Inhibition of MDR1 does not sensitize primitive chronic myeloid leukemia CD34+ cells to imatinib

Experimental Hematology

Volumn 37, Issue 6, 2009, Pages 692-700

  Hatziieremia, Sophia ^a   Jordanides, Niove E ^a   Holyoake, Tessa L ^a   Mountford, Joanne C ^a   Jørgensen, Heather G ^a  

^a Section of Experimental Haematology   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BCR ABL PROTEIN; CD34 ANTIGEN; CD38 ANTIGEN; CRK LIKE PROTEIN; IMATINIB; MULTIDRUG RESISTANCE PROTEIN 1; RHODAMINE 123; VALSPODAR;

APOPTOSIS; ARTICLE; CELL DIVISION; CELL PROLIFERATION; CELL VIABILITY; CHRONIC MYELOID LEUKEMIA; CONTROLLED STUDY; CYTOSTASIS; FLOW CYTOMETRY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN CELL; LEUKAPHERESIS; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ANTIGENS, CD34; APOPTOSIS; BIOLOGICAL TRANSPORT; CELL DIVISION; CELL SEPARATION; CYCLOSPORINS; DRUG RESISTANCE; HUMANS; K562 CELLS; LEUKAPHERESIS; LEUKEMIA, MYELOID, CHRONIC-PHASE; NEOPLASTIC STEM CELLS; P-GLYCOPROTEIN; PIPERAZINES; PYRIMIDINES; TUMOR CELLS, CULTURED;

EID: 67349280901     PISSN: 0301472X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.exphem.2009.02.006     Document Type: Article

References (49)

