spermiogenesis. However, the existence of PM-DSBs is unconfirmed, and the mechanism responsible for their formation is unclear. Here, we report the first direct observation of programmed PM-DSBs via the electrophoretic separation of DSB-generated DNA fragments in the ciliate Tetrahymena thermophila. These PM-DSBs are accompanied by switching from a heterochromatic to euchromatic chromatin structure in the haploid pronucleus. Both a topoisomerase II paralog with exclusive pronuclear expression and Spo11 are prerequisites for PM-DSB induction. Reduced PM-DSB induction blocks euchromatin formation, characterized by histone H3K56 acetylation, leading to a failure in gametic nuclei production. We propose that PM-DSBs are responsible for histone replacement during the reprogramming of generative to undifferentiated progeny nuclei.

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The following previously published data sets were used

Article and author information

Author details

  1. Takahiko Akematsu

    Department of Chromosome Biology, University of Vienna, Vienna, Austria
    For correspondence
    takahiko.akematsu@univie.ac.at
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9396-0243
  2. Yasuhiro Fukuda

    Department of Biodiversity Science, Tohoku University, Oosaki, Japan
    Competing interests
    The authors declare that no competing interests exist.
  3. Jyoti Garg

    Department of Biology, York University, Toronto, Canada
    Competing interests
    The authors declare that no competing interests exist.
  4. Jeffrey S Fillingham

    Department of Chemistry and Biology, Ryerson University, Toronto, Canada
    Competing interests
    The authors declare that no competing interests exist.
  5. Ronald E Pearlman

    Department of Biology, York University, Toronto, Canada
    Competing interests
    The authors declare that no competing interests exist.
  6. Josef Loidl

    Department of Chromosome Biology, University of Vienna, Vienna, Austria
    Competing interests
    The authors declare that no competing interests exist.

Funding

Seventh Framework Programme (609431)

  • Takahiko Akematsu

Japan Society for the Promotion of Science (15K18475)

  • Yasuhiro Fukuda

Canadian Institutes of Health Research (MOP13347)

  • Ronald E Pearlman

Austrian Science Fund (P27313-B20)

  • Josef Loidl

Natural Sciences and Engineering Research Council of Canada (539509)

  • Ronald E Pearlman

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

Reviewing Editor

  1. Kathleen Collins, University of California, Berkeley, United States

Publication history

  1. Received: February 20, 2017
  2. Accepted: June 13, 2017
  3. Accepted Manuscript published: June 16, 2017 (version 1)
  4. Version of Record published: June 23, 2017 (version 2)

Copyright

© 2017, Akematsu 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. Takahiko Akematsu
  2. Yasuhiro Fukuda
  3. Jyoti Garg
  4. Jeffrey S Fillingham
  5. Ronald E Pearlman
  6. Josef Loidl
(2017)
Post-meiotic DNA double-strand breaks occur in Tetrahymena, and require Topoisomerase II and Spo11
eLife 6:e26176.
https://doi.org/10.7554/eLife.26176

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