Selection pressure exerted by imatinib therapy leads to disparate outcomes of imatinib discontinuation trials

Haematologica

Volumn 97, Issue 10, 2012, Pages 1553-1561

  Tang, Min ^a   Foo, Jasmine ^b   Gönen, Mithat ^c   Guilhot, Joëlle ^d   Mahon, François Xavier ^e,f,g   Michor, Franziska ^a  

^a HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

^c MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^d POITIERS UNIVERSITY HOSPITAL   (France)

^e BORDEAUX UNIVERSITY HOSPITAL   (France)

^f UNIVERSITÉ DE BORDEAUX   (France)

^g INSERM   (France)

Author keywords

Biostatistics; Chronic myeloid leukemia; Mathematical modeling; Minimal residual disease; Targeted therapy

Indexed keywords

BCR ABL PROTEIN; IMATINIB;

ARTICLE; CANCER GROWTH; CANCER STEM CELL; CANCER SURVIVAL; CELL DENSITY; CELL DIFFERENTIATION; CELL RENEWAL; CHRONIC MYELOID LEUKEMIA; CLINICAL TRIAL (TOPIC); DRUG RESPONSE; GENETIC HETEROGENEITY; HUMAN; IMMUNE RESPONSE; LEUKEMIA RELAPSE; MATHEMATICAL MODEL; PHENOTYPE; TREATMENT OUTCOME; TREATMENT RESPONSE;

ANTINEOPLASTIC AGENTS; BENZAMIDES; HUMANS; LEUKEMIA, MYELOGENOUS, CHRONIC, BCR-ABL POSITIVE; MODELS, THEORETICAL; PIPERAZINES; PROTEIN KINASE INHIBITORS; PYRIMIDINES; RECURRENCE; TREATMENT OUTCOME;

EID: 84867250391     PISSN: 03906078     EISSN: 15928721     Source Type: Journal    
DOI: 10.3324/haematol.2012.062844     Document Type: Article

References (31)

