Cause and management of therapy resistance

Best Practice and Research: Clinical Haematology

Volumn 22, Issue 3, 2009, Pages 367-379

  Hochhaus, Andreas ^a   Schenk, Thomas ^a   Erben, Philipp ^a   Ernst, Thomas ^a   La Rosée, Paul ^a   Müller, Martin C ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

BCR ABL; CML; dasatinib; imatinib; mutations; nilotinib; resistance; tyrosine kinase inhibitors

Indexed keywords

ALPHA INTERFERON; BCR ABL PROTEIN; DASATINIB; HOMOHARRINGTONINE; HYDROXYUREA; IMATINIB; NILOTINIB; OMACETAXINE; UNCLASSIFIED DRUG;

ACUTE LYMPHOBLASTIC LEUKEMIA; AMINO ACID SUBSTITUTION; ANEMIA; BONE MARROW SUPPRESSION; CHRONIC MYELOID LEUKEMIA; CLINICAL TRIAL; CROSS RESISTANCE; DOSAGE SCHEDULE COMPARISON; DRUG DOSE COMPARISON; DRUG DOSE ESCALATION; DRUG DOSE INCREASE; DRUG MEGADOSE; DRUG TOLERABILITY; DRUG TREATMENT FAILURE; FLUID RETENTION; HUMAN; LEUKEMIA RELAPSE; LEUKEMIA REMISSION; MINIMAL RESIDUAL DISEASE; MULTIDRUG RESISTANCE; MUTATIONAL ANALYSIS; NEUTROPENIA; OVERALL SURVIVAL; PATIENT COMPLIANCE; PERICARDIAL EFFUSION; PHILADELPHIA 1 CHROMOSOME; PLEURA EFFUSION; POINT MUTATION; PRIORITY JOURNAL; PROGRESSION FREE SURVIVAL; REVIEW; SIDE EFFECT; SINGLE NUCLEOTIDE POLYMORPHISM; STEM CELL TRANSPLANTATION; SURVIVAL RATE; THROMBOCYTOPENIA;

DISEASE MANAGEMENT; DRUG RESISTANCE, NEOPLASM; HUMANS; LEUKEMIA, MYELOGENOUS, CHRONIC, BCR-ABL POSITIVE; PHARMACOGENETICS; POINT MUTATION;

EID: 71849105574     PISSN: 15216926     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.beha.2009.05.004     Document Type: Review

References (80)

