Targeting RAD51 phosphotyrosine-315 to prevent unfaithful recombination repair in BCR-ABL1 leukemia

Blood

Volumn 118, Issue 4, 2011, Pages 1062-1068

  Slupianek, Artur ^a   Dasgupta, Yashodhara ^a   Ren, Shu Yue ^a   Gurdek, Ewa ^a   Donlin, Milene ^a   Nieborowska Skorska, Margaret ^a   Fleury, Fabrice ^b   Skorski, Tomasz ^a,b  

^a TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITÉ DE NANTES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BCR ABL PROTEIN; PEPTIDE APTAMER; PHOSPHOTYROSINE; PHOSPHOTYROSINE 315; PROLINE RICH PROTEIN; PROTEIN BCR ABL 1; RAD51 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; HOMOLOGOUS RECOMBINATION; LEUKEMIA CELL; NONHUMAN; NUCLEUS ACCUMBENS; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING;

EID: 79960988632     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2010-09-307256     Document Type: Article

References (50)

1. O'Hare T, Corbin AS, Druker BJ. Targeted CML therapy: controlling drug resistance, seeking cure. Curr Opin Genet Dev. 2006;16(1):92-99. (Pubitemid 43089618)
2. Perrotti D, Jamieson C, Goldman J, Skorski T. Chronic myeloid leukemia: mechanisms of blastic transformation. J Clin Invest. 2010;120(7):2254-2264.
3. Burke BA, Carroll M. BCR-ABL: a multi-faceted promoter of DNAmutation in chronic myelogeneous leukemia. Leukemia. 2010;24(6):1105-1112.
4. Haferlach C, Bacher U, Schnittger S, Weiss T, Kern W, Haferlach T. Similar patterns of chromosome abnormalities in CML occur in addition to the Philadelphia chromosome with or without tyrosine kinase inhibitor treatment. Leukemia. 2009;24(3):638-640.
5. Giuntoli S, Rovida E, Barbetti V, Cipolleschi MG, Olivotto M, Dello Sbarba P. Hypoxia suppresses BCR/Abl and selects imatinib-insensitive progenitors within clonal CML populations. Leukemia. 2006;20(7):1291-1293. (Pubitemid 43905834)
6. Soverini S, Martinelli G, Rosti G, et al. ABL mutations in late chronic phase chronic myeloid leukemia patients with up-front cytogenetic resistance to imatinib are associated with a greater likelihood of progression to blast crisis and shorter survival: a study by the GIMEMAWorking Party on Chronic Myeloid Leukemia. J Clin Oncol. 2005;23(18):4100-4109. (Pubitemid 46211315)
7. Barnes DJ, Palaiologou D, Panousopoulou E, et al. Bcr-Abl expression levels determine the rate of development of resistance to imatinib mesylate in chronic myeloid leukemia. Cancer Res. 2005;65(19):8912-8919. (Pubitemid 41377381)
8. Khorashad JS, De Melo VA, Fiegler H, et al. Multiple sub-microscopic genomic lesions are a universal feature of chronic myeloid leukaemia at diagnosis. Leukemia. 2008;22(9):1806-1807.
9. Brazma D, Grace C, Howard J, et al. Genomic profile of chronic myelogenous leukemia: imbalances associated with disease progression. Genes Chromosomes Cancer. 2007;46(11):1039-1050. (Pubitemid 47502843)
10. Slupianek A, Nowicki MO, Koptyra M, Skorski T. BCR/ABL modifies the kinetics and fidelity of DNA double-strand breaks repair in hematopoietic cells. DNA Repair (Amst). 2006;5(2):243-250. (Pubitemid 43069524)
11. Koptyra M, Cramer K, Slupianek A, Richardson C, Skorski T. BCR/ABL promotes accumulation of chromosomal aberrations induced by oxidative and genotoxic stress. Leukemia. 2008;22(10):1969-1972.
12. Fernandes MS, Reddy MM, Gonneville JR, et al. BCR-ABL promotes the frequency of mutagenic single-strand annealing DNA repair. Blood. 2009;114(9):1813-1819.
13. Cramer K, Nieborowska-Skorska M, Koptyra M, et al. BCR/ABL and other kinases from chronic myeloproliferative disorders stimulate singlestrand annealing, an unfaithful DNA doublestrand break repair. Cancer Res. 2008;68(17):6884-6888.
