Destabilization of Bcr-Abl/Jak2 network by a Jak2/Abl kinase inhibitor ON044580 overcomes drug resistance in blast crisis chronic myelogenous leukemia (CML)

Genes and Cancer

Volumn 1, Issue 4, 2010, Pages 346-359

  Samanta, Ajoy K ^a   Chakraborty, Sandip N ^a   Wang, Yan ^a   Schlette, Ellen ^a   Premkumar Reddy, E ^b,c   Arlinghaus, Ralph B ^a  

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

^b TEMPLE UNIVERSITY   (United States)

^c MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

Apoptosis; Bcr Abl; CML; Drug resistance; Jak2

Indexed keywords

ABELSON KINASE; ALPHA BENZOYLSTYRYLBENZYLSULFIDE; ANTINEOPLASTIC AGENT; BCR ABL PROTEIN; HEAT SHOCK PROTEIN 90; IMATINIB; JANUS KINASE 2; ON 044580; PROTEIN TYROSINE KINASE INHIBITOR; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; BLAST CELL CRISIS; CANCER CELL CULTURE; CANCER RESISTANCE; CELL LYSATE; CHRONIC MYELOID LEUKEMIA; COLUMN CHROMATOGRAPHY; CONTROLLED STUDY; DRUG TARGETING; ENZYME INHIBITION; ENZYME SUBSTRATE; GEL FILTRATION CHROMATOGRAPHY; HUMAN; HUMAN CELL; IN VITRO STUDY; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

PYRONIA TITHONUS;

EID: 79952449224     PISSN: 19476019     EISSN: 19476027     Source Type: Journal    
DOI: 10.1177/1947601910372232     Document Type: Article

References (63)

