Chronic Myeloid Leukemia: Mechanisms of Resistance and Treatment

Hematology/Oncology Clinics of North America

Volumn 25, Issue 5, 2011, Pages 981-995

  Jabbour, Elias ^a   Parikh, Sameer A ^a   Kantarjian, Hagop ^a   Cortes, Jorge ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

Homoharringtonine; Multikinase inhibitors; Mutation screening; Myeloproliferative disorders; Tyrosine kinase inhibitors

Indexed keywords

BCR ABL PROTEIN; BOSUTINIB; DASATINIB; HOMOHARRINGTONINE; IMATINIB; NILOTINIB; PONATINIB; PROTEIN TYROSINE KINASE; PROTEIN TYROSINE KINASE INHIBITOR; XL 228;

ACUTE GRANULOCYTIC LEUKEMIA; ALLOGENEIC STEM CELL TRANSPLANTATION; ANEMIA; ASTHENIA; BILIRUBIN BLOOD LEVEL; BONE MARROW SUPPRESSION; BRADYCARDIA; CANCER CHEMOTHERAPY; CANCER RESISTANCE; CANCER STEM CELL; CANCER SURVIVAL; CANCER TRANSPLANTATION; CHEMOTHERAPY INDUCED EMESIS; CHINESE MEDICINE; CHROMOSOME ABERRATION; CHRONIC MYELOID LEUKEMIA; DIARRHEA; DOSAGE SCHEDULE COMPARISON; DOSE RESPONSE; DRUG APPROVAL; DRUG BIOAVAILABILITY; DRUG BLOOD LEVEL; DRUG DOSE COMPARISON; DRUG DOSE ESCALATION; DRUG EFFICACY; DRUG ERUPTION; DRUG FEVER; DRUG HALF LIFE; DRUG INDICATION; DRUG INDUCED HEADACHE; DRUG INTERACTION; DRUG MECHANISM; DRUG MEGADOSE; DRUG POTENCY; DRUG SAFETY; DRUG SUBSTITUTION; DRUG TOLERABILITY; DRUG TRANSPORT; DRUG TREATMENT FAILURE; DRUG WITHDRAWAL; EVENT FREE SURVIVAL; FATIGUE; FLUID RETENTION; GENE AMPLIFICATION; GENE OVEREXPRESSION; GENETIC SCREENING; HUMAN; HYPERGLYCEMIA; HYPOPHOSPHATEMIA; LEUKEMIA CELL; MEDICATION THERAPY MANAGEMENT; MICROENVIRONMENT; MULTIDRUG RESISTANCE; MUTATIONAL ANALYSIS; NAUSEA; NEUTROPENIA; OVERALL SURVIVAL; PATIENT COMPLIANCE; PERICARDIAL EFFUSION; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); PLEURA EFFUSION; POINT MUTATION; PRACTICE GUIDELINE; PRIORITY JOURNAL; PROTEIN DOMAIN; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; SIDE EFFECT; SIGNAL TRANSDUCTION; SURVIVAL RATE; SYNCOPE; THROMBOCYTOPATHY; THROMBOCYTOPENIA; TREATMENT RESPONSE; TRIACYLGLYCEROL LIPASE BLOOD LEVEL; UNSPECIFIED SIDE EFFECT;

ANTINEOPLASTIC AGENTS; DISEASE-FREE SURVIVAL; DRUG RESISTANCE, NEOPLASM; FOLLOW-UP STUDIES; HUMANS; LEUKEMIA, MYELOGENOUS, CHRONIC, BCR-ABL POSITIVE; PIPERAZINES; PROTEIN KINASE INHIBITORS; PYRIMIDINES; SURVIVAL RATE;

EID: 80755159112     PISSN: 08898588     EISSN: 15581977     Source Type: Journal    
DOI: 10.1016/j.hoc.2011.09.004     Document Type: Review

References (66)

