DYNLL1 binds to MRE11 to limit DNA end resection in BRCA1-deficient cells
Limited DNA end resection is the key to impaired homologous recombination in BRCA1 -mutant cancer cells. Here, using a loss-of-function CRISPR screen, we identify DYNLL1 as an inhibitor of DNA end resection. The loss of DYNLL1 enables DNA end resection and restores homologous recombination in BRCA1...
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| Published in: | Nature (London) Vol. 563; no. 7732; pp. 522 - 526 |
|---|---|
| Main Authors: | , , , , , , , , , , , , , , , , , , |
| Format: | Journal Article |
| Language: | English |
| Published: |
London
Nature Publishing Group UK
01.11.2018
Nature Publishing Group |
| Subjects: | |
| ISSN: | 0028-0836, 1476-4687, 1476-4687 |
| Online Access: | Get full text |
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| Abstract | Limited DNA end resection is the key to impaired homologous recombination in
BRCA1
-mutant cancer cells. Here, using a loss-of-function CRISPR screen, we identify DYNLL1 as an inhibitor of DNA end resection. The loss of DYNLL1 enables DNA end resection and restores homologous recombination in
BRCA1
-mutant cells, thereby inducing resistance to platinum drugs and inhibitors of poly(ADP-ribose) polymerase. Low BRCA1 expression correlates with increased chromosomal aberrations in primary ovarian carcinomas, and the junction sequences of somatic structural variants indicate diminished homologous recombination. Concurrent decreases in DYNLL1 expression in carcinomas with low BRCA1 expression reduced genomic alterations and increased homology at lesions. In cells, DYNLL1 limits nucleolytic degradation of DNA ends by associating with the DNA end-resection machinery (MRN complex, BLM helicase and DNA2 endonuclease). In vitro, DYNLL1 binds directly to MRE11 to limit its end-resection activity. Therefore, we infer that DYNLL1 is an important anti-resection factor that influences genomic stability and responses to DNA-damaging chemotherapy.
DYNLL1 antagonizes end resection of DNA double-strand breaks, thereby inhibiting homologous repair, and the loss of DYNLL1 correlates with poor progression-free survival of patients with
BRCA1
-mutant ovarian cancer. |
|---|---|
| AbstractList | Limited DNA end resection is the key to impaired homologous recombination (HR) in BRCA1-mutant cells. Here through a loss-of-function CRISPR screen we identify DYNLL1 as an inhibitor of DNA end resection. Loss of DYNLL1 allows DNA end resection and restores HR in BRCA1-mutant cells, thereby inducing resistance to platinum drugs and poly(ADP-ribose) polymerase (PARP) inhibitors. Low BRCA1 expression correlates with increased chromosomal aberrations in primary ovarian carcinomas, and the junction sequences of somatic structural variants indicate diminished HR. Concurrent decrease in DYNLL1 expression in BRCA1 low carcinomas reduced genomic alterations and increased homology at lesions. In cells DYNLL1 limits nucleolytic degradation of DNA ends by associating with the DNA end resection machinery (MRN complex, BLM helicase and DNA2). In vitro, DYNLL1 directly binds MRE11 to limit its end resection activity. Therefore, we infer that DYNLL1 is an important anti-resection factor that significantly influences genomic stability and response to DNA damaging chemotherapy. Limited DNA end resection is the key to impaired homologous recombination in BRCA1-mutant cancer cells. Here, using a loss-of-function CRISPR screen, we identify DYNLL1 as an inhibitor of DNA end resection. The loss of DYNLL1 enables DNA end resection and restores homologous recombination in BRCA1-mutant cells, thereby inducing resistance to platinum drugs and inhibitors of poly(ADP-ribose) polymerase. Low BRCA1 expression correlates with increased chromosomal aberrations in primary ovarian carcinomas, and the junction sequences of somatic structural variants indicate diminished homologous recombination. Concurrent decreases in DYNLL1 expression in carcinomas with low BRCA1 expression reduced genomic alterations and increased homology at lesions. In cells, DYNLL1 limits nucleolytic degradation of DNA ends by