Synthetic viability by BRCA2 and PARP1/ARTD1 deficiencies

Nature Communications

Volumn 7, Issue , 2016, Pages

  Ding, Xia ^a   Chaudhuri, Arnab Ray ^b   Callen, Elsa ^b   Pang, Yan ^a   Biswas, Kajal ^a   Klarmann, Kimberly D ^a,c   Martin, Betty K ^a,c   Burkett, Sandra ^a   Cleveland, Linda ^a   Stauffer, Stacey ^a   Sullivan, Teresa ^a   Dewan, Aashish ^a   Marks, Hanna ^a   Tubbs, Anthony T ^b   Wong, Nancy ^b   Buehler, Eugen ^d   Akagi, Keiko ^e   Martin, Scott E ^d,f   Keller, Jonathan R ^a,c   Nussenzweig, André ^b   Sharan, Shyam K ^a   more..

^a NATIONAL CANCER INSTITUTE   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

^c FREDERICK NATIONAL LABORATORY FOR CANCER RESEARCH   (United States)

^d NATIONAL INSTITUTES OF HEALTH   (United States)

^e OHIO STATE UNIVERSITY   (United States)

^f GENENTECH INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRCA2 PROTEIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; OLAPARIB; BRCA2 PROTEIN, MOUSE; CRE RECOMBINASE; DOUBLE STRAND BREAK REPAIR PROTEIN MRE11; INTEGRASE; MRE11A PROTEIN, MOUSE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE INHIBITOR; PARP1 PROTEIN, MOUSE;

ALLELE; CANCER; CELLS AND CELL COMPONENTS; DEGRADATION; HETEROZYGOSITY; INHIBITOR; RECOMBINATION; RODENT; VIABILITY;

ANIMAL CELL; ANIMAL CELL CULTURE; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL; CARCINOGENESIS; CELL DEATH; CELL SURVIVAL; CELL VIABILITY; EMBRYO; FEMALE; GENE MUTATION; GENE SILENCING; HEMATOPOIETIC CELL; HETEROZYGOSITY; HETEROZYGOSITY LOSS; HOMOLOGOUS RECOMBINATION; MOUSE; MOUSE EMBRYONIC STEM CELL; NONHUMAN; PROTEIN DEFECT; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOLOGICAL MODEL; CYTOLOGY; DEFICIENCY; DNA REPLICATION; DRUG EFFECT; HEMATOPOIETIC STEM CELL; HUMAN; METABOLISM;

MUS;

ANIMALS; BRCA2 PROTEIN; CELL SURVIVAL; DNA REPLICATION; HEMATOPOIETIC STEM CELLS; HOMOLOGOUS RECOMBINATION; HUMANS; INTEGRASES; MICE; MODELS, BIOLOGICAL; MOUSE EMBRYONIC STEM CELLS; MRE11 HOMOLOGUE PROTEIN; POLY (ADP-RIBOSE) POLYMERASE-1; POLY(ADP-RIBOSE) POLYMERASE INHIBITORS;

EID: 84979705339     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms12425     Document Type: Article

References (43)

