Current trends in the treatment and diagnostics of chronic myeloid leukaemia
Authors:
H. Klamová; H. Žižková; P. Burda; N. Čuřík; D. Srbová; K. Machová Poláková
Authors‘ workplace:
Ústav hematologie a krevní transfuze, Praha
Published in:
Transfuze Hematol. dnes,23, 2017, No. Supplementum1, p. 34-46.
Category:
Overview
Current CML therapy based on tyrosine kinase inhibitors (TKI) provides excellent outcomes: more than 80% of patients diagnosed in chronic phase of CML survive at least 10 years and a quite high number of patients have a long-term deep molecular response. Nevertheless, modern trends in clinical practice include discontinuation of TKI therapy in patients with sustained deep molecular response. Patient concerns and health care cost considerations have prompted research into the possibility of TKI treatment-free remission for selected patients or into the setting up individual treatment approaches based on the identification of disease progression markers. To apply this strategy, monitoring of minimal residual disease and early detection of relapse is absolutely critical. Digital PCR (dPCR) represents a very precise and sensitive technology for detecting BCR-ABL1 at mRNA or DNA level – with a capability of detecting CML cells lacking expression of BCR-ABL1. Exact measurement of minimal residual disease is key for CML therapy management and eventual TKI discontinuation.
KEY WORDS:
chronic myeloid leukaemia – tyrosine kinase inhibitors – BCR-ABL1 mutations – leukemic stem cell
Sources
1. Rowley JD. Letter: A new consistent chromosomal abnormality in chronic myelogenous leukaemia identified by quinacrine fluorescence and Giemsa staining. Nature 1973;243(5405):290–293.
2. Faderl S, Talpaz M, Estrov Z, et al. The biology of chronic myeloid leukemia. New Engl J Med 1999;341(3):164–172.
3. Sawyers CL. Chronic myeloid leukemia. New Engl J Med 1999;340(17):1330–13340.
4. Faber E, Indrák K, et al. Chronická myeloidní leukémie. Praha: Galén, 2010. ISBN 978-80-7262-680-9.
5. Indrák K. Hematologie a transfuzní lékařství. Praha: TRITON. 2014. ISBN 978-80-7387-722-4.
6. Dušek L, Mužík J, Kubásek M et al. Epidemiologie zhoubných nádorů v České republice. Masarykova univerzita, 2005. (http://www.svod.cz)
7. Kantarjian HM, O’Brien S, Cortes JE, et al. Complete cytogenetic and molecular responses to interferon-alpha-based therapy for chronic myelogenous leukemia are associated with excellent long-term prognosis. Cancer 2003;97(4):1033–1041.
8. O’Brien SG, Guilhot F, Larson RA, et al. Imatinib compared with interferon and low-dose cytarabine for newly diagnosed chronic-phase chronic myeloid leukemia. New Engl J Med 2003;348(11):994–1004.
9. Klamova H, Faber E, Zackova D, et al. Dasatinib in imatinib-resistant or -intolerant CML patients: data from the clinical practice of 6 hematological centers in the Czech Republic. Neoplasma 2010;57(4):355–359.
10. Baccarani M, Deininger MW, Rosti G, et al. European LeukemiaNet recommendations for the management of chronic myeloid leukemia: 2013. Blood 2013;122(6):872–884.
11. Beillard E, Pallisgaard N, van der Velden VH, et al. Evaluation of candidate control genes for diagnosis and residual disease detection in leukemic patients using ‘real-time’ quantitative reverse-transcriptase polymerase chain reaction (RQ-PCR) - a Europe against cancer program. Leukemia 2003;17(12):2474–2486.
12. Branford S, Cross NC, Hochhaus A, et al. Rationale for the recommendations for harmonizing current methodology for detecting BCR-ABL transcripts in patients with chronic myeloid leukaemia. Leukemia 2006;20(11):1925–1930.
13. Branford S, Fletcher L, Cross NC, et al. Desirable performance charac-teristics for BCR-ABL measurement on an international reporting scale to allow consistent interpretation of individual patient response and comparison of response rates between clinical trials. Blood 2008;112(8):3330–3338.