associating with the DNA end-resection machinery (MRN complex, BLM helicase and DNA2 endonuclease). In vitro, DYNLL1 binds directly to MRE11 to limit its end-resection activity. Therefore, we infer that DYNLL1 is an important anti-resection factor that influences genomic stability and responses to DNA-damaging chemotherapy. Limited DNA end resection is the key to impaired homologous recombination in BRCA1-mutant cancer cells. Here, using a loss-of-function CRISPR screen, we identify DYNLL1 as an inhibitor of DNA end resection. The loss of DYNLL1 enables DNA end resection and restores homologous recombination in BRCA1-mutant cells, thereby inducing resistance to platinum drugs and inhibitors of poly(ADP-ribose) polymerase. Low BRCA1 expression correlates with increased chromosomal aberrations in primary ovarian carcinomas, and the junction sequences of somatic structural variants indicate diminished homologous recombination. Concurrent decreases in DYNLL1 expression in carcinomas with low BRCA1 expression reduced genomic alterations and increased homology at lesions. In cells, DYNLL1 limits nucleolytic degradation of DNA ends by associating with the DNA end-resection machinery (MRN complex, BLM helicase and DNA2 endonuclease). In vitro, DYNLL1 binds directly to MRE11 to limit its end-resection activity. Therefore, we infer that DYNLL1 is an important anti-resection factor that influences genomic stability and responses to DNA-damaging chemotherapy. DYNLL1 antagonizes end resection of DNA double-strand breaks, thereby inhibiting homologous repair, and the loss of DYNLL1 correlates with poor progression-free survival of patients with BRCA1-mutant ovarian cancer. Limited DNA end resection is the key to impaired homologous recombination in BRCA1 -mutant cancer cells. Here, using a loss-of-function CRISPR screen, we identify DYNLL1 as an inhibitor of DNA end resection. The loss of DYNLL1 enables DNA end resection and restores homologous recombination in BRCA1 -mutant cells, thereby inducing resistance to platinum drugs and inhibitors of poly(ADP-ribose) polymerase. Low BRCA1 expression correlates with increased chromosomal aberrations in primary ovarian carcinomas, and the junction sequences of somatic structural variants indicate diminished homologous recombination. Concurrent decreases in DYNLL1 expression in carcinomas with low BRCA1 expression reduced genomic alterations and increased homology at lesions. In cells, DYNLL1 limits nucleolytic degradation of DNA ends by associating with the DNA end-resection machinery (MRN complex, BLM helicase and DNA2 endonuclease). In vitro, DYNLL1 binds directly to MRE11 to limit its end-resection activity. Therefore, we infer that DYNLL1 is an important anti-resection factor that influences genomic stability and responses to DNA-damaging chemotherapy. DYNLL1 antagonizes end resection of DNA double-strand breaks, thereby inhibiting homologous repair, and the loss of DYNLL1 correlates with poor progression-free survival of patients with BRCA1 -mutant ovarian cancer. Limited DNA end resection is the key to impaired homologous recombination in BRCA1-mutant cancer cells. Here, using a loss-of-function CRISPR screen, we identify DYNLL1 as an inhibitor of DNA end resection. The loss of DYNLL1 enables DNA end resection and restores homologous recombination in BRCA1-mutant cells, thereby inducing resistance to platinum drugs and inhibitors of poly(ADP-ribose) polymerase. Low BRCA1 expression correlates with increased chromosomal aberrations in primary ovarian carcinomas, and the junction sequences of somatic structural variants indicate diminished homologous recombination. Concurrent decreases in DYNLL1 expression in carcinomas with low BRCA1 expression reduced genomic alterations and increased homology at lesions. In cells, DYNLL1 limits nucleolytic degradation of DNA ends by associating with the DNA end-resection machinery (MRN complex, BLM helicase and DNA2 endonuclease). In vitro, DYNLL1 binds directly to MRE11 to limit its end-resection activity. Therefore, we infer that DYNLL1 is an important anti-resection factor that influences genomic stability and responses