14. Dierov J, Sanchez PV, Burke BA, et al. BCR/ABL induces chromosomal instability after genotoxic stress and alters the cell death threshold. Leukemia. 2009;23(2):279-286.
15. Gaymes TJ, Mufti GJ, Rassool FV. Myeloid leukemias have increased activity of the nonhomologous end-joining pathway and concomitant DNA misrepair that is dependent on the Ku70/86 heterodimer. Cancer Res. 2002;62(10):2791-2797. (Pubitemid 34525762)
16. Moynahan ME, Jasin M. Mitotic homologous recombination maintains genomic stability and suppresses tumorigenesis. Nat Rev Mol Cell Biol. 2010;11(3):196-207.
17. Yang D, Waldman AS. Fine-resolution analysis of products of intrachromosomal homeologous recombination in mammalian cells. Mol Cell Biol. 1997;17(7):3614-3628. (Pubitemid 27281837)
18. Slupianek A, Hoser G, Majsterek I, et al. Fusion tyrosine kinases induce drug resistance by stimulation of homology-dependent recombination repair, prolongation of G(2)/M phase, and protection from apoptosis. Mol Cell Biol. 2002;22(12):4189-4201. (Pubitemid 34556589)
19. Slupianek A, Schmutte C, Tombline G, et al. BCR/ABL regulates mammalian RecA homologs, resulting in drug resistance. Mol Cell. 2001;8(4):795-806. (Pubitemid 33030213)
20. Plo I, Nakatake M, Malivert L, et al. JAK2 stimulates homologous recombination and genetic instability: potential implication in the heterogeneity of myeloproliferative disorders. Blood. 2008;112(4):1402-1412.
21. Trojanek J, Ho T, Del Valle L, et al. Role of the insulin-like growth factor I/insulin receptor substrate 1 axis in Rad51 trafficking and DNA repair by homologous recombination. Mol Cell Biol. 2003;23(21):7510-7524. (Pubitemid 37271452)
22. Ganapathipillai SS, Medova M, Aebersold DM, et al. Coupling of mutated Met variants to DNA repair via Abl and Rad51. Cancer Res. 2008;68(14):5769-5777.
23. Ko JC, Hong JH, Wang LH, Lin YW. The role of repair protein Rad51 in synergistic cytotoxicity and mutagenicity induced by epidermal growth factor receptor inhibitor (Gefitinib, IressaR) and benzo[a]pyrene in human lung cancer. Exp Cell Res. 2008;314(8):1881-1891.
24. Heath C, Cross NC. Critical role of STAT5 activation in transformation mediated by ZNF198-FGFR1. J Biol Chem. 2004;279(8):6666-6673. (Pubitemid 38248805)
25. Smith JA, Bannister LA, Bhattacharjee V,Wang Y, Waldman BC,Waldman AS. Accurate homologous recombination is a prominent double-strand break repair pathway in mammalian chromosomes and is modulated by mismatch repair protein Msh2. Mol Cell Biol. 2007;27(22):7816-7827. (Pubitemid 350086415)
26. Popova M, Shimizu H, Yamamoto K, Lebechec M, Takahashi M, Fleury F. Detection of c-Abl kinase-promoted phosphorylation of Rad51 by specific antibodies reveals that Y54 phosphorylation is dependent on that of Y315. FEBS Lett. 2009;583(12):1867-1872.
27. Borghouts C, Kunz C, Groner B. Current strategies for the development of peptide-based anticancer therapeutics. J Pept Sci. 2005;11(11):713-726. (Pubitemid 41684258)
28. Nowicki MO, Falinski R, Koptyra M, et al. BCR/ABL oncogenic kinase promotes unfaithful repair of the reactive oxygen species-dependent DNA double-strand breaks. Blood. 2004;104(12):3746-3753. (Pubitemid 39564453)
29. Van Etten RA, Debnath J, Zhou H, Casasnovas JM. Introduction of a loss-of-function point mutation from the SH3 region of the Caenorhabditis elegans sem-5 gene activates the transforming ability of c-abl in vivo and abolishes binding of proline-rich ligands in vitro. Oncogene. 1995;10(10):1977-1988.
30. Richardson C, Stark JM, Ommundsen M, Jasin M. Rad51 overexpression promotes alternative doublestrand break repair pathways and genome instability. Oncogene. 2004;23(2):546-553. (Pubitemid 38175009)
31. Zhang W, Johnson JD, Rutter WJ. Association and phosphorylation-dependent dissociation of proteins in the insulin receptor complex. Proc Natl Acad Sci U S A. 1993;90(23):11317-11321. (Pubitemid 23354420)
