Cleavage of BCR-ABL transcripts at the T315I point mutation by DNAzyme promotes apoptotic cell death in imatinib-resistant BCR-ABL leukemic cells

Leukemia

Volumn 27, Issue 8, 2013, Pages 1650-1658

  Kim, J E ^a   Yoon, S ^a   Choi, B R ^a   Kim, K P ^a   Cho, Y H ^a,d   Jung, W ^b   Kim, D W ^c   Oh, S ^a   Kim, D E ^a  

^a Konkuk University   (South Korea)

^b The Catholic University of Korea   (South Korea)

^c Kookmin University   (South Korea)

^d Kyung Hee University College of Medicine   (South Korea)

Author keywords

BCR ABL; DNAzyme; imatinib resistance

Indexed keywords

BCR ABL PROTEIN; CASPASE 3; CASPASE 7; DEOXYRIBOZYME; IMATINIB; OLIGODEOXYRIBOZYME; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; CANCER INHIBITION; CANCER RESISTANCE; CELL CYCLE G0 PHASE; CHEMOSENSITIZATION; CONTROLLED STUDY; ENZYME INDUCTION; G1 PHASE CELL CYCLE CHECKPOINT; LEUKEMIA; LEUKEMIA CELL; MOUSE; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN CLEAVAGE; WILD TYPE;

ANIMALS; APOPTOSIS; BASE PAIRING; BASE SEQUENCE; BENZAMIDES; CATALYSIS; CELL LINE, TUMOR; CELL SURVIVAL; DNA, CATALYTIC; DRUG RESISTANCE, NEOPLASM; FUSION PROTEINS, BCR-ABL; GENE EXPRESSION REGULATION, LEUKEMIC; LEUKEMIA, MYELOGENOUS, CHRONIC, BCR-ABL POSITIVE; MICE; PIPERAZINES; POINT MUTATION; PYRIMIDINES; TRANSCRIPTION, GENETIC;

EID: 84881474517     PISSN: 08876924     EISSN: 14765551     Source Type: Journal    
DOI: 10.1038/leu.2013.60     Document Type: Article

References (49)

