Targeting BRCA1-and BRCA2-deficient cells with RAD52 small molecule inhibitors

Nucleic Acids Research

Volumn 44, Issue 9, 2016, Pages 4189-4199

  Huang, Fei ^a   Goyal, Nadish ^a   Sullivan, Katherine ^b   Hanamshet, Kritika ^a   Patel, Mikir ^a   Mazina, Olga M ^a   Wang, Charles X ^a   An, W Frank ^c   Spoonamore, James ^c   Metkar, Shailesh ^c   Emmitte, Kyle A ^d   Cocklin, Simon ^a   Skorski, Tomasz ^b   Mazin, Alexander V ^a  

^a DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

^b TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^d VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRCA1 PROTEIN; BRCA2 PROTEIN; PROTEIN INHIBITOR; RAD52 PROTEIN; SINGLE STRANDED DNA; ANTINEOPLASTIC AGENT; BRCA1 PROTEIN, HUMAN; BRCA2 PROTEIN, HUMAN; CISPLATIN; PROTEIN BINDING; RAD52 PROTEIN, HUMAN;

ARTICLE; BIOCHEMICAL ANALYSIS; CELL ASSAY; CELL GROWTH; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; DNA REPAIR; FLUORESCENCE ANALYSIS; GENE ACTIVITY; GENE TARGETING; GROWTH INHIBITION; HUMAN; HUMAN CELL; IC50; PRIORITY JOURNAL; RAD52 GENE; TUMOR SUPPRESSOR GENE; ANTAGONISTS AND INHIBITORS; CHEMISTRY; DNA DAMAGE; DRUG EFFECTS; DRUG SCREENING; GENE SILENCING; GENETICS; HIGH THROUGHPUT SCREENING; METABOLISM; TUMOR CELL LINE;

ANTINEOPLASTIC AGENTS; BRCA1 PROTEIN; BRCA2 PROTEIN; CELL LINE, TUMOR; CELL SURVIVAL; CISPLATIN; DNA DAMAGE; DRUG SCREENING ASSAYS, ANTITUMOR; GENE KNOCKDOWN TECHNIQUES; HIGH-THROUGHPUT SCREENING ASSAYS; HUMANS; INHIBITORY CONCENTRATION 50; PROTEIN BINDING; RAD52 DNA REPAIR AND RECOMBINATION PROTEIN;

EID: 84970039361     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkw087     Document Type: Article

References (49)

