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Elife. 2017 Jun 16;6. pii: e26176. doi: 10.7554/eLife.26176.

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

Author information

1
Department of Chromosome Biology, University of Vienna, Vienna, Austria.
2
Department of Biodiversity Science, Tohoku University, Oosaki, Japan.
3
Division of Biological Resource Science, Tohoku University, Oosaki, Japan.
4
Graduate School of Agricultural Science, Tohoku University, Oosaki, Japan.
5
Department of Biology, York University, Toronto, Canada.
6
Department of Chemistry and Biology, Ryerson University, Toronto, 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.

KEYWORDS:

Chromatin remodeling; DNA repair; cell biology; chromosomes; genes; tetrahymena thermophila

PMID:
28621664
PMCID:
PMC5482572
DOI:
10.7554/eLife.26176
[Indexed for MEDLINE]
Free PMC Article

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