1. Druker BJ, Talpaz M, Resta DJ, Peng B, Buchdunger E, Ford JM. Efficacy and safety of a specific inhibitor of the BCR-ABL tyrosine kinase in chronic myeloid leukemia. N Engl J Med. 2001;344(14):1031-7
2. Kantarjian H, Sawyers C, Hochhaus A, Guilhot F, Schiffer C, Gambacorti-Passerini C, et al. Hematologic and cytogenetic responses to imatinib mesylate in chronic myelogenous leukemia. N Engl J Med. 2002;346(9):645-52
3. Branford S, Seymour JF, Grigg A, Arthur C, Rudzki Z, Lynch K, Hughes T. BCR-ABL messenger RNA levels continue to decline in patients with chronic phase chronic myeloid leukemia treated with imatinib for more than 5 years and approximately half of all first-line treated patients have stable undetectable BCR-ABL using strict sensitivity criteria. Clin Cancer Res. 2007;13 (23):7080-5
4. Deininger M, O'Brien SG, Guilhot F, Goldman JM, Hochhaus A, Hughes TP, 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. ASH Annual Meeting Abstracts. 2009;114(22): 1126
5. Mahon FX, Réa D, Guilhot J, Guilhot F, Huguet F, Nicolini F, et al.; Intergroupe Français des Leucémies Myéloïdes Chroniques. Discontinuation of imatinib in patients with chronic myeloid leukaemia who have maintained complete molecular remission for at least 2 years: the prospective, multicentre Stop Imatinib (STIM) trial. Lancet Oncol. 2010;11(11):1029-35
6. Rousselot P, Huguet F, Rea D, Legros L, Cayuela JM, Maarek O, et al. Imatinib mesylate discontinuation in patients with chronic myelogenous leukemia in complete molecular remission for more than 2 years. Blood. 2007;109(1):58-60
7. Ross DM, Grigg A, Schwarer A, Arthur C, Loftus K, Mills AK, et al. The majority of chronic myeloid leukaemia patients who cease imatinib after achieving a sustained complete molecular response (CMR) remain in CMR, and any relapses occur early. ASH Annual Meeting Abstracts. 2008;112(11): 1102
8. Ross DM, Branford S, Seymour JF, Schwarer AP, Arthur C, Bartley PA, et al. Patients with chronic myeloid leukemia who maintain a complete molecular response after stopping imatinib treatment have evidence of persistent leukemia by DNA PCR. Leukemia. 2010;24(10):1719-24
9. Michor F, Hughes TP, Iwasa Y, Branford S, Shah NP, Sawyers CL, et al. Dynamics of chronic myeloid leukaemia. Nature. 2005; 435(7046):1267-70
10. Roeder I, Horn M, Glauche I, Hochhaus A, Mueller MC, Loeffler M. Dynamic modeling of imatinib-treated chronic myeloid leukemia: functional insights and clinical implications. Nat Med. 2006;12(10):1181-4
11. Dingli D, Michor F. Successful therapy must eradicate cancer stem cells. Stem Cells. 2006;24(12):2603-10
12. Komarova NL, Wodarz D. Effect of cellular quiescence on the success of targeted CML therapy. PLoS ONE. 2007;2(10):e990
13. Horn M, Loeffler M, Roeder I. Mathematical modeling of genesis and treatment of chronic myeloid leukemia. Cells Tissues Organs. 2008;188(1-2):236-47
14. Kim PS, Lee PP, Levy D. Dynamics and potential impact of the immune response to chronic myelogenous leukemia. PLoS Comput Biol. 2008; 4(6): e1000095
15. Kim PS, Lee PP, Levy D. A PDE model for imatinib-treated chronic myelogenous leukemia. Bull Math Biol. 2008;70(7):1994-2016
16. Komarova NL, Katouli AA, Wodarz D. Combination of two but not three current targeted drugs can improve therapy of chronic myeloid leukemia. PLoS One. 2009;4(2):e4423
17. Foo J, Drummond MW, Clarkson B, Holyoake T, Michor F. Eradication of chronic myeloid leukemia stem cells: a novel mathematical model predicts no therapeutic benefit of adding G-CSF to imatinib. PLoS Comput Biol. 2009; 5(9): e1000503
18. Lenaerts T, Pacheco JM, Traulsen A, Dingli D. Tyrosine kinase inhibitor therapy can cure chronic myeloid leukemia without hitting leukemic stem cells. Haematologica. 2010; 95(6):900-7
19. Michor F. The long-term response to imatinib treatment of CML. Br J Cancer. 2007;96:679-80
20. Elowitz MB, Levine AJ, Siggia ED, Swain PS. Stochastic gene expression in a single cell. Science. 2002;297(5584):1183-6
21. Becskei A, Kaufmann BB, van Oudenaarden A. Contributions of low molecule number and chromosomal positioning to stochastic gene expression. Nat Genet. 2005;37(9):937-44
22. Kaern M, Elston TC, Blake WJ, Collins JJ. Stochasticity in gene expression: from theories to phenotypes. Nat Rev Genet. 2005;6 (6):451-64
23. Feinerman O, Veiga J, Dorfman JR, Germain RN, Altan-Bonnet G. Variability and robustness in T cell activation from regulated heterogeneity in protein levels. Science. 2008;321(5892):1081-4
24. Barnes DJ, Palaiologou D, Panousopoulou E, Schultheis B, Yong AS, Wong A, et al. Bcr-Abl expression levels determine the rate of development of resistance to imatinib mesylate in chronic myeloid leukemia. Cancer Res. 2005;65 (19):8912-9
25. Skaggs BJ, Gorre ME, Ryvkin A, Burgess MR, Xie Y, Han Y, et al. Phosphorylation of the ATP-binding loop directs oncogenicity of drug-resistant BCR-ABL mutants. Proc Natl Acad Sci USA. 2006;103(51):19466-71
26. Notta F, Mullighan CG, Wang JC, Poeppl A, Doulatov S, Phillips LA, et al. Evolution of human BCR-ABL1 lymphoblastic leukaemiainitiating cells. Nature. 2011;469 (7330):362-7
27. Anderson K, Lutz C, van Delft FW, Bateman CM, Guo Y, Colman SM, et al. Genetic variegation of clonal architecture and propagating cells in leukaemia. Nature. 2011;469 (7330):356-61
28. Ross DM, Hughes TP, Melo JV. Do we have to kill the last CML cell? Leukemia. 2011;25(2):193-200
29. Kaeda J, O'Shea D, Szydlo RM, Olavarria E, Dazzi F, Marin D, et al. Serial measurement of BCR-ABL transcripts in the peripheral blood after allogeneic stem cell transplantation for chronic myeloid leukemia: an attempt to define patients who may not require further therapy. Blood. 2006;107 (10):4171-6
30. Kantarjian H, Shah NP, Hochhaus A, Cortes J, Shah S, Ayala M, et al. Dasatinib versus imatinib in newly diagnosed chronic-phase chronic myeloid leukemia. N Engl J Med. 2010;362(24):2260-70
31. Saglio G, Kim DW, Issaragrisil S, le Coutre P, Etienne G, Lobo C, et al. ENESTnd Investigators. Nilotinib versus imatinib for newly diagnosed chronic myeloid leukemia. N Engl J Med. 2010;362(24):2251-9.