Sensitive detection of BCR-ABL1 mutations in patients with chronic myeloid leukemia after imatinib resistance is predictive of outcome during subsequent therapy

Journal of Clinical Oncology

Volumn 29, Issue 32, 2011, Pages 4250-4259

  Parker, Wendy T ^a   Lawrence, Rebecca M ^a   Ho, Musei ^a   Irwin, Darryl L ^c   Scott, Hamish S ^a,b   Hughes, Timothy P ^a,b   Branford, Susan ^a,b  

^a CENTRE FOR CANCER BIOLOGY   (Australia)

^b UNIVERSITY OF ADELAIDE   (Australia)

^c Sequenom Asia Pacific   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BCR ABL PROTEIN; DASATINIB; IMATINIB; NILOTINIB;

ARTICLE; CANCER CHEMOTHERAPY; CANCER PATIENT; CHRONIC MYELOID LEUKEMIA; CLINICAL ASSESSMENT; CONTROLLED STUDY; CYTOGENETICS; DIAGNOSTIC TEST ACCURACY STUDY; DISEASE FREE SURVIVAL; GENE FREQUENCY; GENE MUTATION; HUMAN; HUMAN CELL; LIMIT OF DETECTION; MAJOR CLINICAL STUDY; MASS SPECTROMETRY; MOLECULAR CLONING; MUTATIONAL ANALYSIS; PREDICTIVE VALUE; PRIORITY JOURNAL; SENSITIVITY AND SPECIFICITY; SEQUENCE ANALYSIS; TREATMENT FAILURE; TREATMENT OUTCOME; TREATMENT RESPONSE;

ANTINEOPLASTIC AGENTS; DRUG RESISTANCE, NEOPLASM; FUSION PROTEINS, BCR-ABL; HUMANS; LEUKEMIA, MYELOGENOUS, CHRONIC, BCR-ABL POSITIVE; MASS SPECTROMETRY; MUTATION; PIPERAZINES; PROTEIN KINASE INHIBITORS; PYRIMIDINES; THIAZOLES; TREATMENT OUTCOME;

EID: 81155123199     PISSN: 0732183X     EISSN: 15277755     Source Type: Journal    
DOI: 10.1200/JCO.2011.35.0934     Document Type: Article

References (49)