1. Jemal A., Siegel R., Ward E., et al. Cancer statistics, 2009. CA Cancer J Clin 2009, 59:225-249.
2. Bartram C.R., de Klein A., Hagemeijer A., et al. Translocation of c-ab1 oncogene correlates with the presence of a Philadelphia chromosome in chronic myelocytic leukaemia. Nature 1983, 306:277-280.
3. Rowley J.D. Letter: a new consistent chromosomal abnormality in chronic myelogenous leukaemia identified by quinacrine fluorescence and Giemsa staining. Nature 1973, 243:290-293.
4. Druker B.J., Tamura S., Buchdunger E., et al. Effects of a selective inhibitor of the Abl tyrosine kinase on the growth of Bcr-Abl positive cells. Nat Med 1996, 2:561-566.
5. Druker B.J., Talpaz M., Resta D.J., 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.
6. Kantarjian H., Sawyers C., Hochhaus A., et al. Hematologic and cytogenetic responses to imatinib mesylate in chronic myelogenous leukemia. N Engl J Med 2002, 346:645-652.
7. 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 2003, 348:994-1004.
8. Deininger M., O'Brien S.G., 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. Blood 2009, 114:1126. (ASH Annual Meeting Abstracts).
9. Zhang W.W., Cortes J.E., Yao H., et al. Predictors of primary imatinib resistance in chronic myelogenous leukemia are distinct from those in secondary imatinib resistance. J Clin Oncol 2009, 27:3642-3649.
10. le Coutre P., Tassi E., Varella-Garcia M., et al. Induction of resistance to the Abelson inhibitor STI571 in human leukemic cells through gene amplification. Blood 2000, 95:1758-1766.
11. 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 2001, 293:876-880.
12. Weisberg E., Griffin J.D. Mechanism of resistance to the ABL tyrosine kinase inhibitor STI571 in BCR/ABL-transformed hematopoietic cell lines. Blood 2000, 95:3498-3505.
13. 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 2003, 102:276-283.
14. Hochhaus A., Kreil S., Corbin A.S., et al. Molecular and chromosomal mechanisms of resistance to imatinib (STI571) therapy. Leukemia 2002, 16:2190-2196.
15. Corbin A.S., La Rosee P., Stoffregen E.P., et al. Several Bcr-Abl kinase domain mutants associated with imatinib mesylate resistance remain sensitive to imatinib. Blood 2003, 101:4611-4614.
16. Soverini S., Colarossi S., Gnani A., et al. Contribution of ABL kinase domain mutations to imatinib resistance in different subsets of Philadelphia-positive patients: by the GIMEMA Working Party on Chronic Myeloid Leukemia. Clin Cancer Res 2006, 12:7374-7379.
17. Jabbour E., Kantarjian H., Jones D., et al. Long-term incidence and outcome of BCR-ABL mutations in patients (pts) with chronic myeloid leukemia (CML) treated with imatinib mesylate P-loop mutations are not associated with worse outcome. Blood 2004, 104:1007. (ASH Annual Meeting Abstracts).
18. Jabbour E., Kantarjian H., Jones D., et al. Frequency and clinical significance of BCR-ABL mutations in patients with chronic myeloid leukemia treated with imatinib mesylate. Leukemia 2006, 20:1767-1773.
19. 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 2004, 50:1205-1213.
20. Deininger M.W., McGreevey L., Willis S., et al. Detection of ABL kinase domain mutations with denaturing high-performance liquid chromatography. Leukemia 2004, 18:864-871.
21. Apperley J.F. Part I: mechanisms of resistance to imatinib in chronic myeloid leukaemia. Lancet Oncol 2007, 8:1018-1029.
22. Hochhaus A., La Rosee P. Imatinib therapy in chronic myelogenous leukemia: strategies to avoid and overcome resistance. Leukemia 2004, 18:1321-1331.
23. Version 2. National Comprehensive Cancer Network 2010, Clinical Practice Guidelines in Oncology.
24. Baccarani M., Cortes J., Pane F., et al. Chronic myeloid leukemia: an update of concepts and management recommendations of European LeukemiaNet. J Clin Oncol 2009, 27:6041-6051.
25. Press R.D., Willis S.G., Laudadio J., et al. Determining the rise in BCR-ABL RNA that optimally predicts a kinase domain mutation in patients with chronic myeloid leukemia on imatinib. Blood 2009, 114:2598-2605.