1. Moynahan, M.E., Jasin, M. (2010) Mitotic homologous recombination maintains genomic stability and suppresses tumorigenesis. Nat. Rev. Mol. Cell Biol., 11, 196-207.
2. Marteijn, J.A., Lans, H., Vermeulen, W., Hoeijmakers, J.H. (2014) Understanding nucleotide excision repair and its roles in cancer and ageing. Nat. Rev. Mol. Cell Biol., 15, 465-481.
3. Iyama, T., Wilson, D.M. 3rd (2013) DNA repair mechanisms in dividing and non-dividing cells. DNA Repair (Amst.), 12, 620-636.
4. Helleday, T. (2011) DNA repair as treatment target. Eur. J. Cancer, 47(Suppl. 3), S333-S335.
5. Lok, B.H., Powell, S.N. (2012) Molecular pathways: understanding the role of Rad52 in homologous recombination for therapeutic advancement. Clin. Cancer Res., 18, 6400-6406.
6. Lord, C.J., Ashworth, A. (2012) The DNA damage response and cancer therapy. Nature, 481, 287-294.
7. Farmer, H., McCabe, N., Lord, C.J., Tutt, A.N., Johnson, D.A., Richardson, T.B., Santarosa, M., Dillon, K.J., Hickson, I., Knights, C. et al. (2005) Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy. Nature, 434, 917-921.
8. Bryant, H.E., Schultz, N., Thomas, H.D., Parker, K.M., Flower, D., Lopez, E., Kyle, S., Meuth, M., Curtin, N.J., Helleday, T. (2005) Specific killing of BRCA2-deficient tumours with inhibitors of poly(ADP-ribose) polymerase. Nature, 434, 913-917.
9. Feng, Z., Scott, S.P., Bussen, W., Sharma, G.G., Guo, G., Pandita, T.K., Powell, S.N. (2011) Rad52 inactivation is synthetically lethal with BRCA2 deficiency. Proc. Natl. Acad. Sci. U.S.A., 108, 686-691.
10. Lok, B.H., Carley, A.C., Tchang, B., Powell, S.N. (2013) RAD52 inactivation is synthetically lethal with deficiencies in BRCA1 and PALB2 in addition to BRCA2 through RAD51-mediated homologous recombination. Oncogene, 32, 3552-3558.
11. Chun, J., Buechelmaier, E.S., Powell, S.N. (2013) Rad51 paralog complexes BCDX2 and CX3 act at different stages in the BRCA1-BRCA2-dependent homologous recombination pathway. Mol. Cell. Biol., 33, 387-395.
12. Antoniou, A.C., Casadei, S., Heikkinen, T., Barrowdale, D., Pylkas, K., Roberts, J., Lee, A., Subramanian, D., De Leeneer, K., Fostira, F. et al. (2014) Breast-cancer risk in families with mutations in PALB2. N. Engl. J. Med., 371, 497-506.
13. Meindl, A., Hellebrand, H., Wiek, C., Erven, V., Wappenschmidt, B., Niederacher, D., Freund, M., Lichtner, P., Hartmann, L., Schaal, H. et al. (2010) Germline mutations in breast and ovarian cancer pedigrees establish RAD51C as a human cancer susceptibility gene. Nat. Genet., 42, 410-414.
14. Fujimori, A., Tachiiri, S., Sonoda, E., Thompson, L.H., Dhar, P.K., Hiraoka, M., Takeda, S., Zhang, Y., Reth, M., Takata, M. (2001) Rad52 partially substitutes for the Rad51 paralog XRCC3 in maintaining chromosomal integrity in vertebrate cells. EMBO J., 20, 5513-5520.
15. Rijkers, T., Van Den Ouweland, J., Morolli, B., Rolink, A.G., Baarends, W.M., Van Sloun, P.P., Lohman, P.H., Pastink, A. (1998) Targeted inactivation of mouse RAD52 reduces homologous recombination but not resistance to ionizing radiation. Mol. Cell. Biol., 18, 6423-6429.
16. Cramer-Morales, K., Nieborowska-Skorska, M., Scheibner, K., Padget, M., Irvine, D.A., Sliwinski, T., Haas, K., Lee, J., Geng, H., Roy, D. et al. (2013) Personalized synthetic lethality induced by targeting RAD52 in leukemias identified by gene mutation and expression profile. Blood, 122, 1293-1304.
17. Bugreev, D.V., Golub, E.I., Stasiak, A.Z., Stasiak, A., Mazin, A.V. (2005) Activation of human meiosis-specific recombinase Dmc1 by Ca2+. J. Biol. Chem., 280, 26886-26895.
18. Rossi, M.J., Mazina, O.M., Bugreev, D.V., Mazin, A.V. (2010) Analyzing the branch migration activities of eukaryotic proteins. Methods, 51, 336-346.
19. Bravman, T., Bronner, V., Lavie, K., Notcovich, A., Papalia, G.A., Myszka, D.G. (2006) Exploring 'one-shot' kinetics and small molecule analysis using the ProteOn XPR36 array biosensor. Anal. Biochem., 358, 281-288.
20. Gunn, A., Bennardo, N., Cheng, A., Stark, J.M. (2011) Correct end use during end joining of multiple chromosomal double strand breaks is influenced by repair protein RAD50, DNA-dependent protein kinase DNA-PKcs, transcription context. J. Biol. Chem., 286, 42470-42482.
21. Gunn, A., Stark, J.M. (2012) I-SceI-based assays to examine distinct repair outcomes of mammalian chromosomal double strand breaks. Methods Mol. Biol., 920, 379-391.
22. Bi, B., Rybalchenko, N., Golub, E.I., Radding, C.M. (2004) Human and yeast Rad52 proteins promote DNA strand exchange. Proc. Natl. Acad. Sci. U.S.A., 101, 9568-9572.
23. Bogliolo, M., Taylor, R.M., Caldecott, K.W., Frosina, G. (2000) Reduced ligation during DNA base excision repair supported by BRCA2 mutant cells. Oncogene, 19, 5781-5787.