1. Druker B.J., Guilhot F., O'Brien S.G., et al. Five-year follow-up of patients receiving imatinib for chronic myeloid leukemia. N Engl J Med 355 (2006) 2408-2417
2. Hughes T., Deininger M., Hochhaus A., et al. Monitoring CML patients responding to treatment with tyrosine kinase inhibitors: review and recommendations for harmonizing current methodology for detecting BCR-ABL transcripts and kinase domain mutations and for expressing results. Blood 108 (2006) 28-37
3. Roumiantsev S., Shah N.P., Gorre M.E., et al. Clinical resistance to the kinase inhibitor STI-571 in chronic myeloid leukemia by mutation of Tyr-253 in the Abl kinase domain P-loop. Proc Natl Acad Sci U S A 99 (2002) 10700-10705
4. 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 293 (2001) 876-880
5. Swords R., Quinn J., Fay M., O'Donnell R., Goldman J., and Murphy P.T. CML clonal evolution with resistance to single agent imatinib therapy. Clin Lab Haematol 27 (2005) 347-349
6. 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 106 (2005) 2128-2137
7. Quintás-Cardama A., Kantarjian H., and Cortes J. Targeting ABL and SRC kinases in chronic myeloid leukemia: experience with dasatinib. Future Oncol 2 (2006) 655-665
8. Melo J.V., and Chuah C. Resistance to imatinib mesylate in chronic myeloid leukaemia. Cancer Lett 249 (2007) 121-132
9. Azam M., Latek R.R., and Daley G.Q. Mechanisms of autoinhibition and STI571/imatinib resistance revealed by mutagenesis of BCR-ABL. Cell 112 (2003) 831-843
10. Corbin A.S., La Rosee P., Stoffregen E.P., Druker B.J., and Deininger M.W. Several Bcr-Abl kinase domain mutants associated with imatinib mesylate resistance remain sensitive to imatinib. Blood 101 (2003) 4611-4614
11. Kantarjian H., Talpaz M., O'Brien S., et al. High-dose imatinib mesylate therapy in newly diagnosed Philadelphia chromosome-positive chronic phase chronic myeloid leukemia. Blood 103 (2004) 2873-2878
12. Talpaz M., Shah N.P., Kantarjian H., et al. Dasatinib in imatinib-resistant Philadelphia chromosome-positive leukemias. N Engl J Med 354 (2006) 2531-2541
13. Kantarjian H., Giles F., Wunderle L., et al. Nilotinib in imatinib-resistant CML and Philadelphia chromosome-positive ALL. N Engl J Med 354 (2006) 2542-2551
14. White D.L., Saunders V.A., 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 110 (2007) 4064-4072
15. White D.L., Saunders V.A., Dang P., et al. OCT-1-mediated influx is a key determinant of the intracellular uptake of imatinib but not nilotinib (AMN107): reduced OCT-1 activity is the cause of low in vitro sensitivity to imatinib. Blood 108 (2006) 697-704
16. Hegedus T., Orfi L., Seprodi A., Varadi A., Sarkadi B., and Keri G. Interaction of tyrosine kinase inhibitors with the human multidrug transporter proteins, MDR1 and MRP1. Biochim Biophys Acta 1587 (2002) 318-325
17. Shukla S., Sauna Z.E., and Ambudkar S.V. Evidence for the interaction of imatinib at the transport-substrate sites of the multidrug-resistance linked ABC drug transporters ABCB1 (P-glycoprotein) and ABCG2. Leukemia 22 (2008) 445-447
18. Hamada A., Miyano H., Watanabe H., and Saito H. Interaction of imatinib mesilate with human P-glycoprotein. J Pharmacol Exp Ther 307 (2003) 824-828
19. Dai H., Marbach P., Lemaire M., Hayes M., and Elmquist W.F. Distribution of STI-571 to the brain is limited by P-glycoprotein-mediated efflux. J Pharmacol Exp Ther 304 (2003) 1085-1092
20. Hirayama C., Watanabe H., Nakashima R., et al. Constitutive overexpression of P-glycoprotein, rather than breast cancer resistance protein or organic cation transporter 1, contributes to acquisition of imatinib-resistance in K562 Cells. Pharm Res 25 (2008) 827-835
21. llmer T., Schaich M., Platzbecker U., et al. P-glycoprotein-mediated drug efflux is a resistance mechanism of chronic myelogenous leukemia cells to treatment with imatinib mesylate. Leukemia 18 (2004) 401-408
22. Mahon F.X., Belloc F., Lagarde V., et al. MDR1 gene overexpression confers resistance to imatinib mesylate in leukemia cell line models. Blood 101 (2003) 2368-2373
23. Widmer N., Rumpold H., Untergasser G., Fayet A., Buclin T., and Decosterd L.A. Resistant reversal by RNAi silencing of MDR1 in CML cells associated with increase in imatinib intracellular levels. Leukemia 21 (2007) 1561-1562
24. Rumpold H., Wolf A.M., Gruenewald K., Gastl G., Gunsilius E., and Wolf D. RNAi-mediated knockdown of P-glycoprotein using a transposon-based vector system durably restores imatinib sensitivity in imatinib-resistant CML cell lines. Exp Hematol 33 (2005) 767-775
25. Ferrao P.T., Frost M.J., Siah S.P., and Ashman L.K. Overexpression of P-glycoprotein in K562 cells does not confer resistance to the growth inhibitory effects of imatinib (STI571) in vitro. Blood 102 (2003) 4499-4503