1. Daley GQ, Van Etten RA, Baltimore D. Induction of chronic myelogenous leukemia in mice by the P210bcr/abl gene of the Philadelphia chromosome. Science 1990; 247: 824-830.
2. Faderl S, Talpaz M, Estrov Z, O'Brien S, Kurzrock R, Kantarjian HM. The biology of chronic myeloid leukemia. N Engl J Med 1999; 341: 164-172. (Pubitemid 29325745)
3. Rowley JD. Letter: A new consistent chromosomal abnormality in chronic mye-logenous leukaemia identified by quinacrine fluorescence and Giemsa staining. Nature 1973; 243: 290-293.
4. Groffen J, Stephenson JR, Heisterkamp N, de Klein A, Bartram CR, Grosveld G. Philadelphia chromosomal breakpoints are clustered within a limited region, bcr, on chromosome 22. Cell 1984; 36: 93-99. (Pubitemid 14155374)
5. Shepherd P, Suffolk R, Halsey J, Allan N. Analysis of molecular breakpoint and m-RNA transcripts in a prospective randomized trial of interferon in chronic myeloid leukaemia: no correlation with clinical features, cytogenetic response, duration of chronic phase, or survival. Br J Haematol 1995; 89: 546-554.
6. Goldman JM, Melo JV. Chronic myeloid leukemia-advances in biology and new approaches to treatment. N Engl J Med 2003; 349: 1451-1464. (Pubitemid 37211061)
7. Cortez D, Reuther G, Pendergast AM. The Bcr-Abl tyrosine kinase activates mitogenic signaling pathways and stimulates G1-to-S phase transition in hematopoietic cells. Oncogene 1997; 15: 2333-2342. (Pubitemid 27496983)
8. Gesbert F, Sellers WR, Signoretti S, Loda M, Griffin JD. BCR/ABL regulates expression of the cyclin-dependent kinase inhibitor p27Kip1 through the phos-phatidylinositol 3-Kinase/AKT pathway. J Biol Chem 2000; 275: 39223-39230. (Pubitemid 32058940)
9. Nimmanapalli R, Fuino L, Bali P, Gasparetto M, Glozak M, Tao J et al. Histone deacetylase inhibitor LAQ824 both lowers expression and promotes proteasomal degradation of Bcr-Abl and induces apoptosis of imatinib mesylate-sensitive or-refractory chronic myelogenous leukemia-blast crisis cells. Cancer Res 2003; 63: 5126-5135. (Pubitemid 37022654)
10. Dubrez L, Eymin B, Sordet O, Droin N, Turhan AG, Solary E. BCR-ABL delays apoptosis upstream of procaspase-3 activation. Blood 1998; 91: 2415-2422. (Pubitemid 28155516)
11. Steinberg M. Dasatinib: a tyrosine kinase inhibitor for the treatment of chronic myelogenous leukemia and philadelphia chromosome-positive acute lymphoblastic leukemia. Clin Ther 2007; 29: 2289-2308.
12. Druker BJ, Talpaz M, Resta DJ, Peng B, Buchdunger E, Ford JM et al. Efficacy and safety of a specific inhibitor of the BCR-ABL tyrosine kinase in chronic myeloid leukemia. N Engl J Med 2001; 344: 1031-1037. (Pubitemid 32267972)
13. Tsao AS, Kantarijian H, Talpaz M. STI-571 in chronic myelogenous leukaemia. Br J Haematol 2002; 119: 15-24. (Pubitemid 35176494)
14. Bradeen HA, Eide CA, O'Hare T, Johnson KJ, Willis SG, Lee FY et al. Comparison of imatinib mesylate, dasatinib (BMS-354825), and nilotinib (AMN107) in an N-ethyl-N-nitrosourea (ENU)-based mutagenesis screen: high efficacy of drug combinations. Blood 2006; 108: 2332-2338. (Pubitemid 44497517)
15. Gorre ME, Mohammed M, Ellwood K, Hsu N, Paquette R, Rao PN et al. Clinical resistance to STI-571 cancer therapy caused by BCR-ABL gene mutation or amplification. Science 2001; 293: 876-880. (Pubitemid 32743979)
16. Hughes T, Deininger M, Hochhaus A, Branford S, Radich J, Kaeda J et al. Monitoring CML patients responding to treatment with tyrosine kinase inhibitors: review and recommendations for harmonizing current methodology for detecting BCR-ABL transcripts and kinase domain mutations and for expressing results. Blood 2006; 108: 28-37. (Pubitemid 43990609)
17. von Bubnoff N, Schneller F, Peschel C, Duyster J. BCR-ABL gene mutations in relation to clinical resistance of Philadelphia-chromosome-positive leukaemia to STI571: a prospective study. Lancet 2002; 359: 487-491. (Pubitemid 34164296)
18. Talpaz M, Shah NP, Kantarjian H, Donato N, Nicoll J, Paquette R et al. Dasatinib in imatinib-resistant Philadelphia chromosome-positive leukemias. N Engl J Med 2006; 354: 2531-2541. (Pubitemid 43882349)
19. O'Hare T, Eide CA, Deininger MW. Bcr-Abl kinase domain mutations, drug resistance, and the road to a cure for chronic myeloid leukemia. Blood 2007; 110: 2242-2249. (Pubitemid 47523141)
20. Santoro SW, Joyce GF. A general purpose RNA-cleaving DNA enzyme. Proc Natl Acad Sci USA 1997; 94: 4262-4266. (Pubitemid 27194229)
21. Wu Y, Yu L, McMahon R, Rossi JJ, Forman SJ, Snyder DS. Inhibition of bcr-abl oncogene expression by novel deoxyribozymes (DNAzymes). Hum Gene Ther 1999; 10: 2847-2857.
22. Kuwabara T, Warashina M, Tanabe T, Tani K, Asano S, Taira K. Comparison of the specificities and catalytic activities of hammerhead ribozymes and DNA enzymes with respect to the cleavage of BCR-ABL chimeric L6 (b2a2) mRNA. Nucleic Acids Res 1997; 25: 3074-3081. (Pubitemid 27331401)
23. Maran A, Waller CF, Paranjape JM, Li G, Xiao W, Zhang K et al. 2', 5'-Oligoadenylate-antisense chimeras cause RNase L to selectively degrade bcr/abl mRNA in chronic myelogenous leukemia cells. Blood 1998; 92: 4336-4343. (Pubitemid 28544351)
