Dynamics of chronic myeloid leukemia response to long-term targeted therapy reveal treatment effects on leukemic stem cells

Blood

Volumn 118, Issue 6, 2011, Pages 1622-1631

  Tang, Min ^a,b   Gonen, Mithat ^c   Quintas Cardama, Alfonso ^d   Cortes, Jorge ^d   Kantarjian, Hagop ^d   Field, Chani ^e   Hughes, Timothy P ^e   Branford, Susan ^e   Michor, Franziska ^a,b  

^a DANA FARBER CANCER INSTITUTE   (United States)

^b HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^c MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

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

^e UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BCR ABL PROTEIN; BCR ABL1 PROTEIN; IMATINIB; NILOTINIB; UNCLASSIFIED DRUG;

ARTICLE; CELL DIFFERENTIATION; CHRONIC MYELOID LEUKEMIA; CONTROLLED STUDY; FEMALE; FOLLOW UP; HUMAN; HUMAN CELL; LEUKEMIA CELL; LONG TERM CARE; MAJOR CLINICAL STUDY; MALE; MATHEMATICAL MODEL; MOLECULARLY TARGETED THERAPY; PRIORITY JOURNAL; STEM CELL; TREATMENT RESPONSE; TURNOVER TIME;

EID: 80051609605     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2011-02-339267     Document Type: Article

References (44)

