Molecular pathogenesis of tyrosine kinase resistance in chronic myeloid leukemia

Current Opinion in Hematology

Volumn 17, Issue 2, 2010, Pages 91-96

  La Rosée, Paul ^a   Hochhaus, Andreas ^a  

^a JENA UNIVERSITY HOSPITAL   (Germany)

Author keywords

Chronic myelomyeloid leukemia; Dasatinib; Imatinib; Mechanisms of tyrosine kinase inhibitor resistance; Nilotinib

Indexed keywords

ALPHA INTERFERON; BCR ABL PROTEIN; BREAST CANCER RESISTANCE PROTEIN; DASATINIB; IMATINIB; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MULTIDRUG RESISTANCE PROTEIN 1; NILOTINIB; PROTEIN TYROSINE KINASE INHIBITOR;

ANTINEOPLASTIC ACTIVITY; CANCER RESISTANCE; CHRONIC MYELOID LEUKEMIA; DRUG HALF LIFE; DRUG METABOLISM; DRUG TRANSPORT; ENZYME INHIBITION; GENE MUTATION; HUMAN; NONHUMAN; PATIENT COMPLIANCE; PHARMACOGENOMICS; PRIORITY JOURNAL; REVIEW; SINGLE NUCLEOTIDE POLYMORPHISM;

DRUG RESISTANCE, NEOPLASM; ENZYME INHIBITORS; EVOLUTION, MOLECULAR; HUMANS; LEUKEMIA, MYELOGENOUS, CHRONIC, BCR-ABL POSITIVE; MUTATION; PIPERAZINES; PROTEIN-TYROSINE KINASES; PYRIMIDINES;

EID: 76749168976     PISSN: 10656251     EISSN: 15317048     Source Type: Journal    
DOI: 10.1097/MOH.0b013e3283366be1     Document Type: Review

References (53)

