Blocking cytokine signaling along with intense Bcr-Abl kinase inhibition induces apoptosis in primary CML progenitors

Leukemia

Volumn 24, Issue 4, 2010, Pages 771-778

  Hiwase, D K ^a,b,c   White, D L ^a,b,c   Powell, J A ^c,d   Saunders, V A ^a,c   Zrim, S A ^a,c   Frede, A K ^a,c   Guthridge, M A ^b,c,d   Lopez, A F ^b,c,d   D'Andrea, R J ^a,b,c   To, L B ^a,b,c   Melo, J V ^a,b,c   Kumar, S ^a,b,c   Hughes, T P ^a,b,c  

^a Division of Haematology   (Australia)

^b UNIVERSITY OF ADELAIDE   (Australia)

^c CENTRE FOR CANCER BIOLOGY   (Australia)

^d Division of Human Immunology   (Australia)

Author keywords

CML; Cytokines; Tyrosine kinase inhibitors

Indexed keywords

BCR ABL PROTEIN; DASATINIB; GRANULOCYTE COLONY STIMULATING FACTOR; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; GROWTH FACTOR; IMATINIB; JANUS KINASE; JANUS KINASE INHIBITOR; PROTEIN KINASE INHIBITOR; STAT5 PROTEIN;

APOPTOSIS; ARTICLE; CD34 SELECTION; CELL DEATH; CELL VIABILITY; CHRONIC MYELOID LEUKEMIA; COLONY FORMING CELL; CONTROLLED STUDY; DRUG POTENCY; DRUG RESISTANCE; DRUG SENSITIVITY; ENZYME INHIBITION; ENZYME REACTIVATION; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; ONCOGENE; PHARMACOLOGICAL BLOCKING; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

EID: 77950949255     PISSN: 08876924     EISSN: 14765551     Source Type: Journal    
DOI: 10.1038/leu.2009.299     Document Type: Article

References (37)

