Homologous recombination as a resistance mechanism to replication-induced double-strand breaks caused by the antileukemia agent CNDAC

Blood

Volumn 116, Issue 10, 2010, Pages 1737-1746

  Liu, Xiaojun ^a   Wang, Yaqing ^a   Benaissa, Sherri ^a   Matsuda, Akira ^b   Kantarjian, Hagop ^a   Estrov, Zeev ^a   Plunkett, William ^a  

^a UNIVERSITY OF TEXAS   (United States)

^b HOKKAIDO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

2'-CYANO-2'-DEOXYARABINOFURANOSYLCYTOSINE; CYTARABINE; SINGLE STRANDED DNA;

ADOLESCENT; ADULT; AGED; ANALOGS AND DERIVATIVES; ANIMAL; CELL LINE; CELL SURVIVAL; CHO CELL LINE; CRICETULUS; DNA REPLICATION; DOUBLE STRANDED DNA BREAK; DRUG EFFECTS; DRUG RESISTANCE; FEMALE; GENETIC RECOMBINATION; GENETICS; HAMSTER; HCT116 CELL LINE; HELA CELL LINE; HUMAN; LEUKEMIA, MYELOID, ACUTE; MALE; MIDDLE AGED; PATHOLOGY; SISTER CHROMATID EXCHANGE; TUMOR CELL LINE; VERY ELDERLY; YOUNG ADULT;

ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; ANIMALS; CELL LINE; CELL LINE, TUMOR; CELL SURVIVAL; CHO CELLS; CRICETINAE; CRICETULUS; CYTARABINE; DNA BREAKS, DOUBLE-STRANDED; DNA REPLICATION; DNA, SINGLE-STRANDED; DRUG RESISTANCE; FEMALE; HCT116 CELLS; HELA CELLS; HUMANS; LEUKEMIA, MYELOID, ACUTE; MALE; MIDDLE AGED; RECOMBINATION, GENETIC; SISTER CHROMATID EXCHANGE; YOUNG ADULT;

EID: 77956597288     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2009-05-220376     Document Type: Article

References (46)