24. Abbott, D.W., Freeman, M.L., Holt, J.T. (1998) Double-strand break repair deficiency and radiation sensitivity in BRCA2 mutant cancer cells. J. Natl. Cancer Inst., 90, 978-985.
25. Su, L.K., Wang, S.C., Qi, Y., Luo, W., Hung, M.C., Lin, S.H. (1998) Characterization of BRCA2: temperature sensitivity of detection and cell-cycle regulated expression. Oncogene, 17, 2377-2381.
26. Yuan, S.S., Lee, S.Y., Chen, G., Song, M., Tomlinson, G.E., Lee, E.Y. (1999) BRCA2 is required for ionizing radiation-induced assembly of Rad51 complex in vivo. Cancer Res., 59, 3547-3551.
27. Podszywalow-Bartnicka, P., Wolczyk, M., Kusio-Kobialka, M., Wolanin, K., Skowronek, K., Nieborowska-Skorska, M., Dasgupta, Y., Skorski, T., Piwocka, K. (2014) Downregulation of BRCA1 protein in BCR-ABL1 leukemia cells depends on stress-triggered TIAR-mediated suppression of translation. Cell Cycle, 13, 3727-3741.
28. Liu, Y., Maizels, N. (2000) Coordinated response of mammalian Rad51 and Rad52 to DNA damage. EMBO Rep., 1, 85-90.
29. Essers, J., Houtsmuller, A.B., van Veelen, L., Paulusma, C., Nigg, A.L., Pastink, A., Vermeulen, W., Hoeijmakers, J.H., Kanaar, R. (2002) Nuclear dynamics of RAD52 group homologous recombination proteins in response to DNA damage. EMBO J., 21, 2030-2037.
30. Stark, J.M., Pierce, A.J., Oh, J., Pastink, A., Jasin, M. (2004) Genetic steps of mammalian homologous repair with distinct mutagenic consequences. Mol. Cell. Biol., 24, 9305-9316.
31. Krogh, B.O., Symington, L.S. (2004) Recombination proteins in yeast. Annu. Rev. Genet., 38, 233-271.
32. Symington, L.S., Gautier, J. (2011) Double-strand break end resection and repair pathway choice. Annu. Rev. Genet., 45, 247-271.
33. van Gent, D.C., Hoeijmakers, J.H., Kanaar, R. (2001) Chromosomal stability and the DNA double-stranded break connection. Nat. Rev. Genet., 2, 196-206.
34. Kowalczykowski, S.C. (2000) Initiation of genetic recombination and recombination-dependent replication. Trends Biochem. Sci., 25, 156-165.
35. van Veelen, L.R., Essers, J., van de Rakt, M.W., Odijk, H., Pastink, A., Zdzienicka, M.Z., Paulusma, C.C., Kanaar, R. (2005) Ionizing radiation-induced foci formation of mammalian Rad51 and Rad54 depends on the Rad51 paralogs, but not on Rad52. Mutat. Res., 574, 34-49.
36. Sung, P. (1997) Function of yeast Rad52 protein as a mediator between replication protein A and the Rad51 recombinase. J. Biol. Chem., 272, 28194-28197.
37. Sugiyama, T., Kowalczykowski, S.C. (2002) Rad52 protein associates with replication protein A (RPA)-single-stranded DNA to accelerate Rad51-mediated displacement of RPA and presynaptic complex formation. J. Biol. Chem., 277, 31663-31672.
38. Jensen, R.B., Carreira, A., Kowalczykowski, S.C. (2010) Purified human BRCA2 stimulates RAD51-mediated recombination. Nature, 467, 678-683.
39. Mortensen, U.H., Bendixen, C., Sunjevaric, I., Rothstein, R. (1996) DNA strand annealing is promoted by the yeast Rad52 protein. Proc. Natl. Acad. Sci. U.S.A., 93, 10729-10734.
40. Sugiyama, T., New, J.H., Kowalczykowski, S.C. (1998) DNA annealing by RAD52 protein is stimulated by specific interaction with the complex of replication protein A and single-stranded DNA. Proc. Natl. Acad. Sci. U.S.A., 95, 6049-6054.
41. Sugiyama, T., Kantake, N., Wu, Y., Kowalczykowski, S.C. (2006) Rad52-mediated DNA annealing after Rad51-mediated DNA strand exchange promotes second ssDNA capture. EMBO J., 25, 5539-5548.
42. Bugreev, D.V., Hanaoka, F., Mazin, A.V. (2007) Rad54 dissociates homologous recombination intermediates by branch migration. Nat. Struct. Mol. Biol., 14, 746-753.
43. McIlwraith, M.J., West, S.C. (2008) DNA repair synthesis facilitates RAD52-mediated second-end capture during DSB repair. Mol. Cell, 29, 510-516.
44. Pâques, F., Haber, J.E. (1999) Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev., 63, 349-404.
45. Kagawa, W., Kagawa, A., Saito, K., Ikawa, S., Shibata, T., Kurumizaka, H., Yokoyama, S. (2008) Identification of a second DNA binding site in the human Rad52 protein. J. Biol. Chem., 283, 24264-24273.
46. Helleday, T., Lo, J., van Gent, D.C., Engelward, B.P. (2007) DNA double-strand break repair: From mechanistic understanding to cancer treatment. DNA Repair (Amst)., 6, 923-935.
47. Kagawa, W., Kurumizaka, H., Ishitani, R., Fukai, S., Nureki, O., Shibata, T., Yokoyama, S. (2002) Crystal structure of the homologous-pairing domain from the human Rad52 recombinase in the undecameric form. Mol. Cell, 10, 359-371.
48. Hansmann, T., Pliushch, G., Leubner, M., Kroll, P., Endt, D., Gehrig, A., Preisler-Adams, S., Wieacker, P., Haaf, T. (2012) Constitutive promoter methylation of BRCA1 and RAD51C in patients with familial ovarian cancer and early-onset sporadic breast cancer. Hum. Mol. Genet., 21, 4669-4679.
49. Esteller, M. (2008) Epigenetics in cancer.N. Engl. J. Med., 358, 1148-1159.