to DNA-damaging chemotherapy.Limited DNA end resection is the key to impaired homologous recombination in BRCA1-mutant cancer cells. Here, using a loss-of-function CRISPR screen, we identify DYNLL1 as an inhibitor of DNA end resection. The loss of DYNLL1 enables DNA end resection and restores homologous recombination in BRCA1-mutant cells, thereby inducing resistance to platinum drugs and inhibitors of poly(ADP-ribose) polymerase. Low BRCA1 expression correlates with increased chromosomal aberrations in primary ovarian carcinomas, and the junction sequences of somatic structural variants indicate diminished homologous recombination. Concurrent decreases in DYNLL1 expression in carcinomas with low BRCA1 expression reduced genomic alterations and increased homology at lesions. In cells, DYNLL1 limits nucleolytic degradation of DNA ends by associating with the DNA end-resection machinery (MRN complex, BLM helicase and DNA2 endonuclease). In vitro, DYNLL1 binds directly to MRE11 to limit its end-resection activity. Therefore, we infer that DYNLL1 is an important anti-resection factor that influences genomic stability and responses to DNA-damaging chemotherapy. Limited DNA end resection is the key to impaired homologous recombination in BRCAl-mutant cancer cells. Here, using a loss-of-function CRISPR screen, we identify DYNLL1 as an inhibitor of DNA end resection. The loss of DYNLL1 enables DNA end resection and restores homologous recombination in BRCA1 -mutant cells, thereby inducing resistance to platinum drugs and inhibitors of poly(ADP-ribose) polymerase. Low BRCA1 expression correlates with increased chromosomal aberrations in primary ovarian carcinomas, and the junction sequences of somatic structural variants indicate diminished homologous recombination. Concurrent decreases in DYNLL1 expression in carcinomas with low BRCA1 expression reduced genomic alterations and increased homology at lesions. In cells, DYNLL1 limits nucleolytic degradation of DNA ends by associating with the DNA end-resection machinery (MRN complex, BLM helicase and DNA2 endonuclease). In vitro, DYNLL1 binds directly to MRE11 to limit its end-resection activity. Therefore, we infer that DYNLL1 is an important anti-resection factor that influences genomic stability and responses to DNA-damaging chemotherapy. |
| Audience | Academic |
| Author | Meghani, Khyati Doench, John G. Root, David E. Sharma, Anchal Masson, Jean-Yves Yang, Chunyu He, Yizhou Joseph Caron, Marie-Christine Moore, Jessica De, Subhajyoti Detappe, Alexandre Bian, Jie D’Andrea, Alan D. Konstantinopoulos, Panagiotis A. Chowdhury, Dipanjan Ronato, Daryl A. Legube, Gaelle Drané, Pascal Niraj, Joshi |
| AuthorAffiliation | 2 Genome Stability Laboratory, CHU de Québec Research Center, HDQ Pavilion, Oncology Axis, 9 McMahon, Québec City, QC G1R 2J6, Canada 4 Rutgers Cancer Institute of New Jersey, New Brunswick, New Jersey, USA 1 Division of Radiation and Genome Stability, Department of Radiation Oncology, Dana-Farber Cancer Institute, Harvard Medical School, Boston, MA 02215, USA 6 Broad Institute of Harvard and MIT, Cambridge, MA 02142, USA 8 Center for DNA Damage and Repair, Dana-Farber Cancer Institute, Harvard Medical School, Boston, MA 02215, USA 3 Department of Molecular Biology, Medical Biochemistry and Pathology; Laval University Cancer Research Center, Québec City, QC G1V 0A6, Canada 5 Department of Medical Oncology, Dana-Farber Cancer Institute, Harvard Medical School, Boston, MA 02215, USA 9 Department of Biological Chemistry & Molecular Pharmacology, Harvard Medical School, Boston, MA, 02115, USA 7 LBCMCP, Centre de Biologie Integrative (CBI), CNRS, Université de Toulouse, UT3, 118 Route de Narbonne, |