1. Kantarjian H, Garcia-Manero G, O'Brien S, et al. Phase I clinical and pharmacokinetic study of oral sapacitabine in patients with acute leukemia and myelodysplastic syndrome. J Clin Oncol. 2010;28(2):285-291.
2. Sankhala K, Takimoto CH, Mita AC, et al. Two phase I, pharmacokinetic (PK) and pharmacodynamic (PD) studies of TAS-109, a novel nucleoside analogue with 14 days and 7 days continuous infusion schedules. Proc Am Soc Clin Oncol. 2008;26(15S). Abstract 2577.
3. Azuma A, Huang P, Matsuda A, Plunkett W. Cellular pharmacokinetics and pharmacodynamics of the deoxycytidine analog 2′-C-cyano-2′-deoxy-1- beta-D-arabino-pentofuranosylcytosine (CNDAC). Biochem Pharmacol. 2001;61(12):1497-1507. (Pubitemid 32479202)
4. Hanaoka K, Suzuki M, Kobayashi T, et al. Antitumor activity and novel DNA-self-strand-breaking mechanism of CNDAC (1-(2-C-cyano-2-deoxybeta-D-arabino- pentofuranosyl) cytosine) and its N4-palmitoyl derivative (CS-682). Int J Cancer. 1999;82(2):226-236.
5. Hayakawa Y, Kawai R, Otsuki K, Kataoka M, Matsuda A. Evidence supporting the activity of 2′-C-cyano-2′-deoxy-1-beta-D-arabino- pentafuranosylcytosine as a terminator in enzymatic DNA-chain elongation. Bioorg Med Chem Lett. 1998;8(18):2559-2562. (Pubitemid 28546771)
6. Matsuda A, Nakajima Y, Azuma A, Tanaka M, Sasaki T. Nucleosides and nucleotides. 100. 2′-C-cyano-2′-deoxy-1-beta-D-arabinofuranosyl- cytosine (CNDAC): design of a potential mechanism-based DNA-strand-breaking antineoplastic nucleoside. J Med Chem. 1991;34(9):2917-2919.
7. Azuma A, Huang P, Matsuda A, Plunkett W. 2′-Ccyano-2′-deoxy- 1-beta-D-arabino-pentofuranosylcytosine: a novel anticancer nucleoside analog that causes both DNA strand breaks and G(2) arrest. Mol Pharmacol. 2001;59(4):725-731.
8. Helleday T, Lo J, van Gent DC, Engelward BP. DNA double-strand break repair: from mechanistic understanding to cancer treatment. DNA Repair (Amst). 2007;6(7):923-935.
9. Arnaudeau C, Lundin C, Helleday T. DNA double-strand breaks associated with replication forks are predominantly repaired by homologous recombination involving an exchange mechanism in mammalian cells. J Mol Biol. 2001;307(5):1235-1245. (Pubitemid 33027636)
10. Strumberg D, Pilon AA, Smith M, et al. Conversion of topoisomerase I cleavage complexes on the leading strand of ribosomal DNA into 5′-phosphorylated DNA double-strand breaks by replication runoff. Mol Cell Biol. 2000;20(11):3977-3987.
11. San Filippo J, Sung P, Klein H. Mechanism of eukaryotic homologous recombination. Annu Rev Biochem. 2008;77:229-257.
12. Lieber MR. The mechanism of human nonhomologous DNA end joining. J Biol Chem. 2008;283(1):1-5.
13. Drouet J, Frit P, Delteil C, et al. Interplay between Ku, Artemis, and the DNA-dependent protein kinase catalytic subunit at DNA ends. J Biol Chem. 2006;281(38):27784-27793.
14. Meek K, Gupta S, Ramsden DA, Lees-Miller SP. The DNA-dependent protein kinase: the director at the end. Immunol Rev. 2004;200:132-141. (Pubitemid 38998198)
15. Nussenzweig A, Chen C, da Costa Soares V, et al. Requirement for Ku80 in growth and immunoglobulin V(D)J recombination. Nature. 1996;382(6591):551-555.
16. Bakkenist CJ, Kastan MB. DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature. 2003;421(6922):499-506.
17. 2. EMBO J. 2009;28(21):3413-3427.
18. Morrison C, Sonoda E, Takao N, et al. The controlling role of ATM in homologous recombinational repair of DNA damage. EMBO J. 2000;19(3):463-471.
19. Brown EJ, Baltimore D. Essential and dispensable roles of ATR in cell cycle arrest and genome maintenance. Genes Dev. 2003;17(5):615-628. (Pubitemid 36307546)
20. Wang Y, Liu X, Matsuda A, Plunkett W. Repair of 2′-C-cyano- 2′-deoxy-1-beta-D-arabino-pentofuranosylcytosine-induced DNA single-strand breaks by transcription-coupled nucleotide excision repair. Cancer Res. 2008;68(10):3881-3889.
21. 2 arrest induced by 2′-C-cyano-2′-deoxy-1-beta-Darabino- pentofuranosylcytosine and consequences of checkpoint abrogation. Cancer Res. 2005;65(15):6874-6881.
22. Yamauchi T, Nowak BJ, Keating MJ, Plunkett W. DNA repair initiated in chronic lymphocytic leukemia lymphocytes by 4-hydroperoxycyclophosphamide is inhibited by fludarabine and clofarabine. Clin Cancer Res. 2001;7(11):3580-3589.
23. Ewald B, Sampath D, Plunkett W. ATM and the Mre11-Rad50-Nbs1 complex respond to nucleoside analogue-induced stalled replication forks and contribute to drug resistance. Cancer Res. 2008;68(19):7947-7955.
