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The Drosophila melanogaster PIF1 Helicase Promotes Survival During Replication Stress and Processive DNA Synthesis During Double-Strand Gap Repair

Ece Kocak, Sarah Dykstra, Alexandra Nemeth, Catherine G. Coughlin, Kasey Rodgers and View ORCID ProfileMitch McVey
Genetics November 1, 2019 vol. 213 no. 3 835-847; https://doi.org/10.1534/genetics.119.302665
Ece Kocak
Department of Biology, Tufts University, Medford, Massachusetts 02155
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Sarah Dykstra
Department of Biology, Tufts University, Medford, Massachusetts 02155
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Alexandra Nemeth
Department of Biology, Tufts University, Medford, Massachusetts 02155
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Catherine G. Coughlin
Department of Biology, Tufts University, Medford, Massachusetts 02155
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Kasey Rodgers
Department of Biology, Tufts University, Medford, Massachusetts 02155
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Mitch McVey
Department of Biology, Tufts University, Medford, Massachusetts 02155
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Abstract

PIF1 is a 5′ to 3′ DNA helicase that can unwind double-stranded DNA and disrupt nucleic acid-protein complexes. In Saccharomyces cerevisiae, Pif1 plays important roles in mitochondrial and nuclear genome maintenance, telomere length regulation, unwinding of G-quadruplex structures, and DNA synthesis during break-induced replication. Some, but not all, of these functions are shared with other eukaryotes. To gain insight into the evolutionarily conserved functions of PIF1, we created pif1 null mutants in Drosophila melanogaster and assessed their phenotypes throughout development. We found that pif1 mutant larvae exposed to high concentrations of hydroxyurea, but not other DNA damaging agents, experience reduced survival to adulthood. Embryos lacking PIF1 fail to segregate their chromosomes efficiently during early nuclear divisions, consistent with a defect in DNA replication. Furthermore, loss of the BRCA2 protein, which is required for stabilization of stalled replication forks in metazoans, causes synthetic lethality in third instar larvae lacking either PIF1 or the polymerase delta subunit POL32. Interestingly, pif1 mutants have a reduced ability to synthesize DNA during repair of a double-stranded gap, but only in the absence of POL32. Together, these results support a model in which Drosophila PIF1 functions with POL32 during times of replication stress but acts independently of POL32 to promote synthesis during double-strand gap repair.

  • break-induced replication
  • polymerase
  • homologous recombination
  • DNA damage
  • replication fork collapse
  • Received August 27, 2019.
  • Accepted September 18, 2019.
  • Copyright © 2019 by the Genetics Society of America
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Volume 213 Issue 3, November 2019

Genetics: 213 (3)

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Genome integrity and transmission
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The Drosophila melanogaster PIF1 Helicase Promotes Survival During Replication Stress and Processive DNA Synthesis During Double-Strand Gap Repair

Ece Kocak, Sarah Dykstra, Alexandra Nemeth, Catherine G. Coughlin, Kasey Rodgers and View ORCID ProfileMitch McVey
Genetics November 1, 2019 vol. 213 no. 3 835-847; https://doi.org/10.1534/genetics.119.302665
Ece Kocak
Department of Biology, Tufts University, Medford, Massachusetts 02155
  • Find this author on Google Scholar
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Sarah Dykstra
Department of Biology, Tufts University, Medford, Massachusetts 02155
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Alexandra Nemeth
Department of Biology, Tufts University, Medford, Massachusetts 02155
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Catherine G. Coughlin
Department of Biology, Tufts University, Medford, Massachusetts 02155
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Kasey Rodgers
Department of Biology, Tufts University, Medford, Massachusetts 02155
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Mitch McVey
Department of Biology, Tufts University, Medford, Massachusetts 02155
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  • ORCID record for Mitch McVey
  • For correspondence: mitch.mcvey@tufts.edu
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Citation

The Drosophila melanogaster PIF1 Helicase Promotes Survival During Replication Stress and Processive DNA Synthesis During Double-Strand Gap Repair

Ece Kocak, Sarah Dykstra, Alexandra Nemeth, Catherine G. Coughlin, Kasey Rodgers and View ORCID ProfileMitch McVey
Genetics November 1, 2019 vol. 213 no. 3 835-847; https://doi.org/10.1534/genetics.119.302665
Ece Kocak
Department of Biology, Tufts University, Medford, Massachusetts 02155
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Sarah Dykstra
Department of Biology, Tufts University, Medford, Massachusetts 02155
  • Find this author on Google Scholar
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  • Search for this author on this site
Alexandra Nemeth
Department of Biology, Tufts University, Medford, Massachusetts 02155
  • Find this author on Google Scholar
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  • Search for this author on this site
Catherine G. Coughlin
Department of Biology, Tufts University, Medford, Massachusetts 02155
  • Find this author on Google Scholar
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  • Search for this author on this site
Kasey Rodgers
Department of Biology, Tufts University, Medford, Massachusetts 02155
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Mitch McVey
Department of Biology, Tufts University, Medford, Massachusetts 02155
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Mitch McVey
  • For correspondence: mitch.mcvey@tufts.edu

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