24. Bhatia R, Verfaillie CM. Inhibition of BCR-ABL expression with antisense oligodeoxynucleotides restores beta1 integrin-mediated adhesion and proliferation inhibition in chronic myelogenous leukemia hematopoietic progenitors. Blood 1998; 91: 3414-3422. (Pubitemid 28193894)
25. Wohlbold L, van der Kuip H, Miething C, Vornlocher HP, Knabbe C, Duyster J et al. Inhibition of bcr-abl gene expression by small interfering RNA sensitizes for imatinib mesylate (STI571). Blood 2003; 102: 2236-2239. (Pubitemid 37122404)
26. Scherr M, Battmer K, Winkler T, Heidenreich O, Ganser A, Eder M. Specific inhibition of bcr-abl gene expression by small interfering RNA. Blood 2003; 101: 1566-1569. (Pubitemid 36182535)
27. Rapozzi V, Burm BE, Cogoi S, van der Marel GA, van Boom JH, Quadrifoglio F et al. Antiproliferative effect in chronic myeloid leukaemia cells by antisense peptide nucleic acids. Nucleic Acids Res 2002; 30: 3712-3721. (Pubitemid 35012443)
28. Rapozzi V, Cogoi S, Xodo LE. Antisense locked nucleic acids efficiently suppress BCR/ABL and induce cell growth decline and apoptosis in leukemic cells. Mol Cancer Ther 2006; 5: 1683-1692. (Pubitemid 44323236)
29. Jang KJ, Lee NR, Yeo WS, Jeong YJ, Kim DE. Isolation of inhibitory RNA aptamers against severe acute respiratory syndrome (SARS) coronavirus NTPase/Helicase. Biochem Biophys Res Commun 2008; 366: 738-744.
30. Kim DE, Joyce GF. Cross-catalytic replication of an RNA ligase ribozyme. Chem Biol 2004; 11: 1505-1512. (Pubitemid 39527277)
31. Lee B, Kim KB, Oh S, Choi JS, Park JS, Min DH et al. Suppression of hepatitis C virus genome replication in cells with RNA-cleaving DNA enzymes and short-hairpin RNA. Oligonucleotides 2010; 20: 285-296.
32. Kronenwett R, Haas R, Sczakiel G. Kinetic selectivity of complementary nucleic acids: bcr-abl-directed antisense RNA and ribozymes. J Mol Biol 1996; 259: 632-644. (Pubitemid 26226004)
33. Patel BB, He YA, Li XM, Frolov A, Vanderveer L, Slater C et al. Molecular mechanisms of action of imatinib mesylate in human ovarian cancer: a proteomic analysis. Cancer Genomics Proteomics 2008; 5: 137-149.
34. Chu S, Holtz M, Gupta M, Bhatia R. BCR/ABL kinase inhibition by imatinib mesylate enhances MAP kinase activity in chronic myelogenous leukemia CD34+ cells. Blood 2004; 103: 3167-3174. (Pubitemid 38451695)
35. Xu Y, Fang F, Sun St Y, Clair St DK, Clair WH. RelB-dependent differential radio-sensitization effect of STI571 on prostate cancer cells. Mol Cancer Ther 2010; 9: 803-812.
36. Matei D, Chang DD, Jeng MH. Imatinib mesylate (Gleevec) inhibits ovarian cancer cell growth through a mechanism dependent on platelet-derived growth factor receptor alpha and Akt inactivation. Clin Cancer Res 2004; 10: 681-690. (Pubitemid 38174008)
37. Klejman A, Rushen L, Morrione A, Slupianek A, Skorski T. Phosphatidylinositol-3 kinase inhibitors enhance the anti-leukemia effect of STI571. Oncogene 2002; 21: 5868-5876. (Pubitemid 35007237)
38. Quintas-Cardama A, Kantarjian H, Cortes J. Imatinib and beyond-exploring the full potential of targeted therapy for CML. Nat Rev Clin Oncol 2009; 6: 535-543.
39. La Rosee P, Deininger MW. Resistance to imatinib: mutations and beyond. Semin Hematol 2010; 47: 335-343.
40. Koldehoff M, Kordelas L, Beelen DW, Elmaagacli AH. Small interfering RNA against BCR-ABL transcripts sensitize mutated T315I cells to nilotinib. Haematologica 2010; 95: 388-397.
41. Rangatia J, Bonnet D. Transient or long-term silencing of BCR-ABL alone induces cell cycle and proliferation arrest, apoptosis and differentiation. Leukemia 2006; 20: 68-76.
42. Bueno-da-Silva AE, Brumatti G, Russo FO, Green DR, Amarante-Mendes GP. Bcr-Abl-mediated resistance to apoptosis is independent of constant tyrosine-kinase activity. Cell Death Differ 2003; 10: 592-598. (Pubitemid 36656648)
43. Kawano T, Horiguchi-Yamada J, Saito S, Iwase S, Furukawa Y, Kano Y et al. Ectopic cyclin D1 expression blocks STI571-induced erythroid differentiation of K562 cells. Leuk Res 2004; 28: 623-629. (Pubitemid 38543200)
44. Baum DA, Silverman SK. Deoxyribozymes: useful DNA catalysts in vitro and in vivo. Cell Mol Life Sci 2008; 65: 2156-2174.
45. Pun SH, Tack F, Bellocq NC, Cheng J, Grubbs BH, Jensen GS et al. Targeted delivery of RNA-cleaving DNA enzyme (DNAzyme) to tumor tissue by transferrin-modified, cyclodextrin-based particles. Cancer Biol Ther 2004; 3: 641-650. (Pubitemid 41351103)
46. Ryoo SR, Jang H, Kim KS, Lee B, Kim KB, Kim YK et al. Functional delivery of DNAzyme with iron oxide nanoparticles for hepatitis C virus gene knockdown. Biomaterials 2012; 33: 2754-2761.
47. Nunamaker EA, Zhang HY, Shirasawa Y, Benoit JN, Dean DA. Electroporation-mediated delivery of catalytic oligodeoxynucleotides for manipulation of vascular gene expression. Am J Physiol Heart Circ Physiol 2003; 285: H2240-H2247. (Pubitemid 37305971)
48. Morgan RA, Anderson WF. Human gene therapy. Annu Rev Biochem 1993; 62: 191-217. (Pubitemid 23237870)
49. Grubbs RD. Intracellular magnesium and magnesium buffering. Biometals 2002; 15: 251-259. (Pubitemid 34816209)