1. Goldman J.M., and Melo J.V. Chronic myeloid leukemia-advances in biology and new approaches to treatment. N Engl J Med 349 15 (2003) 1451-1464
2. Druker B.J. Imatinib as a paradigm of targeted therapies. Adv Cancer Res 91 (2004) 1-30
3. Hochhaus A., and La Rosée P. Imatinib therapy in chronic myelogenous leukemia: strategies to avoid and overcome resistance. Leukemia 18 8 (2004) 1321-1331
4. Dai Y., Rahmani M., Corey S.J., et al. A Bcr/Abl-independent, Lyn-dependent form of imatinib mesylate (STI-571) resistance is associated with altered expression of Bcl-2. J Biol Chem 279 33 (2004) 34227-34239
5. Donato N.J., Wu J.Y., Stapley J., et al. BCR-ABL independence and LYN kinase overexpression in chronic myelogenous leukemia cells selected for resistance to STI571. Blood 101 2 (2003) 690-698
6. Baccarani M., Saglio G., Goldman J., et al. Evolving concepts in the management of chronic myeloid leukemia: recommendations from an expert panel on behalf of the European LeukemiaNet. Blood 108 6 (2006) 1809-1820
7. Hughes T.P., Kaeda J., Branford S., et al. Frequency of major molecular responses to imatinib or interferon alfa plus cytarabine in newly diagnosed chronic myeloid leukemia. N Engl J Med 349 15 (2003) 1423-1432
8. Hughes T., Deininger M., Hochhaus A., 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 108 1 (2006) 28-37
9. Müller M.C., Gattermann N., Lahaye T., et al. Dynamics of BCR-ABL mRNA expression in first-line therapy of chronic myelogenous leukemia patients with imatinib or interferon alpha/ara-C. Leukemia 17 12 (2003) 2392-2400
10. Kantarjian H., Sawyers C., Hochhaus A., et al. Hematologic and cytogenetic responses to imatinib mesylate in chronic myelogenous leukemia. N Engl J Med 346 9 (2002) 645-652
11. O'Brien S.G., Guilhot F., Larson R.A., et al. Imatinib compared with interferon and low-dose cytarabine for newly diagnosed chronic-phase chronic myeloid leukemia. N Engl J Med 348 11 (2003) 994-1004
12. Druker B.J., Guilhot F., O'Brien S.G., et al. Five-year follow-up of patients receiving imatinib for chronic myeloid leukemia. N Engl J Med 355 23 (2006) 2408-2417
13. Talpaz M., Silver R.T., Druker B.J., et al. Imatinib induces durable hematologic and cytogenetic responses in patients with accelerated phase chronic myeloid leukemia: results of a phase 2 study. Blood 99 6 (2002) 1928-1937
14. Sawyers C.L., Hochhaus A., Feldman E., et al. Imatinib induces hematologic and cytogenetic responses in patients with chronic myelogenous leukemia in myeloid blast crisis: results of a phase II study. Blood 99 10 (2002) 3530-3539
15. Lahaye T., Riehm B., Berger U., et al. Response and resistance in 300 patients with BCR-ABL-positive leukemias treated with imatinib in a single center: a 4.5-year follow-up. Cancer 103 8 (2005) 1659-1669
16. Cowan-Jacob S.W., Guez V., Fendrich G., et al. Imatinib (STI571) resistance in chronic myelogenous leukemia: molecular basis of the underlying mechanisms and potential strategies for treatment. Mini Rev Med Chem 4 3 (2004) 285-299
17. Thomas J., Wang L., Clark R.E., et al. Active transport of imatinib into and out of cells: implications for drug resistance. Blood 104 12 (2004) 3739-3745
18. Illmer T., Schaich M., Platzbecker U., et al. P-glycoprotein-mediated drug efflux is a resistance mechanism of chronic myelogenous leukemia cells to treatment with imatinib mesylate. Leukemia 18 3 (2004) 401-408
19. Gorre M.E., and Sawyers C.L. Molecular mechanisms of resistance to STI571 in chronic myeloid leukemia. Curr Opin Hematol 9 4 (2002) 303-307
20. Hochhaus A. Cytogenetic and molecular mechanisms of resistance to imatinib. Semin Hematol 40 2 Suppl. 2 (2003) 69-79
21. Shah N.P., Nicoll J.M., Nagar B., et al. Multiple BCR-ABL kinase domain mutations confer polyclonal resistance to the tyrosine kinase inhibitor imatinib (STI571) in chronic phase and blast crisis chronic myeloid leukemia. Cancer Cell 2 2 (2002) 117-125
