A novel small molecule RAD51 inactivator overcomes imatinib-resistance in chronic myeloid leukaemia

EMBO Molecular Medicine

Volumn 5, Issue 3, 2013, Pages 353-365

  Zhu, Jiewen ^a   Zhou, Longen ^a   Wu, Guikai ^a   Konig, Heiko ^b   Lin, Xiaoqin ^a   Li, Guideng ^a   Qiu, Xiao Long ^a,d   Chen, Chi Fen ^a   Hu, Chun Mei ^a   Goldblatt, Erin ^a   Bhatia, Ravi ^b   Chamberlin, A Richard ^c   Chen, Phang Lang ^a   Lee, Wen Hwa ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d Wisdom Pharmaceutical Co Ltd   (China)

Author keywords

Cancer; CML; Inhibitor; RAD51; Small molecule

Indexed keywords

BCR ABL PROTEIN; IMATINIB; NUCLEOTIDYLTRANSFERASE INHIBITOR; PROTEASOME; PROTEIN RAD51 INHIBIOR; RAD51 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CANCER GROWTH; CHRONIC MYELOID LEUKEMIA; FEMALE; GENE MUTATION; HUMAN; IONIZING RADIATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN MULTIMERIZATION; STEM CELL; SURVIVAL;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; BENZAMIDES; BINDING SITES; CELL LINE, TUMOR; CELL PROLIFERATION; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG RESISTANCE, NEOPLASM; FEMALE; FUSION PROTEINS, BCR-ABL; GENE EXPRESSION REGULATION, NEOPLASTIC; HOMOLOGOUS RECOMBINATION; HUMANS; INDOLES; LEUKEMIA, MYELOGENOUS, CHRONIC, BCR-ABL POSITIVE; MICE; MICE, INBRED NOD; MICE, SCID; MOLECULAR DOCKING SIMULATION; MUTATION; NEOPLASTIC STEM CELLS; PIPERAZINES; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEASOME INHIBITORS; PROTEIN KINASE INHIBITORS; PROTEIN MULTIMERIZATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN-TYROSINE KINASES; PYRIMIDINES; RAD51 RECOMBINASE; RNA INTERFERENCE; TETRAHYDROISOQUINOLINES; TIME FACTORS; TRANSFECTION; TUMOR BURDEN;

EID: 84874692588     PISSN: 17574676     EISSN: 17574684     Source Type: Journal    
DOI: 10.1002/emmm.201201760     Document Type: Article

References (36)

