DNA2 drives processing and restart of reversed replication forks in human cells
Accurate processing of stalled or damaged DNA replication forks is paramount to genomic integrity and recent work points to replication fork reversal and restart as a central mechanism to ensuring high-fidelity DNA replication. Here, we identify a novel DNA2- and WRN-dependent mechanism of reversed...
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| Published in: | The Journal of cell biology Vol. 208; no. 5; p. 545 |
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| Main Authors: | , , , , , , , , , , , , , |
| Format: | Journal Article |
| Language: | English |
| Published: |
United States
02.03.2015
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| Subjects: | |
| ISSN: | 1540-8140, 1540-8140 |
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| Abstract | Accurate processing of stalled or damaged DNA replication forks is paramount to genomic integrity and recent work points to replication fork reversal and restart as a central mechanism to ensuring high-fidelity DNA replication. Here, we identify a novel DNA2- and WRN-dependent mechanism of reversed replication fork processing and restart after prolonged genotoxic stress. The human DNA2 nuclease and WRN ATPase activities functionally interact to degrade reversed replication forks with a 5'-to-3' polarity and promote replication restart, thus preventing aberrant processing of unresolved replication intermediates. Unexpectedly, EXO1, MRE11, and CtIP are not involved in the same mechanism of reversed fork processing, whereas human RECQ1 limits DNA2 activity by preventing extensive nascent strand degradation. RAD51 depletion antagonizes this mechanism, presumably by preventing reversed fork formation. These studies define a new mechanism for maintaining genome integrity tightly controlled by specific nucleolytic activities and central homologous recombination factors. |
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| AbstractList | Accurate processing of stalled or damaged DNA replication forks is paramount to genomic integrity and recent work points to replication fork reversal and restart as a central mechanism to ensuring high-fidelity DNA replication. Here, we identify a novel DNA2- and WRN-dependent mechanism of reversed replication fork processing and restart after prolonged genotoxic stress. The human DNA2 nuclease and WRN ATPase activities functionally interact to degrade reversed replication forks with a 5'-to-3' polarity and promote replication restart, thus preventing aberrant processing of unresolved replication intermediates. Unexpectedly, EXO1, MRE11, and CtIP are not involved in the same mechanism of reversed fork processing, whereas human RECQ1 limits DNA2 activity by preventing extensive nascent strand degradation. RAD51 depletion antagonizes this mechanism, presumably by preventing reversed fork formation. These studies define a new mechanism for maintaining genome integrity tightly controlled by specific nucleolytic activities and central homologous recombination factors. Accurate processing of stalled or damaged DNA replication forks is paramount to genomic integrity and recent work points to replication fork reversal and restart as a central mechanism to ensuring high-fidelity DNA replication. Here, we identify a novel DNA2- and WRN-dependent mechanism of reversed replication fork processing and restart after prolonged genotoxic stress. The human DNA2 nuclease and WRN ATPase activities functionally interact to degrade reversed replication forks with a 5'-to-3' polarity and promote replication restart, thus preventing aberrant processing of unresolved replication intermediates. Unexpectedly, EXO1, MRE11, and CtIP are not involved in the same mechanism of reversed fork processing, whereas human RECQ1 limits DNA2 activity by preventing extensive nascent strand degradation. RAD51 depletion antagonizes this mechanism, presumably by preventing reversed fork formation. These studies define a new mechanism for maintaining genome integrity tightly controlled by specific nucleolytic activities and central homologous recombination factors.Accurate processing of stalled or damaged DNA replication forks is paramount to genomic integrity and recent work points to replication fork reversal and restart as a central mechanism to ensuring high-fidelity DNA replication. Here, we identify a novel DNA2- and WRN-dependent mechanism of reversed replication fork processing and restart after prolonged genotoxic stress. The human DNA2 nuclease and WRN ATPase activities functionally interact to degrade reversed replication forks with a 5'-to-3' polarity and promote replication restart, thus preventing aberrant processing of unresolved replication intermediates. Unexpectedly, EXO1, MRE11, and CtIP are not involved in the same mechanism of reversed fork processing, whereas human RECQ1 limits DNA2 activity by preventing extensive nascent strand degradation. RAD51 depletion antagonizes this mechanism, presumably by preventing reversed fork formation. These studies define a new mechanism for maintaining genome integrity tightly controlled by specific nucleolytic activities and central homologous recombination factors. |