22. Branford S., Rudzki Z., Parkinson I., et al. Real-time quantitative PCR analysis can be used as a primary screen to identify patients with CML treated with imatinib who have BCR-ABL kinase domain mutations. Blood 104 9 (2004) 2926-2932
23. Khorashad J.S., 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 4 (2006) 658-663
24. Roche-Lestienne C., and Preudhomme C. Mutations in the ABL kinase domain pre-exist the onset of imatinib treatment. Semin Hematol 40 2 Suppl. 2 (2003) 80-82
25. Willis S.G., 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 6 (2005) 2128-2137
26. Chu S., Xu H., Shah N.P., et al. Detection of BCR-ABL kinase mutations in CD34+ cells from chronic myelogenous leukemia patients in complete cytogenetic remission on imatinib mesylate treatment. Blood 105 5 (2005) 2093-2098
27. Graham S.M., Jorgensen H.G., Allan E., et al. Primitive, quiescent, Philadelphia-positive stem cells from patients with chronic myeloid leukemia are insensitive to STI571 in vitro. Blood 99 1 (2002) 319-325
28. Angstreich G.R., Matsui W., Huff C.A., et al. Effects of imatinib and interferon on primitive chronic myeloid leukaemia progenitors. Br J Haematol 130 3 (2005) 373-381
29. 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 GIMEMA Working Party on Chronic Myeloid Leukemia. J Clin Oncol 23 18 (2005) 4100-4109
30. 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 1 (2003) 276-283
31. Burchert A., Wang Y., Cai D., et al. Compensatory PI3-kinase/Akt/mTor activation regulates imatinib resistance development. Leukemia 19 10 (2005) 1774-1782
32. Hochhaus A., Kreil S., Corbin A.S., et al. Molecular and chromosomal mechanisms of resistance to imatinib (STI571) therapy. Leukemia 16 11 (2002) 2190-2196
33. O'Dwyer M.E., Mauro M.J., Kurilik G., et al. The impact of clonal evolution on response to imatinib mesylate (STI571) in accelerated phase CML. Blood 100 5 (2002) 1628-1633
34. Schoch C., Haferlach T., Kern W., et al. Occurrence of additional chromosome aberrations in chronic myeloid leukemia patients treated with imatinib mesylate. Leukemia 17 2 (2003) 461-463
35. Mohamed A.N., Pemberton P., Zonder J., et al. The effect of imatinib mesylate on patients with Philadelphia chromosome-positive chronic myeloid leukemia with secondary chromosomal aberrations. Clin Cancer Res 9 4 (2003) 1333-1337
36. O'Dwyer M.E., Mauro M.J., Blasdel C., et al. Clonal evolution and lack of cytogenetic response are adverse prognostic factors for hematologic relapse of chronic phase CML patients treated with imatinib mesylate. Blood 103 2 (2004) 451-455
37. Terre C., Eclache V., Rousselot P., et al. Report of 34 patients with clonal chromosomal abnormalities in Philadelphia-negative cells during imatinib treatment of Philadelphia-positive chronic myeloid leukemia. Leukemia 18 8 (2004) 1340-1346
38. Bacher U., Haferlach T., Hiddemann W., et al. Additional clonal abnormalities in Philadelphia-positive ALL and CML demonstrate a different cytogenetic pattern at diagnosis and follow different pathways at progression. Cancer Genet Cytogenet 157 1 (2005) 53-61
39. Gorre M.E., Mohammed M., Ellwood K., et al. Clinical resistance to STI-571 cancer therapy caused by BCR-ABL gene mutation or amplification. Science 293 5531 (2001) 876-880
40. Baccarani M., Pane F., and Saglio G. Monitoring treatment of chronic myeloid leukemia. Haematologica 93 2 (2008) 161-169
41. Schindler T., Bornmann W., Pellicena P., et al. Structural mechanism for STI-571 inhibition of abelson tyrosine kinase. Science 289 5486 (2000) 1938-1942
42. Deininger M.W., McGreevey L., Willis S., et al. Detection of ABL kinase domain mutations with denaturing high-performance liquid chromatography. Leukemia 18 4 (2004) 864-871