26. Kantarjian H.M., Larson R.A., Guilhot F., et al. Efficacy of imatinib dose escalation in patients with chronic myeloid leukemia in chronic phase. Cancer 2009, 115:551-560.
27. Jabbour E., Kantarjian H.M., Jones D., et al. Imatinib mesylate dose escalation is associated with durable responses in patients with chronic myeloid leukemia after cytogenetic failure on standard-dose imatinib therapy. Blood 2009, 113:2154-2160.
28. Cortes J.E., Kantarjian H.M., Goldberg S.L., et al. High-dose imatinib in newly diagnosed chronic-phase chronic myeloid leukemia: high rates of rapid cytogenetic and molecular responses. J Clin Oncol 2009, 27:4754-4759.
29. Baccarani M., Druker B.J., Cortes-Franco J., et al. 24 months update of the TOPS study: a phase III, of 400mg/d (SD-IM) versus 800mg/d (HD-IM) of imatinib mesylate (IM) in patients (Pts) with newly diagnosed, previously untreated chronic myeloid leukemia in chronic phase (CML-CP). Blood 2009, 114:337. (ASH Annual Meeting Abstracts).
30. Baccarani M., Rosti G., Castagnetti F., et al. Comparison of imatinib 400 mg and 800 mg daily in the front-line treatment of high-risk, Philadelphia-positive chronic myeloid leukemia: a European LeukemiaNet Study. Blood 2009, 113:4497-4504.
31. Lombardo L.J., Lee F.Y., Chen P., et al. Discovery of N-(2-chloro-6-methyl- phenyl)-2-(6-(4-(2-hydroxyethyl)- piperazin-1-yl)-2-methylpyrimidin-4- ylamino)thiazole-5-carboxamide (BMS-354825), a dual Src/Abl kinase inhibitor with potent antitumor activity in preclinical assays. J Med Chem 2004, 47:6658-6661.
32. 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 2007, 109:3207-3213.
33. 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 2007, 109:4143-4150.
34. 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 2008, 22:1200-1206.
35. 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 2008, 26:3204-3212.
36. Cortes J.E., Jones D., O'Brien S., et al. Results of dasatinib therapy in patients with early chronic-phase chronic myeloid leukemia. J Clin Oncol 2010, 28:398-404.
37. Golemovic M., Verstovsek S., Giles F., et al. AMN107, a novel aminopyrimidine inhibitor of Bcr-Abl, has in vitro activity against imatinib-resistant chronic myeloid leukemia. Clin Cancer Res 2005, 11:4941-4947.
38. Weisberg E., Manley P.W., Breitenstein W., et al. Characterization of AMN107, a selective inhibitor of native and mutant Bcr-Abl. Cancer Cell 2005, 7:129-141.
39. Hocchaus A., Cortes J., Appereley J., et al. Nilotinib in chronic myeloid leukemia patients in accelerated phase (CML-AP) with imatinib resistance or intolerance: 24-month follow-up results of a phase 2 study. Haematologica 2009, 94(Suppl 2). [abstract 0631].
40. Kantarjian HM, Giles FJ, Bhalla KN, et al. Update on imatinib-resistant chronic myeloid leukemia patients in chronic phase (CML-CP) on nilotinib therapy at 24 months: clinical response, safety, and long-term outcomes. ASH Annual Meeting Abstracts 2009;114:1129.
41. Cortes J.E., Jones D., O'Brien S., et al. Nilotinib as front-line treatment for patients with chronic myeloid leukemia in early chronic phase. J Clin Oncol 2010, 28:392-397.
42. O'Dwyer MC, Kent E, Parker M, et al. Nilotinib 300 mg twice daily is effective and well tolerated as first line treatment of Ph-positive chronic myeloid leukemia in chronic phase: preliminary results of the ICORG 0802 phase 2 study. ASH Annual Meeting Abstracts 2009;114:3294.
43. Rosti G., Palandri F., Castagnetti F., et al. Nilotinib for the frontline treatment of Ph(+) chronic myeloid leukemia. Blood 2009, 114:4933-4938.
44. Redaelli S., Piazza R., Rostagno R., et al. Activity of bosutinib, dasatinib, and nilotinib against 18 imatinib-resistant BCR/ABL mutants. J Clin Oncol 2009, 27:469-471.
45. Cortes J., Kantarjian H.M., Kim D.W., et al. Efficacy and safety of bosutinib (SKI-606) in patients with chronic phase (CP) Ph+ chronic myelogenous leukemia (CML) with resistance or intolerance to imatinib. Blood 2008, 112:1098. (ASH Annual Meeting Abstracts).
46. Gambacorti-Passerini C., Kantarjian H., Bruemmendorf T., et al. Bosutinib (SKI-606) demonstrates clinical activity and is well tolerated among patients with AP and BP CML and Ph+ ALL. Blood 2007, 110:473. (ASH Annual Meeting Abstracts).