1. Druker BJ. Translation of the Philadelphia chromosome into therapy for CML. Blood 2008; 112:4808-4817.
2. Druker BJ, Guilhot F, O'Brien SG, et al. Five-year follow-up of patients receiving imatinib for chronic myeloid leukemia. N Engl J Med 2006; 355:2408-2417.
3. Hochhaus A, O'Brien SG, Guilhot F, et al. Six-year follow-up of patients receiving imatinib for the first-line treatment of chronic myeloid leukemia. Leukemia 2009; 23:1054-1061.
4. Hochhaus A, Druker B, Sawyers C, et al. Favorable long-term follow-up results over 6 years for response, survival, and safety with imatinib mesylate therapy in chronic-phase chronic myeloid leukemia after failure of interferon-alpha treatment. Blood 2008; 111:1039-1043.
5. Cortes J, O'Brien S, Kantarjian H. Discontinuation of imatinib therapy after achieving a molecular response. Blood 2004; 104:2204-2205.
6. Burchert A, Mueller MC, Kostrewa P, et al. Sustained molecular remissions with interferon alpha (IFN) maintenance therapy after induction with imatinib plus IFN in patients with chronic myeloid leukemia. J Clin Oncol (in press).
7. 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.
8. Apperley JF. Part I: mechanisms of resistance to imatinib in chronic myeloid leukaemia. Lancet Oncol 2007; 8:1018-1029.
9. 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.
10. 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; 114:2168-2171.
11. Schindler T, Bornmann W, Pellicena P, et al. Structural mechanism for STI-571 inhibition of abelson tyrosine kinase. Science 2000; 289:1938-1942.
12. Nagar B, Bornmann WG, Pellicena P, et al. Crystal structures of the kinase domain of c-Abl in complex with the small molecule inhibitors PD1 73955 and imatinib (STI-571). Cancer Res 2002; 62:4236-4243.
13. Azam M, Seeliger MA, Gray NS, et al. Activation of tyrosine kinases by mutation of the gatekeeper threonine. Nat Struct Mol Biol 2008; 15:1109-1118.
14. Nicolini FE, Mauro MJ, Martinelli G, et al. Epidemiological study on survival of chronic myeloid leukemia (CML) and Ph+ acute lymphoblastic leukemia (ALL) patients with BCR-ABL T315I mutation. Blood 2009; 114:5271-5278.
15. Liu J, Joha S, Idziorek T, et al. BCR-ABL mutants spread resistance to nonmutated cells through a paracrine mechanism. Leukemia 2008; 22:791-799.
16. Nambu T, Araki N, Nakagawa A, et al. Contribution of BCR-ABL-independent activation of ERK1/2 to acquired imatinib resistance in K562 chronic myeloid leukemia cells. Cancer Sci 2009 [Epub ahead of print].
17. Aceves-Luquero CI, Agarwal A, Callejas-Valera JL, et al. ERK2, but not ERK1, mediates acquired and 'de novo' resistance to imatinib mesylate: implication for CML therapy. PLoS One 2009; 4:e6124.
18. Stoklosa T, Poplawski T, Koptyra M, et al. BCR/ABL inhibits mismatch repair to protect from apoptosis and induce point mutations. Cancer Res 2008; 68:2576-2580.
19. Koptyra M, Cramer K, SlupianekA, et al. BCR/ABL promotes accumulation of chromosomal aberrations induced by oxidative and genotoxic stress. Leukemia 2008; 22:1969-1972.
20. Fernandes MS, Reddy MM, Gonneville JR, et al. BCR-ABL promotes the frequency of mutagenic single-strand annealing DNA repair. Blood 2009; 114:1813-1819.
21. 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.
22. Copland M, Hamilton A, Elrick LJ, et al. Dasatinib (BMS-354825) targets an earlier progenitor population than imatinib in primary CML but does not eliminate the quiescent fraction. Blood 2006; 107:4532-4539.
23. Konig H, Copland M, Chu S, et al. Effects of dasatinib on SRC kinase activity and downstream intracellular signaling in primitive chronic myelogenous leukemia hematopoietic cells. Cancer Res 2008; 68:9624-9633.
24. Konig H, Holyoake TL, Bhatia R. Effective and selective inhibition of chronic myeloid leukemia primitive hematopoietic progenitors by the dual Src/Abl kinase inhibitor SKI-606. Blood 2008; 111:2329-2338.
25. Konig H, Holtz M, Modi H, et al. Enhanced BCR-ABL kinase inhibition does not result in increased inhibition of downstream signaling pathways or increased growth suppression in CML progenitors. Leukemia 2008; 22: 748-755.
26. Chu S, Xu H, Shah NP, 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 2005; 105:2093-2098.
27. Jiang X, Zhao Y, Smith C, et al. Chronic myeloid leukemia stem cells possess multiple unique features of resistance to BCR-ABL targeted therapies. Leukemia 2007; 21:926-935.
28. Klemm L, Duy C, Iacobucci I, et al. The B cell mutator AID promotes B lymphoid blast crisis and drug resistance in chronic myeloid leukemia. Cancer Cell 2009; 16:232-245.
29. 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.