43. Soverini S., Martinelli G., Amabile M., et al. Denaturing-HPLC-based assay for detection of ABL mutations in chronic myeloid leukemia patients resistant to Imatinib. Clin Chem 50 7 (2004) 1205-1213
44. Irving J.A., O'Brien S., Lennard A.L., et al. Use of denaturing HPLC for detection of mutations in the BCR-ABL kinase domain in patients resistant to Imatinib. Clin Chem 50 7 (2004) 1233-1237
45. Ernst T., Erben P., Müller M.C., et al. Dynamics of BCR-ABL mutated clones prior to hematologic or cytogenetic resistance to imatinib. Haematologica 93 2 (2008) 186-192
46. 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 2 (2007) 727-734
47. Crossman L.C., O'Hare T., Lange T., et al. A single nucleotide polymorphism in the coding region of ABL and its effects on sensitivity to imatinib. Leukemia 19 11 (2005) 1859-1862
48. Ernst T., Hoffmann J., Erben P., et al. ABL single nucleotide polymorphisms may masquerade as BCR-ABL mutations associated with resistance to tyrosine kinase inhibitors in patients with chronic myeloid leukemia. Haematologica 93 9 (2008) 1389-1393
49. Khorashad J.S., de Lavallade H., Apperley J.F., et al. Finding of kinase domain mutations in patients with chronic phase chronic myeloid leukemia responding to imatinib may identify those at high risk of disease progression. J Clin Oncol 26 29 (2008) 4806-4813
50. Sherbenou D.W., Wong M.J., Humayun A., et al. Mutations of the BCR-ABL-kinase domain occur in a minority of patients with stable complete cytogenetic response to imatinib. Leukemia 21 3 (2007) 489-493
51. Müller M.C., Lahaye T., and Hochhaus A. [Resistance to tumor specific therapy with imatinib by clonal selection of mutated cells]. Dtsch Med Wochenschr 127 42 (2002) 2205-2207
52. Hanfstein B., Mueller M.C., Kreil S., et al. Dynamics of mutant BCR-ABL positive clones after cessation of imatinib treatment. Haematologica 93 s1 (2008) 43-44
53. Legros L., Hayette S., Nicolini F.E., et al. BCR-ABL(T315I) transcript disappearance in an imatinib-resistant CML patient treated with homoharringtonine: a new therapeutic challenge?. Leukemia 21 10 (2007) 2204-2206
54. Kantarjian H.M., Talpaz M., O'Brien S., et al. Dose escalation of imatinib mesylate can overcome resistance to standard-dose therapy in patients with chronic myelogenous leukemia. Blood 101 2 (2003) 473-475
55. Kantarjian H., Talpaz M., O'Brien S., et al. High-dose imatinib mesylate therapy in newly diagnosed Philadelphia chromosome-positive chronic phase chronic myeloid leukemia. Blood 103 8 (2004) 2873-2878
56. White D.L., Saunders V.A., Dang P., et al. OCT-1-mediated influx is a key determinant of the intracellular uptake of imatinib but not nilotinib (AMN107): reduced OCT-1 activity is the cause of low in vitro sensitivity to imatinib. Blood 108 2 (2006) 697-704
57. White D.L., Saunders V.A., Dang P., et al. Most CML patients who have a suboptimal response to imatinib have low OCT-1 activity: higher doses of imatinib may overcome the negative impact of low OCT-1 activity. Blood 110 12 (2007) 4064-4072
58. Wang L., Giannoudis A., Lane S., et al. Expression of the uptake drug transporter hOCT1 is an important clinical determinant of the response to imatinib in chronic myeloid leukemia. Clin Pharmacol Ther 83 2 (2008) 258-264
59. Gambacorti-Passerini C., Zucchetti M., Russo D., et al. Alpha1 acid glycoprotein binds to imatinib (STI571) and substantially alters its pharmacokinetics in chronic myeloid leukemia patients. Clin Cancer Res 9 2 (2003) 625-632
60. Shah N.P., Tran C., Lee F.Y., et al. Overriding imatinib resistance with a novel ABL kinase inhibitor. Science 305 5682 (2004) 399-401
61. Weisberg E., Manley P.W., Breitenstein W., et al. Characterization of AMN107, a selective inhibitor of native and mutant Bcr-Abl. Cancer Cell 7 2 (2005) 129-141