1. Deininger M, O'Brien SG, Guilhot F, et al.: International Randomized Study of Interferon Vs STI571 (IRIS) 8-Year Follow up: Sustained survival and low risk for progression or events in patients with newly diagnosed chronic myeloid leukemia in chronic phase (CML-CP) treated with imatinib. 51st ASH Annual Meeting and Exposition, New Orleans, LA, December 5-8, 2009 (abstr 1126)
2. Apperley JF: Part I: Mechanisms of resistance to imatinib in chronic myeloid leukaemia. Lancet Oncol 8:1018-1029, 2007
3. Gorre ME, Mohammed M, Ellwood K, et al.: Clinical resistance to STI-571 cancer therapy caused by BCR-ABL gene mutation or amplification. Science 293:876-880, 2001 (Pubitemid 32743979)
4. von Bubnoff N, Schneller F, Peschel C, et al.: BCR-ABL gene mutations in relation to clinical resistance of Philadelphia-chromosome-positive leukaemia to STI571: A prospective study. Lancet 359:487-491, 2002 (Pubitemid 34164296)
5. Hochhaus A, Kreil S, Corbin AS, et al.: Molecular and chromosomal mechanisms of resistance to imatinib (STI571) therapy. Leukemia 16:2190-2196, 2002 (Pubitemid 35331833)
6. Hughes T, Saglio G, Branford S, et al.: Impact of baseline BCR-ABL mutations on response to nilotinib in patients with chronic myeloid leukemia in chronic phase. J Clin Oncol 27:4204-4210, 2009
7. Soverini S, Colarossi S, Gnani A, et al.: Resistance to dasatinib in Philadelphia-positive leukemia patients and the presence or the selection of mutations at residues 315 and 317 in the BCR-ABL kinase domain. Haematologica 92:401-404, 2007 (Pubitemid 350143551)
8. Shah NP, Skaggs BJ, Branford S, et al.: Sequential ABL kinase inhibitor therapy selects for compound drug-resistant BCR-ABL mutations with altered oncogenic potency. J Clin Invest 117:2562-2569, 2007 (Pubitemid 47494357)
9. 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 114:2168-2171, 2009
10. Müller MC, Cortes JE, Kim DW, et al.: Dasatinib treatment of chronic-phase chronic myeloid leukemia: Analysis of responses according to preexisting BCR-ABL mutations. Blood 114:4944-4953, 2009
11. O'Hare T, Walters DK, Stoffregen EP, et al.: In vitro activity of Bcr-Abl inhibitors AMN107 and BMS-354825 against clinically relevant imatinib-resistant Abl kinase domain mutants. Cancer Res 65:4500-4505, 2005 (Pubitemid 40740783)
12. Redaelli S, Piazza R, Rostagno R, et al.: Activity of bosutinib, dasatinib, and nilotinib against 18 imatinib-resistant BCR/ABL mutants. J Clin Oncol 27:469-471, 2009
13. Branford S, Melo JV, Hughes TP: Selecting optimal second-line tyrosine kinase inhibitor therapy for chronic myeloid leukemia patients after imatinib failure: Does the BCR-ABL mutation status really matter? Blood 114:5426-5435, 2009
14. Baccarani M, Cortes J, Pane F, et al.: Chronic myeloid leukemia: An update of concepts and management recommendations of European LeukemiaNet. J Clin Oncol 27:6041-6051, 2009
15. Jones D, Kamel-Reid S, Bahler D, et al.: Laboratory practice guidelines for detecting and reporting BCR-ABL drug resistance mutations in chronic myelogenous leukemia and acute lymphoblastic leukemia: A report of the Association for Molecular Pathology. J Mol Diagn 11:4-11, 2009
16. Müller MC, Lahaye T, Hochhaus A: Resistance to tumor specific therapy with imatinib by clonal selection of mutated cells [in German]. Dtsch Med Wochenschr 127:2205-2207, 2002
17. Branford S, Hughes TP: Mutational analysis in chronic myeloid leukemia: When and what to do? Curr Opin Hematol 18:111-116, 2011
18. Hanfstein B, Müller MC, Kreil S, et al.: Dynamics of mutant BCR-ABL-positive clones after cessation of tyrosine kinase inhibitor therapy. Haematologica 96:360-366, 2011
19. Roche-Lestienne C, Soenen-Cornu V, Grardel-Duflos N, et al.: Several types of mutations of the Abl gene can be found in chronic myeloid leukemia patients resistant to STI571, and they can pre-exist to the onset of treatment. Blood 100:1014-1018, 2002 (Pubitemid 34832631)
20. Kreuzer KA, Le Coutre P, Landt O, et al.: Preexistence and evolution of imatinib mesylate-resistant clones in chronic myelogenous leukemia detected by a PNA-based PCR clamping technique. Ann Hematol 82:284-289, 2003 (Pubitemid 36701422)
21. Deininger MW, McGreevey L, Willis S, et al.: Detection of ABL kinase domain mutations with denaturing high-performance liquid chromatography. Leukemia 18:864-871, 2004 (Pubitemid 38500206)
22. Sorel N, Chazelas F, Brizard A, et al.: Double-gradient- denaturing-gradient gel electrophoresis for mutation screening of the BCR-ABL tyrosine kinase domain in chronic myeloid leukemia patients. Clin Chem 51:1263-1266, 2005 (Pubitemid 43079409)
23. Gruber FX, Lamark T, Anonli A, et al.: Selecting and deselecting imatinib-resistant clones: Observations made by longitudinal, quantitative monitoring of mutated BCR-ABL. Leukemia 19:2159-2165, 2005 (Pubitemid 41741610)
24. Willis SG, Lange T, Demehri S, et al.: High-sensitivity detection of BCR-ABL kinase domain mutations in imatinib-naive patients: Correlation with clonal cytogenetic evolution but not response to therapy. Blood 106:2128-2137, 2005 (Pubitemid 41291730)
25. Khorashad JS, Anand M, Marin D, et al.: The presence of a BCR-ABL mutant allele in CML does not always explain clinical resistance to imatinib. Leukemia 20:658-663, 2006
26. Vivante A, Amariglio N, Koren-Michowitz M, et al.: High-throughput, sensitive and quantitative assay for the detection of BCR-ABL kinase domain mutations. Leukemia 21:1318-1321, 2007 (Pubitemid 46831827)