1. Baumann P, Benson FE, West SC (1996) Human Rad51 protein promotes ATP-dependent homologous pairing and strand transfer reactions in vitro. Cell 87: 757-766
2. Boeke JD, Trueheart J, Natsoulis G, Fink GR (1987) 5-Fluoroorotic acid as a selective agent in yeast molecular genetics. Methods Enzymol 154: 164-175
3. Bryant HE, Schultz N, Thomas HD, Parker KM, Flower D, Lopez E, Kyle S, Meuth M, Curtin NJ, Helleday T (2005) Specific killing of BRCA2-deficient tumours with inhibitors of poly(ADP-ribose) polymerase. Nature 434: 913-917
4. Celeste A, Petersen S, Romanienko PJ, Fernandez-Capetillo O, Chen HT, Sedelnikova OA, Reina-San-Martin B, Coppola V, Meffre E, Difilippantonio MJ, et al (2002) Genomic instability in mice lacking histone H2AX. Science 296: 922-927
5. Chen C-F, Chen P-L, Zhong Q, Sharp ZD, Lee W-H (1999) Expression of BRC repeats in breast cancer cells disrupts the BRCA2-Rad51 complex and leads to radiation hypersensitivity and loss of G2/M checkpoint control. J Biol Chem 274: 32931-32935
6. Chen P-L, Chen C-F, Chen Y, Xiao J, Sharp ZD, Lee W-H (1998) The BRC repeats in BRCA2 are critical for RAD51 binding and resistance to methyl methanesulfonate treatment. Proc Natl Acad Sci USA 95: 5287-5292
7. Connell PP, Siddiqui N, Hoffman S, Kuang A, Khatipov E-A, Weichselbaum RR, Bishop DK (2004) A hot spot for RAD51C interactions revealed by a peptide that sensitizes cells to cisplatin. Cancer Res 64: 3002-3005
8. Conway AB, Lynch TW, Zhang Y, Fortin GS, Fung CW, Symington LS, Rice PA (2004) Crystal structure of a Rad51 filament. Nat Struct Mol Biol 11: 791-796
9. Davies AA, Masson J-Y, McIlwraith MJ, Stasiak AZ, Stasiak A, Venkitaraman AR, West SC (2001) Role of BRCA2 in control of the RAD51 recombination and DNA repair protein. Mol Cell 7: 273-282
10. Deininger M, Buchdunger E, Druker BJ (2005) The development of imatinib as a therapeutic agent for chronic myeloid leukemia. Blood 105: 2640-2653
11. Dupré A, Boyer-Chatenet L, Sattler RM, Modi AP, Lee J-H, Nicolette ML, Kopelovich L, Jasin M, Baer R, Paull TT, et al (2008) A forward chemical genetic screen reveals an inhibitor of the Mre11-Rad50-Nbs1 complex. Nat Chem Biol 4: 119-125
12. Gorre ME, Mohammed M, Ellwood K, Hsu N, Paquette R, Rao PN, Sawyers CL (2001) Clinical resistance to STI-571 cancer therapy caused by BCR-ABL gene mutation or amplification. Science 293: 876-880
13. Haaf T, Golub EI, Reddy G, Radding CM, Ward DC (1995) Nuclear foci of mammalian Rad51 recombination protein in somatic cells after DNA damage and its localization in synaptonemal complexes. Proc Natl Acad Sci USA 92: 2298-2302
14. Holtz MS, Slovak ML, Zhang F, Sawyers CL, Forman SJ, Bhatia R (2002) Imatinib mesylate (STI571) inhibits growth of primitive malignant progenitors in chronic myelogenous leukemia through reversal of abnormally increased proliferation. Blood 99: 3792-3800
15. Ito M, Yamamoto S, Nimura K, Hiraoka K, Tamai K, Kaneda Y (2005) Rad51 siRNA delivered by HVJ envelope vector enhances the anti-cancer effect of cisplatin. J Gene Med 7: 1044-1052
16. Klein HL (2008) The consequences of Rad51 overexpression for normal and tumor cells. DNA Repair 7: 686-693
17. Kovalenko OV, Plug AW, Haaf T, Gonda DK, Ashley T, Ward DC, Radding CM, Golub EI (1996) Mammalian ubiquitin-conjugating enzyme Ubc9 interacts with Rad51 recombination protein and localizes in synaptonemal complexes. Proc Natl Acad Sci USA 93: 2958-2963
18. Letavayova L, Markova E, Hermanska K, Vlckova V, Vlasakova D, Chovanec M, Brozmanova J (2006) Relative contribution of homologous recombination and non-homologous end-joining to DNA double-strand break repair after oxidative stress in Saccharomyces cerevisiae. DNA Repair 5: 602-610
19. Luo J, Solimini NL, Elledge SJ (2009) Principles of cancer therapy: oncogene and non-oncogene addiction. Cell 136: 823-837
20. Nardi V, Azam M, Daley GQ (2004) Mechanisms and implications of imatinib resistance mutations in BCR-ABL. Curr Opin Hematol 11: 35-43
21. Pellegrini L, Yu DS, Lo T, Anand S, Lee M, Blundell TL, Venkitaraman AR (2002) Insights into DNA recombination from the structure of a RAD51-BRCA2 complex. Nature 420: 287-293
22. Pierce AJ, Johnson RD, Thompson LH, Jasin M (1999) XRCC3 promotes homology-directed repair of DNA damage in mammalian cells. Genes Dev 13: 2633-2638
23. Poole AJ, Li Y, Kim Y, Lin S-CJ, Lee W-H, Lee EY-HP (2006) Prevention of Brca1-mediated mammary tumorigenesis in mice by a progesterone antagonist. Science 314: 1467-1470
24. Raderschall E, Stout K, Freier S, Suckow V, Schweiger S, Haaf T (2002) Elevated levels of Rad51 recombination protein in tumor cells. Cancer Res 62: 219-225
25. Sak A, Stueben G, Groneberg M, Böcker W, Stuschke M (2005) Targeting of Rad51-dependent homologous recombination: implications for the radiation sensitivity of human lung cancer cell lines. Br J Cancer 92: 1089-1097
26. Shah NP, Tran C, Lee FY, Chen P, Norris D, Sawyers CL (2004) Overriding imatinib resistance with a novel ABL kinase inhibitor. Science 305: 399-401
27. Shin DS, Pellegrini L, Daniels DS, Yelent B, Craig L, Bates D, Yu DS, Shivji MK, Hitomi C, Arvai AS, et al (2003) Full-length archaeal Rad51 structure and mutants: mechanisms for RAD51 assembly and control by BRCA2. EMBO J 22: 4566-4576
28. Skorski T (2002) Oncogenic tyrosine kinases and the DNA-damage response. Nat Rev Cancer 2: 351-360
29. Slupianek A, Schmutte C, Tombline G, Nieborowska-Skorska M, Hoser G, Nowicki MO, Pierce AJ, Fishel R, Skorski T (2001) BCR/ABL regulates mammalian reca homologs, resulting in drug resistance. Mol Cell 8: 795-806
30. Sung P, Robberson DL (1995) DNA strand exchange mediated by a RAD51-ssDNA nucleoprotein filament with polarity opposite to that of RecA. Cell 82: 453-461
31. Vassilev LT, Vu BT, Graves B, Carvajal D, Podlaski F, Filipovic Z, Kong N, Kammlott U, Lukacs C, Klein C, et al (2004) In vivo activation of the p53 pathway by small-molecule antagonists of MDM2. Science 303: 844-848
32. Vispe S, Cazaux C, Lesca C, Defais M (1998) Overexpression of Rad51 protein stimulates homologous recombination and increases resistance of mammalian cells to ionizing radiation. Nucl Acids Res 26: 2859-2864
33. Wu G, Qiu X-L, Zhou L, Zhu J, Chamberlin R, Lau J, Chen P-L, Lee W-H (2008) Small molecule targeting the Hec1/Nek2 mitotic pathway suppresses tumor cell growth in culture and in animal. Cancer Res 68: 8393-8399
34. Xia S, Shammas M, Reis R (1997) Elevated recombination in immortal human cells is mediated by HsRAD51 recombinase. Mol Cell Biol 17: 7151-7158
35. Yu DS, Sonoda E, Takeda S, Huang CLH, Pellegrini L, Blundell TL, Venkitaraman AR (2003) Dynamic control of Rad51 recombinase by self-association and interaction with BRCA2. Mol Cell 12: 1029-1041
36. Zhong Q, Chen C-F, Li S, Chen Y, Wang C-C, Xiao J, Chen P-L, Sharp ZD, Lee W-H (1999) Association of BRCA1 with the hRad50-hMre11-p95 complex and the DNA damage response. Science 285: 747-750