Post-meiotic DNA double-strand breaks occur in Tetrahymena, and require Topoisomerase II and Spo11
- University of Vienna, Austria
- Tohoku University, Japan
- York University, Canada
- 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.
Data availability
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Microarray expression from isolated germ cell typesPublicly available at the NCBI Gene Expression Omnibus (accession no: GSE2736).
Article and author information
Author details
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.
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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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