| Author | Pinto, Cosimo Moore, Hayley Cejka, Petr Zellweger, Ralph Thangavel, Saravanabhavan Levikova, Maryna Hendrickson, Eric A Vujanovic, Marko Berti, Matteo Vindigni, Alessandro Lopes, Massimo Gomathinayagam, Shivasankari Lee, Eu Han Stewart, Sheila |
| Author_xml | – sequence: 1 givenname: Saravanabhavan surname: Thangavel fullname: Thangavel, Saravanabhavan organization: Department of Biochemistry and Molecular Biology, Saint Louis University School of Medicine, St. Louis, MO 63104 – sequence: 2 givenname: Matteo surname: Berti fullname: Berti, Matteo organization: Department of Biochemistry and Molecular Biology, Saint Louis University School of Medicine, St. Louis, MO 63104 – sequence: 3 givenname: Maryna surname: Levikova fullname: Levikova, Maryna organization: Institute of Molecular Cancer Research, University of Zurich, CH-8057 Zurich, Switzerland – sequence: 4 givenname: Cosimo surname: Pinto fullname: Pinto, Cosimo organization: Institute of Molecular Cancer Research, University of Zurich, CH-8057 Zurich, Switzerland – sequence: 5 givenname: Shivasankari surname: Gomathinayagam fullname: Gomathinayagam, Shivasankari organization: Department of Biochemistry and Molecular Biology, Saint Louis University School of Medicine, St. Louis, MO 63104 – sequence: 6 givenname: Marko surname: Vujanovic fullname: Vujanovic, Marko organization: Institute of Molecular Cancer Research, University of Zurich, CH-8057 Zurich, Switzerland – sequence: 7 givenname: Ralph surname: Zellweger fullname: Zellweger, Ralph organization: Institute of Molecular Cancer Research, University of Zurich, CH-8057 Zurich, Switzerland – sequence: 8 givenname: Hayley surname: Moore fullname: Moore, Hayley organization: Department of Cell Biology and Physiology, Washington University School of Medicine, St. Louis, MO 63110 – sequence: 9 givenname: Eu Han surname: Lee fullname: Lee, Eu Han organization: Department of Biochemistry, Molecular Biology, and Biophysics, University of Minnesota, Minneapolis, MN 55455 – sequence: 10 givenname: Eric A surname: Hendrickson fullname: Hendrickson, Eric A organization: Department of Biochemistry, Molecular Biology, and Biophysics, University of Minnesota, Minneapolis, MN 55455 – sequence: 11 givenname: Petr surname: Cejka fullname: Cejka, Petr organization: Institute of Molecular Cancer Research, University of Zurich, CH-8057 Zurich, Switzerland – sequence: 12 givenname: Sheila surname: Stewart fullname: Stewart, Sheila organization: Department of Cell Biology and Physiology, Washington University School of Medicine, St. Louis, MO 63110 – sequence: 13 givenname: Massimo surname: Lopes fullname: Lopes, Massimo organization: Institute of Molecular Cancer Research, University of Zurich, CH-8057 Zurich, Switzerland – sequence: 14 givenname: Alessandro surname: Vindigni fullname: Vindigni, Alessandro email: avindign@slu.edu organization: Department of Biochemistry and Molecular Biology, Saint Louis University School of Medicine, St. Louis, MO 63104 avindign@slu.edu |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/25733713$$D View this record in MEDLINE/PubMed |
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| SubjectTerms | Carrier Proteins - genetics Carrier Proteins - metabolism Cell Line DNA Helicases - genetics DNA Helicases - metabolism DNA Repair Enzymes - genetics DNA Repair Enzymes - metabolism DNA Replication - physiology DNA-Binding Proteins - genetics DNA-Binding Proteins - metabolism Exodeoxyribonucleases - genetics Exodeoxyribonucleases - metabolism Humans MRE11 Homologue Protein Nuclear Proteins - genetics Nuclear Proteins - metabolism Rad51 Recombinase - genetics Rad51 Recombinase - metabolism RecQ Helicases - genetics RecQ Helicases - metabolism Werner Syndrome Helicase |
| Title | DNA2 drives processing and restart of reversed replication forks in human cells |
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