47. O'Hare T., Shakespeare W.C., 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 2009, 16:401-412.
48. Cortes J., Talpaz M., Deininger M., et al. A Phase 1 trial of oral AP24534 in patients with refractory chronic myeloid leukemia and other hematologic malignancies: first results of safety and clinical activity against T315I and resistant mutations. Blood 2009, 114:643. (ASH Annual Meeting Abstracts).
49. Cortes J., Paquette R., Talpaz M., et al. Preliminary clinical activity in a Phase I trial of the BCR-ABL/IGF- 1R/aurora kinase inhibitor XL228 in patients with Ph++ leukemias with either failure to multiple TKI therapies or with T315I mutation. Blood 2008, 112:3232. (ASH Annual Meeting Abstracts).
50. O'Brien S., Kantarjian H., Koller C., et al. Sequential homoharringtonine and interferon-alpha in the treatment of early chronic phase chronic myelogenous leukemia. Blood 1999, 93:4149-4153.
51. O'Brien S., Talpaz M., Cortes J., et al. Simultaneous homoharringtonine and interferon-alpha in the treatment of patients with chronic-phase chronic myelogenous leukemia. Cancer 2002, 94:2024-2032.
52. Kantarjian H.M., Talpaz M., Santini V., et al. Homoharringtonine: history, current research, and future direction. Cancer 2001, 92:1591-1605.
53. O'Brien S., Kantarjian H., Keating M., et al. Homoharringtonine therapy induces responses in patients with chronic myelogenous leukemia in late chronic phase. Blood 1995, 86:3322-3326.
54. Cortes-Franco J., Raghunadharao D., Parikh P., et al. Safety and efficacy of subcutaneous-administered omacetaxine mepesuccinate in chronic myeloid leukemia (CML) patients who are resistant or intolerant to two or more tyrosine kinase inhibitors: results of a multicenter Phase 2/3 study. Blood 2009, 114:861. (ASH Annual Meeting Abstracts).
55. Cortes-Franco J., Khoury H.J., Nicolini F.E., et al. Safety and efficacy of subcutaneous-administered omacetaxine mepesuccinate in imatinib-resistant chronic myeloid leukemia (CML) patients who harbor the Bcr- Abl T315I mutation-results of an ongoing multicenter Phase 2/3 study. Blood 2009, 114:644. (ASH Annual Meeting Abstracts).
56. 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 2005, 106:2128-2137.
57. 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 2006, 20:658-663.
58. Mauro M.J. Mutational analysis and overcoming imatinib resistance in chronic myeloid leukemia with novel tyrosine kinase inhibitors. Curr Treat Options Oncol 2007, 8:287-295.
59. 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 2007, 21:489-493.
60. Laneuville P., Dilea C., Yin O.Q., et al. Comparative In vitro cellular data alone are insufficient to predict clinical responses and guide the choice of BCR-ABL inhibitor for treating imatinib-resistant chronic myeloid leukemia. J Clin Oncol 2010, 28:e169-e171. [author reply: e172].
61. Jabbour E., Jones D., Kantarjian H.M., et al. Long-term outcome of patients with chronic myeloid leukemia treated with second-generation tyrosine kinase inhibitors after imatinib failure is predicted by the in vitro sensitivity of BCR-ABL kinase domain mutations. Blood 2009, 114:2037-2043.
62. Muller M.C., Cortes J.E., Kim D.W., et al. Dasatinib treatment of chronic-phase chronic myeloid leukemia: analysis of responses according to preexisting BCR-ABL mutations. Blood 2009, 114:4944-4953.
63. 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 2009, 27:4204-4210.
64. Quintas-Cardama A., Kantarjian H., O'Brien S., et al. Pleural effusion in patients with chronic myelogenous leukemia treated with dasatinib after imatinib failure. J Clin Oncol 2007, 25:3908-3914.
65. Quintas-Cardama A., Kantarjian H., Ravandi F., et al. Bleeding diathesis in patients with chronic myelogenous leukemia receiving dasatinib therapy. Cancer 2009, 115:2482-2490.
66. Sillaber C., Herrmann H., Bennett K., et al. Immunosuppression and atypical infections in CML patients treated with dasatinib at 140 mg daily. Eur J Clin Invest 2009, 39:1098-1109.