1. Venkitaraman, A. R. Linking the cellular functions of BRCA genes to cancer pathogenesis and treatment. Annu. Rev. Pathol. 4, 461-487 (2009).
2. Schlacher, K. et al. Double-strand break repair-independent role for BRCA2 in blocking stalled replication fork degradation by MRE11. Cell 145, 529-542 (2011).
3. Schlacher, K.,Wu, H. & Jasin, M. A distinct replication fork protection pathway connects Fanconi anemia tumor suppressors to RAD51-BRCA1/2. Cancer Cell 22, 106-116 (2012).
4. Bryant, H. E. et al. Specific killing of BRCA2-deficient tumours with inhibitors of poly(ADP-ribose) polymerase. Nature 434, 913-917 (2005).
5. Farmer, H. et al. Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy. Nature 434, 917-921 (2005).
6. Fong, P. C. et al. Inhibition of poly(ADP-ribose) polymerase in tumors from BRCA mutation carriers. N. Engl. J. Med. 361, 123-134 (2009).
7. Kaelin, Jr W. G. The concept of synthetic lethality in the context of anticancer therapy. Nat. Rev. Cancer 5, 689-698 (2005).
8. Rouleau, M., Patel, A., Hendzel, M. J., Kaufmann, S. H. & Poirier, G. G. PARP inhibition: PARP1 and beyond. Nat. Rev. Cancer 10, 293-301 (2010).
9. Teloni, F. & Altmeyer, M. Readers of poly(ADP-ribose): designed to be fit for purpose. Nucleic Acids Res. 44, 993-1006 (2016).
10. Luijsterburg, M. S. et al. PARP1 Links CHD2-Mediated chromatin expansion and H3.3 deposition to DNA Repair by non-homologous end-joining. Mol. Cell 61, 547-562 (2016).
11. Wang, Z. Q. et al. Mice lacking ADPRT and poly(ADP-ribosyl)ation develop normally but are susceptible to skin disease. Genes Dev. 9, 509-520 (1995).
12. Murai, J. et al. Trapping of PARP1 and PARP2 by clinical PARP inhibitors. Cancer Res. 72, 5588-5599 (2012).
13. Patel, A. G., Sarkaria, J. N. & Kaufmann, S. H. Nonhomologous end joining drives poly(ADP-ribose) polymerase (PARP) inhibitor lethality in homologous recombination-deficient cells. Proc. Natl Acad. Sci. USA 108, 3406-3411 (2011).
14. Lord, C. J. & Ashworth, A. BRCAness revisited. Nat. Rev. Cancer 16, 110-120 (2016).
15. Ledermann, J. et al. Olaparib maintenance therapy in platinum-sensitive relapsed ovarian cancer. N. Engl. J. Med. 366, 1382-1392 (2012).
16. Ledermann, J. et al. Olaparib maintenance therapy in patients with platinumsensitive relapsed serous ovarian cancer: a preplanned retrospective analysis of outcomes by BRCA status in a randomised phase 2 trial. Lancet Oncol. 15, 852-861 (2014).
17. Ogino, H. et al. Loss of Parp-1 affects gene expression profile in a genome-wide manner in ES cells and liver cells. BMC Genomics 8, 41 (2007).
18. Tichy, E. D. et al. Mouse embryonic stem cells, but not somatic cells, predominantly use homologous recombination to repair double-strand DNA breaks. Stem Cells Dev. 19, 1699-1711 (2010).
19. Min, W. et al. Poly(ADP-ribose) binding to Chk1 at stalled replication forks is required for S-phase checkpoint activation. Nat. Commun. 4, 2993 (2013).
20. Kuznetsov, S. G., Liu, P. & Sharan, S. K. Mouse embryonic stem cell-based functional assay to evaluate mutations in BRCA2. Nat. Med. 14, 875-881 (2008).
21. Sharan, S. K. et al. Embryonic lethality and radiation hypersensitivity mediated by Rad51 in mice lacking Brca2. Nature 386, 804-810 (1997).
22. Bryant, H. E. et al. PARP is activated at stalled forks to mediate Mre11-dependent replication restart and recombination. EMBO J. 28, 2601-2615 (2009).
23. Ray Chaudhuri, A. et al. Topoisomerase I poisoning results in PARP-mediated replication fork reversal. Nat. Struct. Mol. Biol. 19, 417-423 (2012).
24. Ying, S., Hamdy, F. C. & Helleday, T. Mre11-dependent degradation of stalled DNA replication forks is prevented by BRCA2 and PARP1. Cancer Res. 72, 2814-2821 (2012).
25. Bunting, S. F. et al. 53BP1 inhibits homologous recombination in Brca1-deficient cells by blocking resection of DNA breaks. Cell 141, 243-254 (2010).
26. Polato, F. et al. CtIP-mediated resection is essential for viability and can operate independently of BRCA1. J. Exp. Med. 211, 1027-1036 (2014).
27. Haince, J. F. et al. PARP1-dependent kinetics of recruitment of MRE11 and NBS1 proteins to multiple DNA damage sites. J. Biol. Chem. 283, 1197-1208 (2008).
28. Sirbu, B. M. et al. Analysis of protein dynamics at active, stalled, and collapsed replication forks. Genes Dev. 25, 1320-1327 (2011).
29. Bouwman, P. et al. 53BP1 loss rescues BRCA1 deficiency and is associated with triple-negative and BRCA-mutated breast cancers. Nat. Struct. Mol. Biol. 17, 688-695 (2010).
30. Dantzer, F. et al. Involvement of poly(ADP-ribose) polymerase in base excision repair. Biochimie 81, 69-75 (1999).
31. Schreiber, V. et al. A dominant-negative mutant of human poly(ADP-ribose) polymerase affects cell recovery, apoptosis, and sister chromatid exchange following DNA damage. Proc. Natl Acad. Sci. USA 92, 4753-4757 (1995).
32. Wang, Z. Q. et al. PARP is important for genomic stability but dispensable in apoptosis. Genes Dev. 11, 2347-2358 (1997).
33. Ray Chaudhuri et al. Replication Fork stability confers chemoresistance in BRCA-deficient cells. Nature 535, 382-387 (2016).
34. Guillemette, S. et al. Resistance to therapy in BRCA2 mutant cells due to loss of the nucleosome remodeling factor CHD4. Genes Dev. 29, 489-494 (2015).
35. Ran, F. A. et al. Genome engineering using the CRISPR-Cas9 system. Nat. Protoc. 8, 2281-2308 (2013).
36. Rickert, R. C., Roes, J. & Rajewsky, K. B lymphocyte-specific, Cre-mediated mutagenesis in mice. Nucleic Acids Res. 25, 1317-1318 (1997).
37. Jonkers, J. et al. Synergistic tumor suppressor activity of BRCA2 and p53 in a conditional mouse model for breast cancer. Nat. Genet. 29, 418-425 (2001).
38. Nagy, A. in Manipulating the Mouse Embryo: A Laboratory Manual 3rd edn (Cold Spring Harbor Laboratory Press, 2003).
39. Golubeva, Y. & R. K. in Methods in Molecular Biology (ed. Kozlov, S. V.) (Humana, 2009).
40. Golubeva, Y., Salcedo, R., Mueller, C., Liotta, L. A. & Espina, V. in Cell Imaging Techniques Methods and Protocols (ed. Taatjes, D. J. & Roth, J.) 213-257 (Humana, 2013).
41. Callen, E. et al. ATM prevents the persistence and propagation of chromosome breaks in lymphocytes. Cell 130, 63-75 (2007).
42. Sirbu, B. M., Couch, F. B. & Cortez, D. Monitoring the spatiotemporal dynamics of proteins at replication forks and in assembled chromatin using isolation of proteins on nascent DNA. Nat. Protoc. 7, 594-605 (2012).
43. Xie, S. et al. Timeless interacts with PARP-1 to promote homologous recombination repair. Mol. Cell 60, 163-176 (2015).