62. Bradeen H.A., Eide C.A., O'Hare T., 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 108 7 (2006) 2332-2338
63. Burgess M.R., Skaggs B.J., Shah N.P., et al. Comparative analysis of two clinically active BCR-ABL kinase inhibitors reveals the role of conformation-specific binding in resistance. Proc Natl Acad Sci U S A 102 9 (2005) 3395-3400
64. Ray A., Cowan-Jacob S.W., Manley P.W., et al. Identification of BCR-ABL point mutations conferring resistance to the Abl kinase inhibitor AMN107 (nilotinib) by a random mutagenesis study. Blood 109 11 (2007) 5011-5015
65. 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 3 (2009) 469-471
66. Hochhaus A., Kantarjian H.M., Baccarani M., et al. Dasatinib induces notable hematologic and cytogenetic responses in chronic-phase chronic myeloid leukemia after failure of imatinib therapy. Blood 109 6 (2007) 2303-2309
67. Hochhaus A., Baccarani M., Deininger M., et al. Dasatinib induces durable cytogenetic responses in patients with chronic myelogenous leukemia in chronic phase with resistance or intolerance to imatinib. Leukemia 22 6 (2008) 1200-1206
68. Ottmann O., Dombret H., Martinelli G., et al. Dasatinib induces rapid hematologic and cytogenetic responses in adult patients with Philadelphia chromosome positive acute lymphoblastic leukemia with resistance or intolerance to imatinib: interim results of a phase 2 study. Blood 110 7 (2007) 2309-2315
69. Cortes J., Rousselot P., Kim D.W., et al. Dasatinib induces complete hematologic and cytogenetic responses in patients with imatinib-resistant or -intolerant chronic myeloid leukemia in blast crisis. Blood 109 8 (2007) 3207-3213
70. Guilhot F., Apperley J., Kim D.W., et al. Dasatinib induces significant hematologic and cytogenetic responses in patients with imatinib-resistant or -intolerant chronic myeloid leukemia in accelerated phase. Blood 109 10 (2007) 4143-4150
71. Shah N.P., Kantarjian H.M., Kim D.W., et al. Intermittent target inhibition with dasatinib 100 mg once daily preserves efficacy and improves tolerability in imatinib-resistant and -intolerant chronic-phase chronic myeloid leukemia. J Clin Oncol 26 19 (2008) 3204-3212
72. Kantarjian H.M., 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 10 (2007) 3540-3546
73. Gratwohl A., Baldomero H., Schwendener A., et al. Hematopoietic stem cell transplants for chronic myeloid leukemia in Europe-impact of cost considerations. Leukemia 21 3 (2007) 383-386
74. Hehlmann R., Berger U., Pfirrmann M., et al. Drug treatment is superior to allografting as first-line therapy in chronic myeloid leukemia. Blood 109 11 (2007) 4686-4692
75. Saussele S., Lauseker M., Gratwohl A., et al. Allogeneic hematopoietic stem cell transplantation (HSCT) in the imatinib-era: high survival rate following allogeneic HSCT after imatinib failure: results of the German CML Study IV. Blood 112 (2008) 171a
76. Shah N.P., Skaggs B.J., 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 9 (2007) 2562-2569
77. Müller M., Hanfstein B., Erben P., et al. Molecular response to first line imatinib therapy is predictive for long term event free survival in patients with chronic phase chronic myelogeneous leukemia - An interim analysis of the randomized German CML Study IV. Blood 112 (2008) 129a
78. Khorashad J.S., Milojkovic D., Mehta P., et al. In vivo kinetics of kinase domain mutations in CML patients treated with dasatinib after failing imatinib. Blood 111 4 (2008) 2378-2381
79. Jabbour E., Kantarjian H., Jones D., et al. Characteristics and outcomes of patients with chronic myeloid leukemia and T315I mutation following failure of imatinib mesylate therapy. Blood 112 1 (2008) 53-55
80. T315I mutated transcripts in chronic phase chromin myelogenous leukemia patients resistant to tyrosine kinase inhibitors. Blood 112 (2008) 403a