27. Ernst T, Erben P, Müller MC, et al.: Dynamics of BCR-ABL mutated clones prior to hematologic or cytogenetic resistance to imatinib. Haematologica 93:186-192, 2008 (Pubitemid 351397706)
28. Poláková KM, Lopotová T, Klamová H, et al.: High-resolution melt curve analysis: Initial screening for mutations in BCR-ABL kinase domain. Leuk Res 32:1236-1243, 2008
29. Pelz-Ackermann O, Cross M, Pfeifer H, et al.: Highly sensitive and quantitative detection of BCR-ABL kinase domain mutations by ligation PCR. Leukemia 22:2288-2291, 2008
30. Gruber FX, Ernst T, Kiselev Y, et al.: Detection of drug-resistant clones in chronic myelogenous leukemia patients during dasatinib and nilotinib treatment. Clin Chem 56:469-473, 2010
31. Nicolini FE, Chomel JC, Roy L, et al.: The durable clearance of the T315I BCR-ABL mutated clone in chronic phase chronic myelogenous leukemia patients on omacetaxine allows tyrosine kinase inhibitor rechallenge. Clin Lymphoma Myeloma Leuk 10:394-399, 2010
32. Kantarjian HM, Giles F, Gattermann N, et al.: Nilotinib (formerly AMN107), a highly selective BCR-ABL tyrosine kinase inhibitor, is effective in patients with Philadelphia chromosome-positive chronic myelogenous leukemia in chronic phase following imatinib resistance and intolerance. Blood 110:3540-3546, 2007 (Pubitemid 350159618)
33. le Coutre P, Ottmann OG, Giles F, et al.: Nilotinib (formerly AMN107), a highly selective BCR-ABL tyrosine kinase inhibitor, is active in patients with imatinib-resistant or -intolerant accelerated-phase chronic myelogenous leukemia. Blood 111:1834-1839, 2008 (Pubitemid 351451490)
34. Giles FJ, Larson RA, Kantarjian HM, et al.: Nilotinib in patients with Philadelphia chromosome-positive chronic myelogenous leukemia in blast crisis (CML-BC) who are resistant or intolerant to imatinib. J Clin Oncol 26:376s, 2008 (suppl; abstr 7017)
35. Cortes J, Rousselot P, Kim DW, et al.: Dasatinib induces complete hematologic and cytogenetic responses in patients with imatinib-resistant or -intolerant chronic myeloid leukemia in blast crisis. Blood 109:3207-3213, 2007 (Pubitemid 46572505)
36. Apperley JF, Cortes JE, Kim DW, et al.: Dasatinib in the treatment of chronic myeloid leukemia in accelerated phase after imatinib failure: The START a trial. J Clin Oncol 27:3472-3479, 2009
37. Hochhaus A, Kantarjian HM, Baccarani M, et al.: Dasatinib induces notable hematologic and cytogenetic responses in chronic-phase chronic myeloid leukemia after failure of imatinib therapy. Blood 109:2303-2309, 2007 (Pubitemid 46425867)
38. Branford S, Hughes T: Diagnosis and monitoring of chronic myeloid leukemia by qualitative and quantitative RT-PCR, in Illand H, Hertzgerg M, Marlton P (eds): Myeloid Leukemia: Methods and Protocols (Methods in Molecular Medicine). Totawa, New Jersey, Humana Press, 2006, pp 69-92
39. Branford S, Rudzki Z, Walsh S, et al.: Detection of BCR-ABL mutations in patients with CML treated with imatinib is virtually always accompanied by clinical resistance, and mutations in the ATP phosphate-binding loop (P-loop) are associated with a poor prognosis. Blood 102:276-283, 2003 (Pubitemid 36759665)
40. Ding C, Chiu RW, Lau TK, et al.: MS analysis of single-nucleotide differences in circulating nucleic acids: Application to noninvasive prenatal diagnosis. Proc Natl Acad Sci U S A 101:10762-10767, 2004 (Pubitemid 38955816)
41. Hughes TP, Hochhaus A, Branford S, et al.: Long-term prognostic significance of early molecular response to imatinib in newly diagnosed chronic myeloid leukemia: An analysis from the International Randomized Study of Interferon and STI571 (IRIS). Blood 116:3758-3765, 2010
42. 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 110:727-734, 2007 (Pubitemid 47108165)
43. Ernst T, Gruber FX, Pelz-Ackermann O, et al.: A co-operative evaluation of different methods of detecting BCR-ABL kinase domain mutations in patients with chronic myeloid leukemia on second-line dasatinib or nilotinib therapy after failure of imatinib. Haematologica 94:1227-1235, 2009
44. Nicolini FE, Mauro MJ, Martinelli G, et al.: Epidemiologic study on survival of chronic myeloid leukemia and Ph(+) acute lymphoblastic leukemia patients with BCR-ABL T315I mutation. Blood 114:5271-5278, 2009
45. Nicolini FE, Morisset S, Hochhaus A, et al.: The presence of the BCR-ABL T315I mutation in chronic phase chronic myelogenous leukemia resistant to tyrosine kinase inhibitors profoundly compromises overall survival and progression free survival: Preliminary results of a matched pair analysis. 52nd ASH Annual Meeting and Exposition, Orlando, FL, 2010 (abstr 3410)
46. O'Hare T, Shakespeare WC, Zhu X, et al.: AP24534, a pan-BCR-ABL inhibitor for chronic myeloid leukemia, potently inhibits the T315I mutant and overcomes mutation-based resistance. Cancer Cell 16:401-412, 2009
47. von Bubnoff N, Manley PW, Mestan J, et al.: Bcr-Abl resistance screening predicts a limited spectrum of point mutations to be associated with clinical resistance to the Abl kinase inhibitor nilotinib (AMN107). Blood 108:1328-1333, 2006 (Pubitemid 44232032)
48. Faber E, Mojzikova R, Plachy R, et al.: Major molecular response achieved with dasatinib in a CML patient with F317L BCR-ABL kinase domain mutation. Leuk Res 34:e91-e93, 2010
49. Zhang J, Adrián FJ, Jahnke W, et al.: Targeting Bcr-Abl by combining allosteric with ATP-binding-site inhibitors. Nature 463:501-506, 2010