14. Zemanová K, Žižková H, Jurček T, et al. Chronická myeloidní leukemie-standardizace molekulárního monitorování hladiny transkriptů BCR--ABL1 v České republice. Transfuze Hematol dnes 2016;22(1):56–64.
15. Klamova H, Polakova KM, Muzik J, et al. Evaluation of 5-year imatinib treatment of 458 patients with CP-CML in routine clinical practice and prognostic impact of different BCR-ABL cutoff levels. Cancer Med 2013;2(2):216–225.
16. Hanfstein B, Muller MC, Hehlmann R, et al. Early molecular and cytogenetic response is predictive for long-term progression-free and overall survival in chronic myeloid leukemia (CML). Leukemia 2012;26(9):2096–2102.
17. Marin D, Ibrahim AR, Lucas C, et al. Assessment of BCR-ABL1 transcript levels at 3 months is the only requirement for predicting outcome for patients with chronic myeloid leukemia treated with tyrosine kinase inhibitors. J Clin Oncol 2012;30(3):232–238.
18. Soverini S, Hochhaus A, Nicolini FE, et al. BCR-ABL kinase domain mutation analysis in chronic myeloid leukemia patients treated with tyrosine kinase inhibitors: recommendations from an expert panel on behalf of European LeukemiaNet. Blood 2011;118(5):1208–1215.
19. Polakova KM, Polivkova V, Rulcova J, et al. Constant BCR-ABL transcript level >or=0.1% (IS) in patients with CML responding to imatinib with complete cytogenetic remission may indicate mutation analysis. Exp Hematol 2010;38(1):20–26.
20. Soverini S, De Benedittis C, Machova Polakova K, et al. Unraveling the complexity of tyrosine kinase inhibitor-resistant populations by ultra-deep sequencing of the BCR-ABL kinase domain. Blood 2013;122(9):1634–1648.
21. Machova Polakova K, Kulvait V, Benesova A, et al. Next-generation deep sequencing improves detection of BCR-ABL1 kinase domain mutations emerging under tyrosine kinase inhibitor treatment of chronic myeloid leukemia patients in chronic phase. J Cancer Res Clin Oncol 2015;141(5):887–899.
22. Vasiliou V, Vasiliou K, Nebert DW. Human ATP-binding cassette (ABC) transporter family. Human Genomics 2009;3(3):281–290.
23. Kuwazuru Y, Yoshimura A, Hanada S, et al. Expression of the multidrug transporter, P-glycoprotein, in chronic myelogenous leukaemia cells in blast crisis. Br J Haematol 1990;74(1):24–29.
24. Singh O, Chan JY, Lin K, Heng, Chowbay. SLC22A1-ABCB1 haplotype profiles predict imatinib pharmacokinetics in Asian patients with chronic myeloid leukemia. PloS ONE 2012;7(12):e51771.
25. He L, Vasiliou K, Nebert DW. Analysis and update of the human solute carrier (SLC) gene superfamily. Human Genomics 2009;3(2):195–206.
26. White DL, Saunders VA, 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 2007;110(12):4064–4072.
27. Gromicho M, Magalhaes M, Torres F, et al. Instability of mRNA expression signatures of drug transporters in chronic myeloid leukemia patients resistant to imatinib. Oncol Rep 2013;29(2):741–750.
28. Kim DH, Sriharsha L, Xu W, et al. Clinical relevance of a pharmacogenetic approach using multiple candidate genes to predict response and resistance to imatinib therapy in chronic myeloid leukemia. Clin Cancer Res 2009;15(14):4750–4758.
29. Angelini S, Soverini S, Ravegnini G, et al. Association between imatinib transporters and metabolizing enzymes genotype and response in newly diagnosed chronic myeloid leukemia patients receiving imatinib therapy. Haematologica 2013;98(2):193–200.
30. 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(5):2024–2027.
