Genomic instability in chronic myeloid leukemia: Targets for therapy?

Current Hematologic Malignancy Reports

Volumn 7, Issue 2, 2012, Pages 94-102

  Muvarak, N ^a   Nagaria, P ^a   Rassool, F V ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

BCR ABL; Chronic myeloid leukemia; CML .DNA repair; Genomic instability; Imatinib resistance; NHEJ; ROS; Therapeutic targets; Therapy

Indexed keywords

ADVANCED CANCER; ARTICLE; BLAST TRANSFORMATION; CHRONIC MYELOID LEUKEMIA; DNA DAMAGE; DNA REPAIR; GENOMIC INSTABILITY; HUMAN; LEUKEMOGENESIS; NONHUMAN; PHILADELPHIA 1 CHROMOSOME;

CELL TRANSFORMATION, NEOPLASTIC; DISEASE PROGRESSION; DNA DAMAGE; GENOMIC INSTABILITY; HUMANS; LEUKEMIA, MYELOGENOUS, CHRONIC, BCR-ABL POSITIVE; MOLECULAR TARGETED THERAPY; REACTIVE OXYGEN SPECIES;

EID: 84860829034     PISSN: 15588211     EISSN: 1558822X     Source Type: Journal    
DOI: 10.1007/s11899-012-0119-0     Document Type: Article

References (84)