1. Druker BJ, 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(5):561-566.
2. Druker BJ, Talpaz M, Resta DJ, 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(14):1031-1037. (Pubitemid 32267972)
3. 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(9):645-652. (Pubitemid 34815868)
4. Branford S, Seymour JF, Grigg A, et al. 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):7080-7085. (Pubitemid 350276891)
5. Deininger M ea. 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 [abstract]. Blood. 2009;114(22):Abstract 1126.
6. Cortes JE, 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(3):392-397.
7. Cortes JE, Jones D, O'Brien S, et al. Results of dasatinib therapy in patients with early chronicphase chronic myeloid leukemia. J Clin Oncol. 2010;28(3):398-404.
8. Ross DM, Branford S, Seymour JF, 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):1719-1724.
9. Kaeda J, O'Shea D, Szydlo RM, 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;107:4171-4176. (Pubitemid 43726829)
10. Hughes TP, Branford S, White DL, et al. Impact of early dose intensity on cytogenetic and molecular responses in chronic-phase CML patients receiving 600 mg/day of imatinib as initial therapy. Blood. 2008;112(10):3965-3973.
11. Michor F, Hughes TP, Iwasa Y, et al. Dynamics of chronic myeloid leukaemia. Nature. 2005;435(7046):1267-1270. (Pubitemid 40943094)
12. 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):1181-1184. (Pubitemid 44527354)
13. Michor F. The long-term response to imatinib treatment of CML. Br J Cancer. 2007;96:679-680.
14. Mahon FX, Rea D, Guilhot J, 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):1029-1035.
15. Rousselot P, Huguet F, Rea D, 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. (Pubitemid 46053043)
16. Ross DDM, Grigg A, Schwarer A, 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 [abstract]. Blood. 2008;112(11):Abstract 1102.
17. Branford S, Hughes TP. Practical considerations for monitoring patients with chronic myeloid leukemia. Semin Hematol. 2010;47(4):327-334.
18. Kim HJ, Fay MP, Feuer EJ, Midthune DN. Permutation tests for joinpoint regression with applications to cancer rates. Stat Med. 2000;19(3):335-351. (Pubitemid 30070608)
19. Ross DM, Hughes TP, Melo JV. Do we have to kill the last CML cell? Leukemia. 2011;25(2):193-200.
20. Mauro MJ, Druker BJ, Maziarz RT. Divergent clinical outcome in two CML patients who discontinued imatinib therapy after achieving a molecular remission. Leuk Res. 2004;28(Suppl 1):S71-S73. (Pubitemid 38251502)
21. Cortes J, O'Brien S, Kantarjian H. Discontinuation of imatinib therapy after achieving a molecular response. Blood. 2004;104(7):2204-2205. (Pubitemid 39297882)
22. Marin D, Bazeos A, Mahon FX, et al. Adherence is the critical factor for achieving molecular responses in patients with chronic myeloid leukemia who achieve complete cytogenetic responses on imatinib. J Clin Oncol. 2010;28(14):2381-2388.
23. Elowitz MB, Levine AJ, Siggia ED, Swain PS. Stochastic gene expression in a single cell. Science. 2002;297(5584):1183-1186. (Pubitemid 36193353)
24. Becskei A, Kaufmann BB, van Oudenaarden A. Contributions of low molecule number and chromosomal positioning to stochastic gene expression. Nat Genet. 2005;37(9):937-944. (Pubitemid 43086149)
25. Kaern M, Elston TC, Blake WJ, Collins JJ. Stochasticity in gene expression: from theories to phenotypes. Nat Rev Genet. 2005;6(6):451-464. (Pubitemid 40733890)
26. 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):1081-1084.
27. Barnes DJ, Palaiologou D, Panousopoulou E, 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):8912-8919. (Pubitemid 41377381)
28. Skaggs BJ, Gorre ME, Ryvkin A, et al. Phosphorylation of the ATP-binding loop directs oncogenicity of drug-resistant BCR-ABL mutants. Proc Natl Acad Sci U S A. 2006;103(51):19466-19471. (Pubitemid 46026054)
29. Notta F, Mullighan CG, Wang JC, et al. Evolution of human BCR-ABL1 lymphoblastic leukaemiainitiating cells. Nature. 2011;469(7330):362-367.
30. Anderson K, Lutz C, van Delft FW, et al. Genetic variegation of clonal architecture and propagating cells in leukaemia. Nature. 2011;469(7330):356-361.
31. 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(5):926-935. (Pubitemid 46672068)
32. Dorsey JF, Cunnick JM, Lanehart R, et al. Interleukin-3 protects Bcr-Abl-transformed hematopoietic progenitor cells from apoptosis induced by Bcr-Abl tyrosine kinase inhibitors. Leukemia. 2002;16(9):1589-1595.
33. Holyoake TL, Jiang X, Jorgensen HG, et al. Primitive quiescent leukemic cells from patients with chronic myeloid leukemia spontaneously initiate factor-independent growth in vitro in association with up-regulation of expression of interleukin-3. Blood. 2001;97(3):720-728. (Pubitemid 32113406)
34. Hirano N, Takahashi T, Ohtake S, et al. Expression of costimulatory molecules in human leukemias. Leukemia. 1996;10(7):1168-1176. (Pubitemid 26254022)
35. Yong AS, Szydlo RM, Goldman JM, Apperley JF, Melo JV. Molecular profiling of CD34+ cells identifies low expression of CD7, along with high expression of proteinase 3 or elastase, as predictors of longer survival in patients with CML. Blood. 2006;107(1):205-212. (Pubitemid 43053545)
36. Holyoake T, Jiang X, Eaves C, et al. Considerations for targeting malignant stem cells in leukemia: chronic myeloid leukemia. Blood. 1999;94:2056-2064. (Pubitemid 29430422)
37. 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(11):4532-4539. (Pubitemid 43801382)
38. Corbin AS, Agarwal A, Loriaux M, Cortes J, Deininger MW, Druker BJ. Human chronic myeloid leukemia stem cells are insensitive to imatinib despite inhibition of BCR-ABL activity. J Clin Invest. 2011;121(1):396-409.
39. Bottino D, Chia Y, Stein A, et al. Inference of imatinib (IM) effects on leukemic stem cell (SC) compartment via mathematical modeling of IRIS treatment response data [abstract]. ASCO Meeting Abstracts. 2009:7056.
40. Lange T, Bumm T, Mueller M, et al. Durability of molecular remission in chronic myeloid leukemia patients treated with imatinib vs allogeneic stem cell transplantation. Leukemia. 2005;19(7):1262-1265. (Pubitemid 40946013)
41. Kiladjian JJ, Cassinat B, Turlure P, et al. High molecular response rate of polycythemia vera patients treated with pegylated interferon alpha-2a. Blood. 2006;108(6):2037-2040. (Pubitemid 44395018)
42. Quintas-Cardama A, Kantarjian H, Manshouri T, et al. Pegylated interferon alfa-2a yields high rates of hematologic and molecular response in patients with advanced essential thrombocythemia and polycythemia vera. J Clin Oncol. 2009;27(32):5418-5424.
43. Alimena G, Breccia M, Luciano L, et al. Imatinib mesylate therapy in chronic myeloid leukemia patients in stable complete cytogenic response after interferon-alpha results in a very high complete molecular response rate. Leuk Res. 2008;32(2):255-261. (Pubitemid 351215539)
44. Angstreich GR, Matsui W, Huff CA, et al. Effects of imatinib and interferon on primitive chronic myeloid leukaemia progenitors. Br J Haematol. 2005;130(3):373-381. (Pubitemid 43899585)