31. Ni LN, Li JY, Miao KR, et al. Multidrug resistance gene (MDR1) polymorphisms correlate with imatinib response in chronic myeloid leukemia. Med Oncol 2011;28(1):265–269.
32. Maffioli M, Camos M, Gaya A, et al. Correlation between genetic polymorphisms of the hOCT1 and MDR1 genes and the response to imatinib in patients newly diagnosed with chronic-phase chronic myeloid leukemia. Leuk Res 2011;35(8):1014–1019.
33. Hesselson SE, Matsson P, Shima JE, et al. Genetic variation in the proximal promoter of ABC and SLC superfamilies: liver and kidney specific expression and promoter activity predict variation. PloS ONE 2009;4(9):e6942.
34. Jaruskova M, Curik N, Hercog R, et al. Genotypes of SLC22A4 and SLC22A5 regulatory loci are predictive of the response of chronic myeloid leukemia patients to imatinib treatment. J Exp Clin Cancer Res 2017;36(1):55.
35. Hochhaus A, Dreyling M, Group EGW. Chronic myelogenous leukemia: ESMO clinical recommendations for the diagnosis, treatment and follow-up. Ann Oncol 2008;19(Suppl 2):ii63–64.
36. Hochhaus A, Larson RA, Guilhot F, et al. Long-term outcomes of imatinib treatment for chronic myeloid leukemia. New Engl J Med 2017;376(10):917–927.
37. Cortes JE, Saglio G, Kantarjian HM, et al. Final 5-year study results of DASISION: The dasatinib versus imatinib study in treatment-naive chronic myeloid leukemia patients trial. J Clin Oncol 2016;34(20):2333–2340.
38. Kalmanti L, Saussele S, Lauseker M, et al. Safety and efficacy of imatinib in CML over a period of 10 years: data from the randomized CML-study IV. Leukemia 2015;29(5):1123-1132.
39. Hochhaus A, Saglio G, Hughes TP, et al. Long-term benefits and risks of frontline nilotinib vs imatinib for chronic myeloid leukemia in chronic phase: 5-year update of the randomized ENESTnd trial. Leukemia 2016;30(5):1044–1054.
40. Baccarani M, Pane F, Rosti G, et al. Chronic myeloid leukemia: room for improvement? Haematologica 2017;102(7):1131–1133.
41. White H, Deprez L, Corbisier P, et al. A certified plasmid reference material for the standardisation of BCR-ABL1 mRNA quantification by real-time quantitative PCR. Leukemia 2015;29(2):369–376.
42. Cross NC, White HE, Ernst T, et al. Development and evaluation of a secondary reference panel for BCR-ABL1 quantification on the International Scale. Leukemia 2016;30(9):1844–1852.
43. Etienne G, Guilhot J, Rea D, et al. Long-term follow-up of the French Stop Imatinib (STIM1) Study in patients with chronic myeloid leukemia. J Clin Oncol 2017;35(3):298–305.
44. Mahon XF, Richter J, Guilhot J, et al. Iterim analysis of a pan European Stop Tyrosine Kinase Inhibitor Trial in CML: The EURO-SKI study. Blood 2014;124:Abs.151
45. Saussele S, Richter J, Guilhot J, et al. First iterim analysis of a Pan-European Stop Trial using standardized moolecular criteria: results of the EURO-SKI trial. Haematologica 2014;99:792.
46. Saussele S, Richter J, Hochhaus A, Mahon FX. The concept of treatment-free remission in chronic myeloid leukemia. Leukemia 2016;30(8):1638–1647.
47. Cross NC, White HE, Colomer D, et al. Laboratory recommendations for scoring deep molecular responses following treatment for chronic myeloid leukemia. Leukemia 2015;29(5):999–1003.
48. Palani R, Milojkovic D, Apperley JF. Managing pregnancy in chronic myeloid leukaemia. Ann Hematol 2015;94(Suppl 2):S167–176.