1. Guilhot F, Apperley J, Kim DW, et al. Dasatinib induces significant hematologic and cytogenetic responses in patients with imatinib-resistant or -intolerant chronic myeloid leukemia in accelerated phase. Blood. 2007;109:4143-50. (Pubitemid 46743375)
2. Melo JV, Deininger MW. Biology of chronic myelogenous leukemia-signaling pathways of initiation and transformation. Hematol Oncol Clin North Am. 2004;18:545-68. vii-viii. (Pubitemid 38969131)
3. Collins SJ, Groudine MT. Chronic myelogenous leukemia: amplification of a rearranged c-abl oncogene in both chronic phase and blast crisis. Blood. 1987;69:893-8. (Pubitemid 17057474)
4. Johansson B, Fioretos T, Mitelman F. Cytogenetic and molecular genetic evolution of chronic myeloid leukemia. Acta Haematol. 2002;107:76-94. (Pubitemid 34264171)
5. Elder PT, McMullin MF, Humphreys MW, et al. The finding of a reciprocal whole-arm translocation t (X;12) (p10;p10) in association with atypical chronic myeloid leukaemia. Med Oncol. 2010;27:760-2.
6. Kolomietz E, Al-Maghrabi J, Brennan S, et al. Primary chromosomal rearrangements of leukemia are frequently accompanied by extensive submicroscopic deletions and may lead to altered prognosis. Blood. 2001;97:3581-8.
7. Stuppia L, Calabrese G, Peila R, et al. p53 loss and point mutations are associated with suppression of apoptosis and progression of CML into myeloid blastic crisis. Cancer Genet Cytogenet. 1997;98:28-35. (Pubitemid 27400849)
8. Sadamori N, Matsunaga M, Yao E, et al. Chromosomal characteristics of chronic and blastic phases of Ph-positive chronic myeloid leukemia. Cancer Genet Cytogenet. 1985;15:17-24. (Pubitemid 15164019)
9. Becher R, Carbonell F, Bartram CR. Isochromosome 17q in Ph1- negative leukemia: a clinical, cytogenetic, and molecular study. Blood. 1990;75:1679-83. (Pubitemid 20145756)
10. Collins S, Groudine M. Amplification of endogenous myc-related DNA sequences in a human myeloid leukaemia cell line. Nature. 1982;298:679-81. (Pubitemid 12099731)
11. O'Brien SG, Guilhot F, Larson RA, et al. Imatinib compared with interferon and low-dose cytarabine for newly diagnosed chronicphase chronic myeloid leukemia. N Engl J Med. 2003;348:994-1004. (Pubitemid 36302244)
12. Santos FP, Kantarjian H, Quintas-Cardama A, Cortes J. Evolution of therapies for chronic myelogenous leukemia. Cancer J. 2011;17:465-76.
13. Soverini S, Gnani A, Colarossi S, et al. Philadelphia-positive patients who already harbor imatinib-resistant Bcr-Abl kinase domain mutations have a higher likelihood of developing additional mutations associated with resistance to second- or third-line tyrosine kinase inhibitors. Blood. 2009;114:2168-71. This important study indicates that Ph+ patients already harboring BCR-ABL mutations that lead to imatinib resistance have a higher likelihood of relapse associated with development of further mutations resistant to second-line or third-line TKIs, compared with patients who do not harbor mutations..
14. Pfeifer H, Wassmann B, Pavlova A, et al. Kinase domain mutations of BCR-ABL frequently precede imatinib-based therapy and give rise to relapse in patients with de novo Philadelphia-positive acute lymphoblastic leukemia (Ph+ ALL). Blood. 2007;110:727-34. (Pubitemid 47108165)
15. Wang JY. DNA damage and apoptosis. Cell Death Differ. 2001;8:1047-8. (Pubitemid 33061821)
16. Willman C, Hromas RA. Genomic alterations and chromosomal aberrations in human cancer. In: Kufe DW, Holland JF, Frei E, editors. Cancer medicine. London: BC Decker Inc; 2006. p. 104-34. 17.
17. Popp HD, Bohlander SK. Genetic instability in inherited and sporadic leukemias. Genes Chromosomes Cancer. 2010;49:1071- 81.
18. Giehl M, Fabarius A, Frank O, et al. Centrosome aberrations in chronic myeloid leukemia correlate with stage of disease and chromosomal instability. Leukemia. 2005;19:1192-7. (Pubitemid 40946003)