24. Moufarij MA, Sampath D, Keating MJ, Plunkett W. Fludarabine increases oxaliplatin cytotoxicity in normal and chronic lymphocytic leukemia lymphocytes by suppressing interstrand DNA crosslink removal. Blood. 2006;108(13):4187-4193.
25. Wang X, Zou L, Lu T, et al. Rad17 phosphorylation is required for claspin recruitment and Chk1 activation in response to replication stress. Mol Cell. 2006;23(3):331-341. (Pubitemid 44128854)
26. Sampath D, Cortes J, Estrov Z, et al. Pharmacodynamics of cytarabine alone and in combination with 7-hydroxystaurosporine (UCN-01) in AML blasts in vitro and during a clinical trial. Blood. 2006;107(6):2517-2524.
27. Azuma A, Hanaoka K, Kurihara A, et al. Nucleosides and nucleotides. 141. Chemical stability of a new antitumor nucleoside, 2′-C-cyano-2′- deoxy-1-beta-D-arabino-pentofuranosylcytosine in alkaline medium: formation of 2′-C-cyano-2′-deoxy-1-beta-D-ribo-pentofuranosylcytosine and its antitumor activity. J Med Chem. 1995;38(17):3391-3397.
28. Pilch DR, Sedelnikova OA, Redon C, et al. Characteristics of gamma-H2AX foci at DNA doublestrand breaks sites. Biochem Cell Biol. 2003;81(3):123-129.
29. Rogakou EP, Pilch DR, Orr AH, Ivanova VS, Bonner WM. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J Biol Chem. 1998;273(10):5858-5868.
30. Kunugi KA, Vazquez-Padua MA, Miller EM, Kinsella TJ. Modulation of IdUrd-DNA incorporation and radiosensitization in human bladder carcinoma cells. Cancer Res. 1990;50(16):4962-4967.
31. Lees-Miller SP, Godbout R, Chan DW, et al. Absence of p350 subunit of DNA-activated protein kinase from a radiosensitive human cell line. Science. 1995;267(5201):1183-1185.
32. Feldmann E, Schmiemann V, Goedecke W, Reichenberger S, Pfeiffer P. DNA double-strand break repair in cell-free extracts from Ku80-deficient cells: implications for Ku serving as an alignment factor in non-homologous DNA end joining. Nucleic Acids Res. 2000;28(13):2585-2596. (Pubitemid 30420858)
33. Jazayeri A, Falck J, Lukas C, et al. ATM- and cell cycle-dependent regulation of ATR in response to DNA double-strand breaks. Nat Cell Biol. 2006;8(1):37-45.
34. Shiotani B, Zou L. Single-stranded DNA orchestrates an ATM-to-ATR switch at DNA breaks. Mol Cell. 2009;33(5):547-558.
35. Thompson LH, Schild D. Homologous recombinational repair of DNA ensures mammalian chromosome stability. Mutat Res. 2001;477(1):131-153. (Pubitemid 32480197)
36. Pierce AJ, Johnson RD, Thompson LH, Jasin M. XRCC3 promotes homology-directed repair of DNA damage in mammalian cells. Genes Dev. 1999;13(20):2633-2638. (Pubitemid 29508550)
37. Orelli BJ, Bishop DK. BRCA2 and homologous recombination. Breast Cancer Res. 2001;3(5):294-298.
38. Wilson DM 3rd, Thompson LH. Molecular mechanisms of sister-chromatid exchange. Mutat Res. 2007;616(1):11-23.
39. Kufe DW, Major PP, Egan EM, Beardsley GP. Correlation of cytotoxicity with incorporation of ara-C into DNA. J Biol Chem. 1980;255(19):8997-9000.
40. Ewald B, Sampath D, Plunkett W. Nucleoside analogs: molecular mechanisms signaling cell death. Oncogene. 2008;27(50):6522-6537.
41. 2 checkpoint activation by the DNA strand-breaking nucleoside analogue 2′-C-cyano-2′-deoxy-1- beta-D-arabino-pentofuranosylcytosine. Mol Cancer Ther. 2008;7(1):133-142.
42. Tsimberidou AM, Tam C, Abruzzo LV, et al. Chemoimmunotherapy may overcome the adverse prognostic significance of 11q deletion in previously untreated patients with chronic lymphocytic leukemia. Cancer. 2009;115(2):373-380.
43. Austen B, Skowronska A, Baker C, et al. Mutation status of the residual ATM allele is an important determinant of the cellular response to chemotherapy and survival in patients with chronic lymphocytic leukemia containing an 11q deletion. J Clin Oncol. 2007;25(34):5448-5457.
44. Cohn MA, D'Andrea AD. Chromatin recruitment of DNA repair proteins: lessons from the Fanconi anemia and double-strand break repair pathways. Mol Cell. 2008;32(3):306-312.
45. Scardocci A, Guidi F, D'Alo F, et al. Reduced BRCA1 expression due to promoter hypermethylation in therapy-related acute myeloid leukaemia. Br J Cancer. 2006;95(8):1108-1113.
46. Golding SE, Rosenberg E, Valerie N, et al. Improved ATM kinase inhibitor KU-60019 radiosensitizes glioma cells, compromises insulin, AKT and ERK prosurvival signaling, and inhibits migration and invasion. Mol Cancer Ther. 2009;8(10):2894-2902.