49. Milojkovic D, Apperley JF. How I treat leukemia during pregnancy. Blood 2014;123(7):974–984.
50. Abruzzese E, Trawinska MM, de Fabritiis P, Baccarani M. Management of pregnant chronic myeloid leukemia patients. Exp Rev Hematol 2016;9(8):781–791.
51. Klamova H, Markova M, Moravcova J, et al. Response to treatment in women with chronic myeloid leukemia during pregnancy and after delivery. Leuk Res 2009;33(11):1567–1569.
52. Polivkova V, Rohon P, Klamova H, et al. Interferon-alpha revisited: individualized treatment management eased the selective pressure of tyrosine kinase inhibitors on BCR-ABL1 mutations resulting in a molecular response in high-risk CML patients. PloS ONE 2016;11(5):e0155959.
53. Linhartova J, Hovorkova L, Soverini S, et al. Characterization of 46 patient-specific BCR-ABL1 fusions and detection of SNPs upstream and downstream the breakpoints in chronic myeloid leukemia using next generation sequencing. Mol Cancer 2015;14:89.
54.Cramer K, Nieborowska-Skorska M, Koptyra M, et al. BCR/ABL and other kinases from chronic myeloproliferative disorders stimulate single-strand annealing, an unfaithful DNA double-strand break repair. Cancer Res 2008;68(17):6884–6888.
55. Holyoake TL, Vetrie D. The chronic myeloid leukemia stem cell: stemming the tide of persistence. Blood 2017;129(12):1595–1606.
56. Chen XS, Sheller JR, Johnson EN, Funk CD. Role of leukotrienes revealed by targeted disruption of the 5-lipoxygenase gene. Nature 1994;372(6502):179–182.
57. Reya T, Morrison SJ, Clarke MF, Weissman IL. Stem cells, cancer, and cancer stem cells. Nature 2001;414(6859):105–111.
58. Saudy NS, Fawzy IM, Azmy E, Goda EF, Eneen A, Abdul Salam EM. BMI1 gene expression in myeloid leukemias and its impact on prognosis. Blood Cell Molec Dis 2014;53(4):194–198.
59. Morrison SJ, Uchida N, Weissman IL. The biology of hematopoietic stem cells. Annual review of cell and developmental biology. 1995;11:35–71.
60. Williams DA, Zheng Y, Cancelas JA. Rho GTPases and regulation of hematopoietic stem cell localization. Meth Enzymol 2008;439:365–393.
61. Hu Y, Chen Y, Douglas L, Li S. beta-Catenin is essential for survival of leukemic stem cells insensitive to kinase inhibition in mice with BCR--ABL-induced chronic myeloid leukemia. Leukemia 2009;23(1):109–116.
62. Gerber JM, Gucwa JL, Esopi D, et al. Genome-wide comparison of the transcriptomes of highly enriched normal and chronic myeloid leukemia stem and progenitor cell populations. Oncotarget 2013;4(5):715–728.
63. Passegue E, Jochum W, Schorpp-Kistner M, Mohle-Steinlein U, Wagner EF. Chronic myeloid leukemia with increased granulocyte progenitors in mice lacking junB expression in the myeloid lineage. Cell 2001;104(1):21–32.
64. 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(5):2093–2098.
65. Wang Z, Yuan H, Roth M, Stark JM, Bhatia R, Chen WY. SIRT1 deace-tylase promotes acquisition of genetic mutations for drug resistance in CML cells. Oncogene 2013;32(5):589–598.
66. Li L, Wang L, Li L, et al. Activation of p53 by SIRT1 inhibition enhances elimination of CML leukemia stem cells in combination with imatinib. Cancer Cell 2012;21(2):266–281.
67. Salati S, Salvestrini V, Carretta C, et al. Deregulated expression of miR-29a-3p, miR-494-3p and miR-660-5p affects sensitivity to tyrosine kinase inhibitors in CML leukemic stem cells. Oncotarget 2017;8(30):49451–49469.
68. Machova Polakova K, Lopotova T, Klamova H, et al. Expression patterns of microRNAs associated with CML phases and their disease related targets. Mol Cancer 2011;10:41.
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