19. Wada C, Shionoya S, Fujino Y, et al. Genomic instability of microsatellite repeats and its association with the evolution of chronic myelogenous leukemia. Blood. 1994;83:3449-56.
20. Rai R, Zheng H, He H, et al. The function of classical and alternative non-homologous end-joining pathways in the fusion of dysfunctional telomeres. EMBO J. 2010;29:2598-610.
21. Sallmyr A, Fan J, Rassool FV. Genomic instability in myeloid malignancies: increased reactive oxygen species (ROS), DNA double strand breaks (DSBs) and error-prone repair. Cancer Lett. 2008;270:1-9.
22. Canitrot Y, Lautier D, Laurent G, et al. Mutator phenotype of BCR-ABL transfected Ba/F3 cell lines and its association with enhanced expression of DNA polymerase beta. Oncogene. 1999;18:2676-80. (Pubitemid 29237655)
23. Stoklosa T, Poplawski T, Koptyra M, et al. BCR/ABL inhibits mismatch repair to protect from apoptosis and induce point mutations. Cancer Res. 2008;68:2576-80. (Pubitemid 351556254)
24. Burke BA, Carroll M. BCR-ABL: a multi-faceted promoter of DNA mutation in chronic myelogeneous leukemia. Leukemia. 2010;24:1105-12.
25. Negrini S, Gorgoulis VG, Halazonetis TD. Genomic instability-an evolving hallmark of cancer. Nat RevMol Cell Biol. 2010;11:220-8.
26. Fialkow PJ, Martin PJ, Najfeld V, et al. Evidence for a multistep pathogenesis of chronic myelogenous leukemia. Blood. 1981;58:158-63. (Pubitemid 11064473)
27. O'Dwyer ME, Gatter KM, Loriaux M, et al. Demonstration of Philadelphia chromosome negative abnormal clones in patients with chronic myelogenous leukemia during major cytogenetic responses induced by imatinib mesylate. Leukemia. 2003;17:481-7. (Pubitemid 36395639)
28. Brady N, Gaymes TJ, Cheung M, et al. Increased error-prone NHEJ activity in myeloid leukemias is associated with DNA damage at sites that recruit key nonhomologous end-joining proteins. Cancer Res. 2003;63:1798-805. (Pubitemid 36460840)
29. 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;62:2791-7. (Pubitemid 34525762)
30. Sallmyr A, Tomkinson AE, Rassool FV. Up-regulation of WRN and DNA ligase IIIalpha in chronic myeloid leukemia: consequences for the repair of DNA double-strand breaks. Blood. 2008;112:1413-23.
31. Salloukh HF, Laneuville P. Increase in mutant frequencies in mice expressing the BCR-ABL activated tyrosine kinase. Leukemia. 2000;14:1401-4. (Pubitemid 30599320)
32. Voncken JW, Kaartinen V, Pattengale PK, et al. BCR/ABL P210 and P190 cause distinct leukemia in transgenic mice. Blood. 1995;86:4603-11.
33. Dierov J, Sanchez PV, Burke BA, et al. BCR/ABL induces chromosomal instability after genotoxic stress and alters the cell death threshold. Leukemia. 2009;23:279-86.
34. Melo JV, Barnes DJ. Chronic myeloid leukaemia as a model of disease evolution in human cancer. Nat Rev Cancer. 2007;7:441-53. (Pubitemid 46823444)
35. Sattler M, Verma S, Shrikhande G, et al. The BCR/ABL tyrosine kinase induces production of reactive oxygen species in hematopoietic cells. J Biol Chem. 2000;275:24273-8. (Pubitemid 30626515)
36. Nowicki MO, Falinski R, Koptyra M, et al. BCR/ABL oncogenic kinase promotes unfaithful repair of the reactive oxygen speciesdependent DNA double-strand breaks. Blood. 2004;104:3746-53. (Pubitemid 39564453)
37. Koptyra M, Falinski R, Nowicki MO, et al. BCR/ABL kinase induces self-mutagenesis via reactive oxygen species to encode imatinib resistance. Blood. 2006;108:319-27. (Pubitemid 43990645)
38. Tarumoto T, Nagai T, Ohmine K, et al. Ascorbic acid restores sensitivity to imatinib via suppression of Nrf2-dependent gene expression in the imatinib-resistant cell line. Exp Hematol. 2004;32:375-81. (Pubitemid 38410914)
39. Bedard K, Krause KH. The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev. 2007;87:245-313. (Pubitemid 46209993)
40. Kim JH, Chu SC, Gramlich JL, et al. Activation of the PI3K/ mTOR pathway by BCR-ABL contributes to increased production of reactive oxygen species. Blood. 2005;105:1717-23. (Pubitemid 40223695)
