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Endonucleolytic processing of covalent protein-linked DNA double-strand breaks

Author

Listed:
  • Matthew J. Neale

    (Memorial Sloan-Kettering Cancer Center)

  • Jing Pan

    (Memorial Sloan-Kettering Cancer Center)

  • Scott Keeney

    (Memorial Sloan-Kettering Cancer Center
    Weill Graduate School of Medical Sciences of Cornell University)

Abstract

DNA double-strand breaks (DSBs) with protein covalently attached to 5′ strand termini are formed by Spo11 to initiate meiotic recombination1,2. The Spo11 protein must be removed for the DSB to be repaired, but the mechanism for removal is unclear3. Here we show that meiotic DSBs in budding yeast are processed by endonucleolytic cleavage that releases Spo11 attached to an oligonucleotide with a free 3′-OH. Two discrete Spo11–oligonucleotide complexes were found in equal amounts, differing with respect to the length of the bound DNA. We propose that these forms arise from different spacings of strand cleavages flanking the DSB, with every DSB processed asymmetrically. Thus, the ends of a single DSB may be biochemically distinct at or before the initial processing step—much earlier than previously thought. SPO11–oligonucleotide complexes were identified in extracts of mouse testis, indicating that this mechanism is evolutionarily conserved. Oligonucleotide–topoisomerase II complexes were also present in extracts of vegetative yeast, although not subject to the same genetic control as for generating Spo11–oligonucleotide complexes. Our findings suggest a general mechanism for repair of protein-linked DSBs.

Suggested Citation

  • Matthew J. Neale & Jing Pan & Scott Keeney, 2005. "Endonucleolytic processing of covalent protein-linked DNA double-strand breaks," Nature, Nature, vol. 436(7053), pages 1053-1057, August.
    • Handle: RePEc:nat:nature:v:436:y:2005:i:7053:d:10.1038_nature03872
    DOI: 10.1038/nature03872
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    Cited by:

    1. Ulaganathan, Kandasamy & Goud, Sravanthi & Reddy, Madhavi & Kayalvili, Ulaganathan, 2017. "Genome engineering for breaking barriers in lignocellulosic bioethanol production," Renewable and Sustainable Energy Reviews, Elsevier, vol. 74(C), pages 1080-1107.
    2. Ihsan Dereli & Vladyslav Telychko & Frantzeskos Papanikos & Kavya Raveendran & Jiaqi Xu & Michiel Boekhout & Marcello Stanzione & Benjamin Neuditschko & Naga Sailaja Imjeti & Elizaveta Selezneva & Has, 2024. "Seeding the meiotic DNA break machinery and initiating recombination on chromosome axes," Nature Communications, Nature, vol. 15(1), pages 1-23, December.

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