Post-meiotic DNA double-strand breaks occur in Tetrahymena, and require Topoisomerase II and Spo11
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.
Reviewing Editor
- Kathleen Collins, University of California, Berkeley, United States
Version history
- Received: February 20, 2017
- Accepted: June 13, 2017
- Accepted Manuscript published: June 16, 2017 (version 1)
- 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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