32. Forget AL, Kowalczykowski SC. Single-molecule imaging brings Rad51 nucleoprotein filaments into focus. Trends Cell Biol. 2010;20(5):269-276.
33. Shimizu H, Popova M, Fleury F, et al. c-ABL tyrosine kinase stabilizes RAD51 chromatin association. Biochem Biophys Res Commun. 2009;382(2):286-291.
34. Lander ES, Linton LM, Birren B, et al. Initial sequencing and analysis of the human genome. Nature. 2001;409(6822):860-921.
35. Albano F, Anelli L, Zagaria A, et al. Non random distribution of genomic features in breakpoint regions involved in chronic myeloid leukemia cases with variant t(9;22) or additional chromosomal rearrangements. Mol Cancer. 2010;9(120):120.
36. de Wind N, Dekker M, Berns A, Radman M, te Riele H. Inactivation of the mouse Msh2 gene results in mismatch repair deficiency, methylation tolerance, hyperrecombination, and predisposition to cancer. Cell. 1995;82(2):321-330.
37. Stoklosa T, Poplawski T, Koptyra M, et al. BCR/ABL inhibits mismatch repair to protect from apoptosis and induce point mutations. Cancer Res. 2008;68(8):2576-2580. (Pubitemid 351556254)
38. Marley SB, Gordon MY. Chronic myeloid leukaemia: stem cell derived but progenitor cell driven. Clin Sci (Lond). 2005;109(1):13-25. (Pubitemid 40943029)
39. Jamieson CH, Ailles LE, Dylla SJ, et al. Granulocyte-macrophage progenitors as candidate leukemic stem cells in blast-crisis CML. N Engl J Med. 2004;351(7):657-667. (Pubitemid 39063268)
40. Jiang X, Saw KM, Eaves A, Eaves C. Instability of BCR-ABL gene in primary and cultured chronic myeloid leukemia stem cells. J Natl Cancer Inst. 2007;99(9):680-693. (Pubitemid 47073530)
41. Johansson B, Fioretos T, Mitelman F. Cytogenetic and molecular genetic evolution of chronic myeloid leukemia. Acta Haematol. 2002;107(2):76-94. (Pubitemid 34264171)
42. Perez-Caro M, Cobaleda C, Gonzalez-Herrero I, et al. Cancer induction by restriction of oncogene expression to the stem cell compartment. EMBO J. 2009;28(1):8-20.
43. Worrillow LJ, Allan JM. Deregulation of homologous recombination DNA repair in alkylating agent-treated stem cell clones: a possible role in the aetiology of chemotherapy-induced leukaemia. Oncogene. 2006;25(12):1709-1720.
44. Jorgensen HG, Copland M, Allan EK, et al. Intermittent exposure of primitive quiescent chronic myeloid leukemia cells to granulocyte-colony stimulating factor in vitro promotes their elimination by imatinib mesylate. Clin Cancer Res. 2006;12(2):626-633. (Pubitemid 43166158)
45. Konig H, Copland M, Chu S, Jove R, Holyoake TL, Bhatia R. Effects of dasatinib on SRC kinase activity and downstream intracellular signaling in primitive chronic myelogenous leukemia hematopoietic cells. Cancer Res. 2008;68(23):9624-9633.
46. Nomme J, Takizawa Y, Martinez SF, et al. Inhibition of filament formation of human Rad51 protein by a small peptide derived from the BRC-motif of the BRCA2 protein. Genes Cells. 2008;13(5):471-481. (Pubitemid 351567048)
47. Ishida T, Takizawa Y, Kainuma T, et al. DIDS, a chemical compound that inhibits RAD51-mediated homologous pairing and strand exchange. Nucleic Acids Res. 2009;37(10):3367-3376.
48. Martinez SF, Renodon-Corniere A, Nomme J, et al. Targeting human Rad51 by specific DNA aptamers induces inhibition of homologous recombination. Biochimie. 2010;92(12):1832-1838.
49. Sonoda E, Sasaki MS, Buerstedde JM, et al. Rad51-deficient vertebrate cells accumulate chromosomal breaks prior to cell death. EMBO J. 1998;17:598-608. (Pubitemid 28045499)
50. Urena DE, Zhang Z, Tsai YC, Wang YZ, Chen J. From strand exchange to branch migration: bypassing of nonhomologous sequences by human Rad51 and Rad54. J Mol Biol. 2011;405(1):77-91.