26. Zong Y., Zhou S., and Sorrentino B.P. Loss of P-glycoprotein expression in hematopoietic stem cells does not improve responses to imatinib in a murine model of chronic myelogenous leukemia. Leukemia 19 (2005) 1590-1596
27. Udomsakdi C., Eaves C.J., Swolin B., Reid D.S., Barnett M.J., and Eaves A.C. Rapid decline of chronic myeloid leukemic cells in long-term culture due to a defect at the leukemic stem cell level. Proc Natl Acad Sci U S A 89 (1990) 6192-6196
28. Holyoake T., Jiang X., Eaves C., and Eaves A. Isolation of a highly quiescent subpopulation of primitive leukemic cells in chronic myeloid leukemia. Blood 94 (1999) 2056-2064
29. Holyoake T.L., Jiang X., Jorgensen H.G., 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 97 (2001) 720-728
30. Copland M., Hamilton A., Elrick L.J., et al. Dasatinib (BMS-354825) targets an earlier progenitor population than imatinib in primary CML but does not eliminate the quiescent fraction. Blood 107 (2006) 4532-4539
31. Graham S.M., Jørgensen H.G., Allan E., et al. Primitive, quiescent, Philadelphia-positive stem cells from patients with chronic myeloid leukemia are insensitive to STI571 in vitro. Blood 99 (2002) 319-325
32. Larson R.A., Druker B.J., 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 111 (2008) 4022-4028
33. Jordanides N.E., Jorgensen H.G., Holyoake T.L., and Mountford J.C. Functional ABCG2 is overexpressed on primary CML CD34+ cells and is inhibited by imatinib mesylate. Blood 108 (2006) 1370-1373
34. Noonan K.E., Beck C., Holzmayer T.A., et al. Quantitative analysis of MDR1 (multidrug resistance) gene expression in human tumors by polymerase chain reaction. Proc Natl Acad Sci U S A 87 (1990) 7160-7164
35. Galimberti S., Guerrini F., Palumbo G.A., et al. Evaluation of BCRP and MDR-1 co-expression by quantitative molecular assessment in AML patients. Leuk Res 28 (2004) 367-372
36. Livak K.J., and Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C[T]) method. Methods 25 (2001) 402-408
37. Guetens G., Prenen H., De Boeck G., et al. Simultaneous determination of AMN107 and Imatinib (Gleevec, Glivec, STI571) in cultured tumour cells using an isocratic high-performance liquid chromatography procedure with UV detection. J Chromatogr B Analyt Technol Biomed Life Sci 846 (2007) 341-345
38. Robey R.W., Honjo Y., van de Laar A., et al. A functional assay for detection of the mitoxantrone resistance protein, MXR (ABCG2). Biochim Biophys Acta 1512 (2001) 171-182
39. Hamilton A., Elrick L., Myssina S., et al. BCR-ABL activity and its response to drugs can be determined in CD34 + CML stem cells by CrkL phosphorylation status using flow cytometry. Leukemia 20 (2006) 1035-1039
40. 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 21 (2007) 926-935
41. Thomas J., Wang L., Clark R.E., and Pirmohamed M. Active transport of imatinib into and out of cells: implications for drug resistance. Blood 104 (2004) 3739-3745
42. Stavrovskaya A., Turkina A., Sedyakhina N., et al. Prognostic value of p-glycoprotein and leukocyte differentiation antigens in chronic myeloid leukemia. Leuk Lymphoma 28 (1998) 469-482
43. Carter A., Dann E.J., Katz T., et al. Cells from chronic myelogenous leukaemia patients at presentation exhibit multidrug resistance not mediated by either MDR1 or MRP1. Br J Haematol 114 (2001) 581-590
44. White D.L., Saunders V.A., Quinn S.R., Manley P.W., and Hughes T.P. Imatinib increases the intracellular concentration of nilotinib, which may explain the observed synergy between these drugs. Blood 109 (2007) 3609-3610
45. Houghton P.J., Germain G.S., Harwood F.C., et al. Imatinib mesylate is a potent inhibitor of the ABCG2 (BCRP) transporter and reverses resistance to topotecan and SN-38 in vitro. Cancer Res 64 (2004) 2333-2337
46. Burger H., van Tol H., Boersma A.W., et al. Imatinib mesylate (STI571) is a substrate for the breast cancer resistance protein (BCRP)/ABCG2 drug pump. Blood 104 (2004) 2940-2942
47. Peng B., Hayes M., Resta D., et al. Pharmacokinetics and pharmacodynamics of imatinib in a phase I trial with chronic myeloid leukemia patients. J Clin Oncol 22 (2004) 935-942
48. Wang L., Giannoudis A., Lane S., Williamson P., Pirmohamed M., and Clark R.E. Expression of the uptake drug transporter hOCT1 is an important clinical determinant of the response to imatinib in chronic myeloid leukemia. Clin Pharmacol Ther 83 (2008) 258-264
49. Szakács G., Váradi A., Ozvegy-Laczka C., and Sarkadi B. The role of ABC transporters in drug absorption, distribution, metabolism, excretion and toxicity (ADME-Tox). Drug Discov Today 13 (2008) 379-393