41. Naughton R, Quiney C, Turner SD, Cotter TG. Bcr-Abl-mediated redox regulation of the PI3K/AKT pathway. Leukemia. 2009;23:1432-40. This study demonstrates for the first time that Bcr-Abl-induced ROS increase survival signaling through the PI3K/AKT pathway..
42. Abraham RT. Cell cycle checkpoint signaling through the ATM and ATR kinases. Genes Dev. 2001;15:2177-96. (Pubitemid 32843830)
43. Dierov J, Dierova R, Carroll M. BCR/ABL translocates to the nucleus and disrupts an ATR-dependent intra-S phase checkpoint. Cancer Cell. 2004;5:275-85. (Pubitemid 38402119)
44. Bae I, Rih JK, Kim HJ, et al. BRCA1 regulates gene expression for orderly mitotic progression. Cell Cycle. 2005;4:1641-66.
45. Wang RH, Yu H, Deng CX. A requirement for breast-cancerassociated gene 1 (BRCA1) in the spindle checkpoint. Proc Natl Acad Sci U S A. 2004;101:17108-13. (Pubitemid 39627782)
46. Deutsch E, Jarrousse S, Buet D, et al. Down-regulation of BRCA1 in BCR-ABL-expressing hematopoietic cells. Blood. 2003;101:4583-8. (Pubitemid 36857831)
47. Wolanin K, Magalska A, Kusio-Kobialka M, et al. Expression of oncogenic kinase Bcr-Abl impairs mitotic checkpoint and promotes aberrant divisions and resistance to microtubule-targeting agents. Mol Cancer Ther. 2010;9:1328-38.
48. Shah JV, Cleveland DW. Waiting for anaphase: Mad2 and the spindle assembly checkpoint. Cell. 2000;103:997-1000. (Pubitemid 32037387)
49. Valeri A, Alonso-Ferrero ME, Rio P, et al. Bcr/Abl interferes with the Fanconi anemia/BRCA pathway: implications in the chromosomal instability of chronic myeloid leukemia cells. PLoS One. 2010;5:e15525. This study demonstrates for the first time that BCR-ABL can disrupt the Fanconi anemia/BRCA pathway, leading to an increase in chromosomal aberrations.
50. D'Andrea AD, Grompe M. The Fanconi anaemia/BRCA pathway. Nat Rev Cancer. 2003;3:23-34. (Pubitemid 37328884)
51. Helleday T, Lo J, van Gent DC, Engelward BP. DNA doublestrand break repair: from mechanistic understanding to cancer treatment. DNA Repair (Amst). 2007;6:923-35. (Pubitemid 46880473)
52. Hartlerode AJ, Scully R. Mechanisms of double-strand break repair in somatic mammalian cells. Biochem J. 2009;423:157-68.
53. Khanna KK, Jackson SP. DNA double-strand breaks: signaling, repair and the cancer connection. Nat Genet. 2001;27:247-54. (Pubitemid 32201842)
54. Keller KL, Overbeck-Carrick TL, Beck DJ. Survival and induction of SOS in Escherichia coli treated with cisplatin, UV-irradiation, or mitomycin C are dependent on the function of the RecBC and RecFOR pathways of homologous recombination. Mutat Res. 2001;486:21-9. (Pubitemid 32441821)
55. Lieber MR. The mechanism of human nonhomologous DNA end joining. J Biol Chem. 2008;283:1-5.
56. Lieber MR, Ma Y, Pannicke U, Schwarz K. Mechanism and regulation of human non-homologous DNA end-joining. Nat Rev Mol Cell Biol. 2003;4:712-20. (Pubitemid 37082186)
57. Slupianek A, Schmutte C, Tombline G, et al. BCR/ABL regulates mammalian RecA homologs, resulting in drug resistance. Mol Cell. 2001;8:795-806. (Pubitemid 33030213)
58. Martin RW, Orelli BJ, Yamazoe M, et al. RAD51 up-regulation bypasses BRCA1 function and is a common feature of BRCA1- deficient breast tumors. Cancer Res. 2007;67:9658-65. (Pubitemid 47621212)
59. Slupianek A, Dasgupta Y, Ren SY, et al. Targeting RAD51 phosphotyrosine-315 to prevent unfaithful recombination repair in BCR-ABL1 leukemia. Blood. 2011;118:1062-8.
60. Weinstock DM, Richardson CA, Elliott B, Jasin M. Modeling oncogenic translocations: distinct roles for double-strand break repair pathways in translocation formation in mammalian cells. DNA Repair (Amst). 2006;5:1065-74. (Pubitemid 44291619)
61. Fernandes MS, Reddy MM, Gonneville JR, et al. BCR-ABL promotes the frequency of mutagenic single-strand annealing DNA repair. Blood. 2009;114:1813-9.
62. Jin S, Weaver DT. Double-strand break repair by Ku70 requires heterodimerization with Ku80 and DNA binding functions. EMBO J. 1997;16:6874-85. (Pubitemid 27503498)