1. Rowley JD. Letter: A new consistent chromosomal abnormality in chronic myelogenous leukaemia identified by quinacrine fluorescence and Giemsa staining. Nature 1973; 243: 290-293.
2. Daley GQ, Van Etten RA, Baltimore D. Induction of chronic myelogenous leukemia in mice by the P210bcr/abl gene of the Philadelphia chromosome. Science 1990; 247: 824-830.
3. Lugo TG, Pendergast AM, Muller AJ, Witte ON. Tyrosine kinase activity and transformation potency of bcr-abl oncogene products. Science 1990; 247: 1079-1082.
4. Druker BJ, Guilhot F, O'Brien SG, Gathmann I, Kantarjian H, Gattermann N et al. Five-year follow-up of patients receiving imatinib for chronic myeloid leukemia. N Engl J Med 2006; 355: 2408-2417.
5. 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: 58-60.
6. Bocchia M, Ippoliti M, Gozzetti A, Abruzzese E, Calabrese S, Amabile M et al. CD34+/Ph+ cells are still detectable in chronic myeloid leukemia patients with sustained and prolonged complete cytogenetic remission during treatment with imatinib mesylate. Leukemia 2008; 22: 426-428.
7. Copland M, Hamilton A, Elrick LJ, Baird JW, Allan EK, Jordanides N 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.
8. Graham SM, Jorgensen HG, Allan E, Pearson C, Alcorn MJ, Richmond L 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.
9. Jorgensen HG, Allan EK, Jordanides NE, Mountford JC, Holyoake TL. Nilotinib exerts equipotent antiproliferative effects to imatinib and does not induce apoptosis in CD34+CML cells. Blood 2007; 109: 4016-4019.
10. Holtz MS, Forman SJ, Bhatia R. Nonproliferating CML CD34+ progenitors are resistant to apoptosis induced by a wide range of proapoptotic stimuli. Leukemia 2005; 19: 1034-1041.
11. Jorgensen HG, Allan EK, Graham SM, Godden JL, Richmond L, Elliott MA et al. Lonafarnib reduces the resistance of primitive quiescent CML cells to imatinib mesylate in vitro. Leukemia 2005; 19: 1184-1191.
12. Konig H, Copland M, Chu S, Jove R, Holyoake TL, Bhatia R. Effects of dasatinib on SRC kinase activity and downstream intracellular signaling in primitive chronic myelogenous leukemia hematopoie-tic cells. Cancer Res 2008; 68: 9624-9633.
13. Shah NP, Kasap C, Weier C, Balbas M, Nicoll JM, Bleickardt E et al. Transient potent BCR-ABL inhibition is sufficient to commit chronic myeloid leukemia cells irreversibly to apoptosis. Cancer Cell 2008; 14: 485-493.
14. Konig H, Holtz M, Modi H, Manley P, Holyoake TL, Forman SJ 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.
15. le Coutre P, Mologni L, Cleris L, Marchesi E, Buchdunger E, Giardini R et al. In vivo eradication of human BCR/ABL-positive leukemia cells with an ABL kinase inhibitor. J Natl Cancer Inst 1999; 91: 163-168.
16. Peng B, Hayes M, Resta D, Racine-Poon A, Druker BJ, Talpaz M et al. Pharmacokinetics and pharmacodynamics of imatinib in a phase I trial with chronic myeloid leukemia patients. J Clin Oncol 2004; 22: 935-942. (Pubitemid 41103606)
17. Cortes JE, Egorin MJ, Guilhot F, Molimard M, Mahon FX. Pharmacokinetic/pharmacodynamic correlation and blood-level testing in imatinib therapy for chronic myeloid leukemia. Leukemia 2009; 23: 1537-1544.
18. Hochhaus A, Muller MC, Radich J, Branford S, Kantarjian HM, Hanfstein B et al. Dasatinib-associated major molecular responses in patients with chronic myeloid leukemia in chronic phase following imatinib failure: response dynamics and predictive value. Leukemia 2009; 23: 1628-1633.
19. Shah NP, Kantarjian HM, Kim DW, Rea D, Dorlhiac-Llacer PE, Milone JH 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.
20. Snead JL, O'Hare T, Adrian LT, Eide CA, Lange T, Druker BJ et al. Acute dasatinib exposure commits Bcr-Abl-dependent cells to apoptosis. Blood 2009; 114: 3459-3463.
21. Hiwase DK, White DL, Saunders VA, Kumar S, Melo JV, Hughes TP. Short-term intense Bcr-Abl kinase inhibition with nilotinib is adequate to trigger cell death in BCR-ABL(+) cells. Leukemia 2009; 23: 1205-1206.
22. Hiwase DK, Saunders V, Hewett D, Frede A, Zrim S, Dang P et al. Dasatinib cellular uptake and efflux in chronic myeloid leukemia cells: therapeutic implications. Clin Cancer Res 2008; 14: 3881-3888.
23. White D, Saunders V, Lyons AB, Branford S, Grigg A, To LB et al. In vitro sensitivity to imatinib-induced inhibition of ABL kinase activity is predictive of molecular response in patients with de novo CML. Blood 2005; 106: 2520-2526.
24. Bullock J, Noory C, Men A, Ramchandani RLK. Clinical Pharmacology Review: Spycel, Dasatinib, Application number 21-986. US Food and Drug Administration, Center for Drug Evaluation and Research 2006, http://www.fda.gov/ohrms/dockets/ ac/06/briefing/2006-4220-B1-01BristolMyersSquibb-Background.pdf.
25. Jiang X, Zhao Y, Smith C, Gasparetto M, Turhan A, Eaves A et al. Chronic myeloid leukemia stem cells possess multiple unique features of resistance to BCR-ABL targeted therapies. Leukemia 2007; 21: 926-935.
26. Misaghian N, Ligresti G, Steelman LS, Bertrand FE, Basecke J, Libra M et al. Targeting the leukemic stem cell: the Holy Grail of leukemia therapy. Leukemia 2009; 23: 25-42.
27. Jordanides NE, Jorgensen HG, Holyoake TL, Mountford JC. Functional ABCG2 is overexpressed on primary CML CD34+ cells and is inhibited by imatinib mesylate. Blood 2006; 108: 1370-1373.
28. Burchert A, Wang Y, Cai D, von Bubnoff N, Paschka P, Muller-Brusselbach S et al. Compensatory PI3-kinase/Akt/mTor activation regulates imatinib resistance development. Leukemia 2005; 19: 1774-1782.
29. Wang Y, Cai D, Brendel C, Barett C, Erben P, Manley PW et al. Adaptive secretion of granulocyte-macrophage colony-stimulating factor (GM-CSF) mediates imatinib and nilotinib resistance in BCR/ABL+ progenitors via JAK-2/STAT-5 pathway activation. Blood 2007; 109: 2147-2155.
30. 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.
31. Jiang X, Lopez A, Holyoake T, Eaves A, Eaves C. Autocrine production and action of IL-3 and granulocyte colony-stimulating factor in chronic myeloid leukemia. Proc Natl Acad Sci USA 1999; 96: 12804-12809.
32. Tian SS, Lamb P, Seidel HM, Stein RB, Rosen J. Rapid activation of the STAT3 transcription factor by granulocyte colony-stimulating factor. Blood 1994; 84: 1760-1764.
33. Bashey A, Healy L, Marshall CJ. Proliferative but not nonproli-ferative responses to granulocyte colony-stimulating factor are associated with rapid activation of the p21ras/MAP kinase signalling pathway. Blood 1994; 83: 949-957.
34. Dong F, Larner AC. Activation of Akt kinase by granulocyte colony-stimulating factor (G-CSF): evidence for the role of a tyrosine kinase activity distinct from the Janus kinases. Blood 2000; 95: 1656-1662.
35. Belloc F, Airiau K, Jeanneteau M, Garcia M, Guerin E, Lippert E et al. The stem cell factor-c-KIT pathway must be inhibited to enable apoptosis induced by BCR-ABL inhibitors in chronic myelogenous leukemia cells. Leukemia 2009; 23: 679-685.
36. Chalandon Y, Jiang X, Loutet S, Eaves AC, Eaves CJ. Growth autonomy and lineage switching in BCR-ABL-transduced human cord blood cells depend on different functional domains of BCR-ABL. Leukemia 2004; 18: 1006-1012.
37. Liu J, Joha S, Idziorek T, Corm S, Hetuin D, Philippe N et al. BCR-ABL mutants spread resistance to non-mutated cells through a paracrine mechanism. Leukemia 2008; 22: 791-799.