30. Muller 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 2009; 114:4944-4953.
31. Jabbour E, Hochhaus A, Cortes J, et al. Choosing the best treatment strategy for chronic myeloid leukemia patients resistant to imatinib: weighing the efficacy and safety of individual drugs with BCR-ABL mutations and patient history. Leukemia 2009 [Epub ahead of print].
32. Castagnetti F, Palandri F, Amabile M, et al. Results of high-dose imatinib mesylate in intermediate Sokal risk chronic myeloid leukemia patients in early chronic phase: a phase 2 trial of the GIMEMA CML Working Party. Blood 2009; 113:3428-3434.
33. Rosti G, Palandri F, Castagnetti F, et al. Nilotinib for the frontline treatment of Ph+ chronic myeloid leukemia. Blood 2009; 114:4933-4938.
34. La Rosee P, O'Dwyer ME, Druker BJ. Insights from preclinical studies for new combination treatment regimens with the Bcr-Abl kinase inhibitor imatinib mesylate (Gleevec/Glivec) in chronic myelogenous leukemia: a translational perspective. Leukemia 2002; 16:1213-1219.
35. 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 2009; 16:401-412.
36. Giles FJ, Cortes J, Jones D, et al. MK-0457,a novel kinase inhibitor, is active in patients with chronic myeloid leukemia or acute lymphocytic leukemia with the T315I BCR-ABL mutation. Blood 2007; 109:500-502.
37. Crossman LC, Mori M, Hsieh YC, et al. In chronic myeloid leukemia white cells from cytogenetic responders and nonresponders to imatinib have very similar gene expression signatures. Haematologica 2005; 90:459-464.
38. Radich JP, Dai H, Mao M, et al. Gene expression changes associated with progression and response in chronic myeloid leukemia. Proc Natl Acad Sci USA 2006; 103:2794-2799.
39. McWeeney SK, Pemberton LC, Loriaux MM, et al. A gene expression signature of CD34+ cells to predict major cytogenetic response in chronic phase chronic myeloid leukemia patients treated with imatinib. Blood 2009 [Epub ahead of print].
40. Jamieson CH, Ailles LE, Dylla SJ, et al. Granulocyte-macrophage progenitors as candidate leukemic stem cells in blast-crisis CML. N Engl J Med 2004; 351:657-667.
41. Weisberg E, Wright RD, McMillin DW, et al. Stromal-mediated protection of tyrosine kinase inhibitor-treated BCR-ABL-expressing leukemia cells. Mol Cancer Ther 2008; 7:1121-1129.
42. Graham SM, Jorgensen HG, Allan E, et al. Primitive, quiescent, Philadelphia-positive stem cells from patients with chronic myeloid leukemia are insensitive to STI571 in vitro. Blood 2002; 99:319-325.
43. Lemoli RM, Salvestrini V, Bianchi E, et al. Molecular and functional analysis of the stem cell compartment of chronic myelogenous leukemia reveals the presence of a CD34-cell population with intrinsic resistance to imatinib. Blood 2009; 114:5191-5200.
44. Essers MA, Offner S, Blanco-Bose WE, et al. IFNalpha activates dormant haematopoietic stem cells in vivo. Nature 2009; 458:904-908.
45. Koschmieder S, Gottgens B, Zhang P, et al. Inducible chronic phase of myeloid leukemia with expansion of hematopoietic stem cells in a transgenic model of BCR-ABL leukemogenesis. Blood 2005; 105:324-334.
46. Dulucq S, Bouchet S, Turcq B, et al. Multidrug resistance gene (MDR1) polymorphisms are associated with major molecular responses to standard-dose imatinib in chronic myeloid leukemia. Blood 2008; 112:2024-2027.
47. Noens L, van Lierde MA, de Bock R, et al. Prevalence, determinants, and outcomes of nonadherence to imatinib therapy in patients with chronic myeloid leukemia: the ADAGIO study. Blood 2009; 113:5401-5411.
48. Larson RA, Druker BJ, Guilhot F, et al. Imatinib pharmacokinetics and its correlation with response and safety in chronic-phase chronic myeloid leukemia: a subanalysis of the IRIS study. Blood 2008; 111:4022-4028.
49. Talpaz M, Shah NP, Kantarjian H, et al. Dasatinib in imatinib-resistant Philadelphia chromosome-positive leukemias. N Engl J Med 2006; 354:2531-2541. (Pubitemid 43882349)
50. Shah NP, Kantarjian HM, Kim DW, et al. Intermittent target inhibition with dasatinib 100mg once daily preserves efficacy and improves tolerability in imatinib-resistant and-intolerant chronic-phase chronic myeloid leukemia. J Clin Oncol 2008; 26:3204-3212.
51. Shah NP, Kasap C, Weier C, et al. Transient potent BCR-ABL inhibition is sufficient to commit chronic myeloid leukemia cells irreversibly to apoptosis. Cancer Cell 2008; 14:485-493.
52. Snead JL, O'Hare T, Adrian LT, et al. Acute dasatinib exposure commits Bcr-Abl-dependent cells to apoptosis. Blood 2009; 114:3459-3463.
53. Hiwase DK, White DL, Saunders VA, et al. Short-term intense Bcr-Abl kinase inhibition with nilotinib is adequate to trigger cell death in BCR-ABL(+) cells. Leukemia 2009; 23:1205-1206.