63. Lees-Miller SP, Chen YR, Anderson CW. Human cells contain aDNA-activated protein kinase that phosphorylates simian virus 40 T antigen, mouse p53, and the human Ku autoantigen. Mol Cell Biol. 1990;10:6472-81. (Pubitemid 120004591)
64. Ahnesorg P, Smith P, Jackson SP. XLF interacts with the XRCC4- DNA ligase IV complex to promote DNA nonhomologous endjoining. Cell. 2006;124:301-13. (Pubitemid 43121979)
65. Buck D, Malivert L, de Chasseval R, et al. Cernunnos, a novel nonhomologous end-joining factor, is mutated in human immunodeficiency with microcephaly. Cell. 2006;124:287-99. (Pubitemid 43121978)
66. Nussenzweig A, Nussenzweig MC. A backup DNA repair pathway moves to the forefront. Cell. 2007;131:223-5.
67. Deutsch E,DugrayA,AbdulKarimB, et al. BCR-ABL down-regulates the DNA repair protein DNA-PKcs. Blood. 2001;97:2084-90.
68. Slupianek A, Poplawski T, Jozwiakowski SK, et al. BCR/ABL stimulates WRN to promote survival and genomic instability. Cancer Res. 2011;71:842-51.
69. Canitrot Y, Laurent G, Astarie-Dequeker C, et al. Enhanced expression and activity of DNA polymerase beta in chronic myelogenous leukemia. Anticancer Res. 2006;26:523-5. (Pubitemid 43206009)
70. Canitrot Y, Falinski R, Louat T, et al. p210 BCR/ABL kinase regulates nucleotide excision repair (NER) and resistance to UV radiation. Blood. 2003;102:2632-7. (Pubitemid 37193605)
71. Sliwinski T, Czechowska A, Szemraj J, et al. STI571 reduces NER activity in BCR/ABL-expressing cells. Mutat Res. 2008;654:162-7.
72. Quintas-Cardama A, Kantarjian HM, Cortes JE. Mechanisms of primary and secondary resistance to imatinib in chronic myeloid leukemia. Cancer Control. 2009;16:122-31.
73. Hole PS, Darley RL, Tonks A. Do reactive oxygen species play arole in myeloid leukemias? Blood. 2011;117:5816-26.
74. Mochizuki T, Furuta S, Mitsushita J, et al. Inhibition of NADPH oxidase 4 activates apoptosis via the AKT/apoptosis signalregulating kinase 1 pathway in pancreatic cancer PANC-1 cells. Oncogene. 2006;25:3699-707. (Pubitemid 43980491)
75. Itoh K, Chiba T, Takahashi S, et al. An Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements. Biochem Biophys Res Commun. 1997;236:313-22. (Pubitemid 27373291)
76. Bonovolias ID, Tsiftsoglou AS. Hemin counteracts the repression of Bcl-2 and NrF2 genes and the cell killing induced by imatinib in human Bcr-Abl (+) CML cells. Oncol Res. 2009;17:535-47.
77. Mayerhofer M, Florian S, Krauth MT, et al. Identification of heme oxygenase-1 as a novel BCR/ABL-dependent survival factor in chronic myeloid leukemia. Cancer Res. 2004;64:3148-54. (Pubitemid 38581416)
78. Mayerhofer M, Gleixner KV, Mayerhofer J, et al. Targeting of heat shock protein 32 (Hsp32)/heme oxygenase-1 (HO-1) in leukemic cells in chronic myeloid leukemia: a novel approach to overcome resistance against imatinib. Blood. 2008;111:2200-10. (Pubitemid 351451534)
79. Larson RA, Wang Y, Banerjee M, et al. Prevalence of the inactivating 609C->T polymorphism in the NAD (P)H:quinone oxidoreductase (NQO1) gene in patients with primary and therapyrelated myeloid leukemia. Blood. 1999;94:803-7. (Pubitemid 29323895)
80. Winger JA, Hantschel O, Superti-Furga G, Kuriyan J. The structure of the leukemia drug imatinib bound to human quinine reductase 2 (NQO2). BMC Struct Biol. 2009;9:7.
81. Rassool FV, Tomkinson AE. Targeting abnormal DNA double strand break repair in cancer. Cell Mol Life Sci. 2010;67:3699-710.
82. Nelson EA, Walker SR, Weisberg E, et al. The STAT5 inhibitor pimozide decreases survival of chronic myelogenous leukemia cells resistant to kinase inhibitors. Blood. 2011;117:3421-9.
83. Poplawski T, Blasiak J. BCR/ABL downregulates DNA-PK (CS)- dependent and upregulates backup non-homologous end joining in leukemic cells. Mol Biol Rep. 2010;37:2309-15.
84. Tobin LA, Robert C, Nagaria P, et al. Targeting abnormal DNA repair in therapy-resistant breast cancers. Mol Cancer Res. 2012;10 (1):96-107.