| AuthorAffiliation_xml | – name: 7 LBCMCP, Centre de Biologie Integrative (CBI), CNRS, Université de Toulouse, UT3, 118 Route de Narbonne, 31062, Toulouse, France – name: 6 Broad Institute of Harvard and MIT, Cambridge, MA 02142, USA – name: 2 Genome Stability Laboratory, CHU de Québec Research Center, HDQ Pavilion, Oncology Axis, 9 McMahon, Québec City, QC G1R 2J6, Canada – name: 8 Center for DNA Damage and Repair, Dana-Farber Cancer Institute, Harvard Medical School, Boston, MA 02215, USA – name: 1 Division of Radiation and Genome Stability, Department of Radiation Oncology, Dana-Farber Cancer Institute, Harvard Medical School, Boston, MA 02215, USA – name: 4 Rutgers Cancer Institute of New Jersey, New Brunswick, New Jersey, USA – name: 3 Department of Molecular Biology, Medical Biochemistry and Pathology; Laval University Cancer Research Center, Québec City, QC G1V 0A6, Canada – name: 9 Department of Biological Chemistry & Molecular Pharmacology, Harvard Medical School, Boston, MA, 02115, USA – name: 5 Department of Medical Oncology, Dana-Farber Cancer Institute, Harvard Medical School, Boston, MA 02215, USA |
| Author_xml | – sequence: 1 givenname: Yizhou Joseph surname: He fullname: He, Yizhou Joseph organization: Division of Radiation and Genome Stability, Department of Radiation Oncology, Dana-Farber Cancer Institute, Harvard Medical School – sequence: 2 givenname: Khyati surname: Meghani fullname: Meghani, Khyati organization: Division of Radiation and Genome Stability, Department of Radiation Oncology, Dana-Farber Cancer Institute, Harvard Medical School – sequence: 3 givenname: Marie-Christine surname: Caron fullname: Caron, Marie-Christine organization: Genome Stability Laboratory, CHU de Québec Research Center, HDQ Pavilion, Oncology Axis, Québec City, Department of Molecular Biology, Medical Biochemistry and Pathology, Laval University Cancer Research Center, Québec City – sequence: 4 givenname: Chunyu surname: Yang fullname: Yang, Chunyu organization: Division of Radiation and Genome Stability, Department of Radiation Oncology, Dana-Farber Cancer Institute, Harvard Medical School – sequence: 5 givenname: Daryl A. surname: Ronato fullname: Ronato, Daryl A. organization: Genome Stability Laboratory, CHU de Québec Research Center, HDQ Pavilion, Oncology Axis, Québec City, Department of Molecular Biology, Medical Biochemistry and Pathology, Laval University Cancer Research Center, Québec City – sequence: 6 givenname: Jie surname: Bian fullname: Bian, Jie organization: Division of Radiation and Genome Stability, Department of Radiation Oncology, Dana-Farber Cancer Institute, Harvard Medical School – sequence: 7 givenname: Anchal surname: Sharma fullname: Sharma, Anchal organization: Rutgers Cancer Institute of New Jersey – sequence: 8 givenname: Jessica surname: Moore fullname: Moore, Jessica organization: Division of Radiation and Genome Stability, Department of Radiation Oncology, Dana-Farber Cancer Institute, Harvard Medical School – sequence: 9 givenname: Joshi surname: Niraj fullname: Niraj, Joshi organization: Division of Radiation and Genome Stability, Department of Radiation Oncology, Dana-Farber Cancer Institute, Harvard Medical School – sequence: 10 givenname: Alexandre surname: Detappe fullname: Detappe, Alexandre organization: Department of Medical Oncology, Dana-Farber Cancer Institute, Harvard Medical School – sequence: 11 givenname: John G. surname: Doench fullname: Doench, John G. organization: Broad Institute of Harvard and MIT – sequence: 12 givenname: Gaelle surname: Legube fullname: Legube, Gaelle organization: LBCMCP, Centre de Biologie Integrative (CBI), CNRS, Université de Toulouse, UT3 – sequence: 13 givenname: David E. surname: Root fullname: Root, David E. organization: Broad Institute of Harvard and MIT – sequence: 14 givenname: Alan D. surname: D’Andrea fullname: D’Andrea, Alan D. organization: Division of Radiation and Genome Stability, Department of Radiation Oncology, Dana-Farber Cancer Institute, Harvard Medical School, Center for DNA Damage and Repair, Dana-Farber Cancer Institute, Harvard Medical School – sequence: 15 givenname: Pascal surname: Drané fullname: Drané, Pascal organization: Division of Radiation and Genome Stability, Department of Radiation Oncology, Dana-Farber Cancer Institute, Harvard Medical School – sequence: 16 givenname: Subhajyoti surname: De fullname: De, Subhajyoti organization: Rutgers Cancer Institute of New Jersey – sequence: 17 givenname: Panagiotis A. surname: Konstantinopoulos fullname: Konstantinopoulos, Panagiotis A. organization: Department of Medical Oncology, Dana-Farber Cancer Institute, Harvard Medical School – sequence: 18 givenname: Jean-Yves surname: Masson fullname: Masson, Jean-Yves organization: Genome Stability Laboratory, CHU de Québec Research Center, HDQ Pavilion, Oncology Axis, Québec City, Department of Molecular Biology, Medical Biochemistry and Pathology, Laval University Cancer Research Center, Québec City – sequence: 19 givenname: Dipanjan surname: Chowdhury fullname: Chowdhury, Dipanjan email: dipanjan_chowdhury@dfci.harvard.edu organization: Division of Radiation and Genome Stability, Department of Radiation Oncology, Dana-Farber Cancer Institute, Harvard Medical School, Broad Institute of Harvard and MIT, Department of Biological Chemistry & Molecular Pharmacology, Harvard Medical School |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/30464262$$D View this record in MEDLINE/PubMed https://hal.science/hal-02352382$$DView record in HAL |
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| Keywords | Somatic Structural Variants Homologous Recombination-mediated Repair BRCA Mutant Cells Clustered Regularly Interspaced Short Palindromic Repeats (CRISPR) High-grade Serous Ovarian Carcinoma (HGSOC) |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 PMCID: PMC7155769 Author Contributions YJH and D.C designed the study with input from PK and ADD. YJH and KM performed most of the cell-based experiments with assistance from CY, JB, JM, and PD. AD did the statistical analysis of images. MCC, DAR and JN conducted the in vitro studies under JYM’s supervision. GL provided the guidance and reagents on the AsiSI system. JD and DR provided all the reagents and the analysis of CRISPR library. AS did statistical and computational analysis of clinical data under SD’s guidance. D.C. wrote the manuscript with input from PK and ADD. |
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| Snippet | Limited DNA end resection is the key to impaired homologous recombination in
BRCA1
-mutant cancer cells. Here, using a loss-of-function CRISPR screen, we... Limited DNA end resection is the key to impaired homologous recombination in BRCA1-mutant cancer cells. Here, using a loss-of-function CRISPR screen, we... Limited DNA end resection is the key to impaired homologous recombination in BRCAl-mutant cancer cells. Here, using a loss-of-function CRISPR screen, we... Limited DNA end resection is the key to impaired homologous recombination (HR) in BRCA1-mutant cells. Here through a loss-of-function CRISPR screen we identify... |
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| SubjectTerms | 13/1 13/106 13/109 13/89 14/19 14/63 38/77 631/337/1427/2190 631/67/1059/2326 Adenosine diphosphate Biochemistry, Molecular Biology Biotechnology BRCA genes BRCA1 protein BRCA1 Protein - deficiency BRCA1 Protein - genetics Breast cancer Cancer Cancer cells Cancer genetics Cancer therapies Cell Line, Tumor Chemotherapy Chromosome Aberrations Chromosome abnormalities CRISPR CRISPR-Cas Systems - genetics Cytoplasmic Dyneins - metabolism Deoxyribonucleic acid DNA DNA - metabolism DNA damage DNA Damage - drug effects DNA helicase DNA methylation DNA repair Drug resistance Drug Resistance, Neoplasm - drug effects Drugs Endonuclease FDA approval Female Gene Editing Gene expression Genes Genes, BRCA1 Genetic research Genomes Genomic Instability - drug effects Homologous recombination Homologous Recombination - drug effects Homology Humanities and Social Sciences Humans Ionizing radiation Lesions Life Sciences Molecular biology Monosaccharides MRE11 Homologue Protein - metabolism MRE11 protein multidisciplinary Mutation Nucleases Ovarian cancer Ovarian carcinoma Ovarian Neoplasms - genetics Ovarian Neoplasms - pathology Platinum Platinum - pharmacology Poly(ADP-ribose) Poly(ADP-ribose) polymerase Poly(ADP-ribose) Polymerase Inhibitors - pharmacology Protein Binding Proteins Recombinational DNA Repair - drug effects Ribose Science Science (multidisciplinary) Surgery Transcription Factors - metabolism |
| Title | DYNLL1 binds to MRE11 to limit DNA end resection in BRCA1-deficient cells |
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