1. Rudkin CT, Hungerford DA, Nowell PC. DNA contents of chromosome Ph1 and chromosome 21 in human chronic granulocytic leukemia. Science. 1964;144:1229-31.
2. Rowley JD. A new consistent chromosomal abnormality in chronic myelogenous leukaemia identified by quinacrine fluorescence and Giemsa staining [letter]. Nature. 1973;243(5405):290-3.
3. Sawyers CL. Chronic myeloid leukemia. N Engl J Med. 1999; 340(17):1330-40.
4. Pendergast AM, Quilliam LA, Cripe LD, Bassing CH, Dai Z, Li N, et al. BCR-ABL-induced oncogenesis is mediated by direct interaction with the SH2 domain of the GRB-2 adaptor protein. Cell.1993;75(1):175-85.
5. Puil L, Liu J, Gish G, Mbamalu G, Bowtell D, Pelicci PG, et al. Bcr- Abl oncoproteins bind directly to activators of the Ras signalling pathway. Embo J. 1994;13(4):764-73.
6. Ilaria RL Jr, Hawley RG, Van Etten RA. Dominant negative mutants implicate STAT5 in myeloid cell proliferation and neutrophil differentiation. Blood. 1999;93(12):4154-66.
7. Klejman A, Schreiner SJ, Nieborowska-Skorska M, Slupianek A, Wilson M, Smithgall TE, et al. The Src family kinase Hck couples BCR/ABL to STAT5 activation in myeloid leukemia cells. Embo J.2002;21(21):5766-74.
8. Wilson-Rawls J, Xie S, Liu J, Laneuville P, Arlinghaus RB. P210 Bcr-Abl interacts with the interleukin 3 receptor beta(c) subunit and constitutively induces its tyrosine phosphorylation. Cancer Res.1996;56(15):3426-30.
9. Xie S, Wang Y, Liu J, Sun T, Wilson MB, Smithgall TE, et al. Involvement of Jak2 tyrosine phosphorylation in Bcr-Abl transformation. Oncogene. 2001;20(43):6188-95.
10. 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(8):3167-74.
11. Shah NP, Nicoll JM, Nagar B, Gorre ME, Paquette RL, Kuriyan J, et al. Multiple BCR-ABL kinase domain mutations confer polyclonal resistance to the tyrosine kinase inhibitor imatinib (STI571) in chronic phase and blast crisis chronic myeloid leukemia. Cancer Cell. 2002;2(2):117-25.
12. Branford S, Rudzki Z, Walsh S, Parkinson I, Grigg A, Szer J, et al. Detection of BCR-ABL mutations in patients with CML treated with imatinib is virtually always accompanied by clinical resistance, and mutations in the ATP phosphate-binding loop (P-loop) are associated with a poor prognosis. Blood. 2003;102(1):276-83.
13. Quintas-Cardama A, Kantarjian H, Jones D, Nicaise C, O'Brien S, Giles F, et al. Dasatinib (BMS-354825) is active in Philadelphia chromosome- positive chronic myelogenous leukemia after imatinib and nilotinib (AMN107) therapy failure. Blood. 2007;109(2):497-9.
14. Gorre ME, Ellwood-Yen K, Chiosis G, Rosen N, Sawyers CL. BCR-ABL point mutants isolated from patients with imatinib mesylate-resistant chronic myeloid leukemia remain sensitive to inhibitors of the BCR-ABL chaperone heat shock protein 90. Blood. 2002;100(8):3041-4.
15. Donato NJ, Wu JY, Stapley J, Gallick G, Lin H, Arlinghaus R, et al. BCR-ABL independence and LYN kinase overexpression in chronic myelogenous leukemia cells selected for resistance to STI571. Blood.2003;101(2):690-8.
16. Donato NJ, Wu JY, Stapley J, Lin H, Arlinghaus R, Aggarwal BB, et al. Imatinib mesylate resistance through BCR-ABL independence in chronic myelogenous leukemia. Cancer Res. 2004;64(2):672-7.
17. Radich JP. The biology of CML blast crisis. Hematology Am Soc Hematol Educ Program. 2007;2007:384-91.
18. Calabretta B, Perrotti D. The biology of CML blast crisis. Blood.2004;103(11):4010-22.
19. Stuart SA, Minami Y, Wang JY. The CML stem cell: evolution of the progenitor. Cell Cycle. 2009;8(9):1338-43.
20. Jorgensen HG, Holyoake TL. Characterization of cancer stem cells in chronic myeloid leukaemia. Biochem Soc Trans. 2007;35(pt 5):1347-51.
21. Ilaria RL Jr. Pathobiology of lymphoid and myeloid blast crisis and management issues. Hematology Am Soc Hematol Educ Program.2005:188-94.
22. Melo JV, Barnes DJ. Chronic myeloid leukaemia as a model of disease evolution in human cancer. Nat Rev Cancer. 2007;7(6):441-53.
23. Hochhaus A. Management of Bcr-Abl-positive leukemias with dasatinib. Expert Rev Anticancer Ther. 2007;7(11):1529-36.
24. Cortes J, Rousselot P, Kim DW, Ritchie E, Hamerschlak N, Coutre S, et al. Dasatinib induces complete hematologic and cytogenetic responses in patients with imatinib-resistant or -intolerant chronic myeloid leukemia in blast crisis. Blood. 2007;109(8):3207-13.
25. Soverini S, Martinielli G, Colarossi S, Gnani A, Castagnetti F, Rosti G, et al. Presence or the emergence of a F317L BCR-ABL mutation may be associated with resistance to dasatanib in Philadelphia chromosome- positive leukemia. J Clin Oncol. 2006;24(33):e51-2.
26. Soverini S, Martinelli G, Colarossi S, Gnani A, Rondoni M, Castagnetti F, et al. Second-line treatment with dasatinib in patients resistant to imatinib can select novel inhibitor-specific BCR-ABL mutants in Ph+ALL. Lancet Oncol. 2007;8(3):273-4.
27. Weisberg E, Manley PW, Cowan-Jacob SW, Hochhaus A, Griffin JD. Second generation inhibitors of BCR-ABL for the treatment of imatinibresistant chronic myeloid leukaemia. Nat Rev Cancer. 2007;7(5):345-56.
28. Neviani P, Santhanam R, Trotta R, Notari M, Blaser BW, Liu S, et al. The tumor suppressor PP2A is functionally inactivated in blast crisis CML through the inhibitory activity of the BCR/ABL-regulated SET protein. Cancer Cell. 2005;8(5):355-68.
29. Perrotti D, Neviani P. ReSETting PP2A tumour suppressor activity in blast crisis and imatinib-resistant chronic myelogenous leukaemia. Br J Cancer. 2006;95(7):775-81.
30. Xie S, Lin H, Sun T, Arlinghaus RB. Jak2 is involved in c-Myc induction by Bcr-Abl. Oncogene. 2002;21(47):7137-46.
31. Samanta AK, Lin H, Sun T, Kantarjian H, Arlinghaus RB. Janus kinase 2: a critical target in chronic myelogenous leukemia. Cancer Res. 2006;66(13):6468-72.
32. Samanta AK, Chakraborty SN, Wang Y, Kantarjian H, Sun X, Hood J, et al. Jak2 inhibition deactivates Lyn kinase through the SET-PP2A-SHP1 pathway, causing apoptosis in drug-resistant cells from chronic myelogenous leukemia patients. Oncogene.2009;28(14):1669-81.
33. Whitesell L, Lindquist SL. HSP90 and the chaperoning of cancer. Nat Rev Cancer. 2005;5(10):761-72.
34. Maloney A, Workman P. HSP90 as a new therapeutic target for cancer therapy: the story unfolds. Expert Opin Biol Ther. 2002;2(1):3-24.
35. Chaudhury S, Welch TR, Blagg BS. Hsp90 as a target for drug development. ChemMedChem. 2006;1(12):1331-40.
36. Neckers L, Mimnaugh E, Schulte TW. Hsp90 as an anti-cancer target. Drug Resist Updat. 1999;2(3):165-72.
37. Goetz MP, Toft DO, Ames MM, Erlichman C. The Hsp90 chaperone complex as a novel target for cancer therapy. Ann Oncol.2003;14(8):1169-76.
38. Neckers L, Neckers K. Heat-shock protein 90 inhibitors as novel cancer chemotherapeutic agents. Expert Opin Emerg Drugs.2002;7(2):277-88.
39. Xu W, Yuan X, Jung YJ, Yang Y, Basso A, Rosen N, et al. The heat shock protein 90 inhibitor geldanamycin and the ErbB inhibitor ZD1839 promote rapid PP1 phosphatase-dependent inactivation of AKT in ErbB2 overexpressing breast cancer cells. Cancer Res.2003;63(22):7777-84.
40. Neckers L, Neckers K. Heat-shock protein 90 inhibitors as novel cancer chemotherapeutics: an update. Expert Opin Emerg Drugs.2005;10(1):137-49.
41. Blagosklonny MV, Fojo T, Bhalla KN, Kim JS, Trepel JB, Figg WD, et al. The Hsp90 inhibitor geldanamycin selectively sensitizes Bcr- Abl-expressing leukemia cells to cytotoxic chemotherapy. Leukemia.2001;15(10):1537-43.
42. Jatiani SS, Cosenza SC, Reddy MVR, Ha JH, Baker SJ, Samanta AK, et al. A non-ATP-competitive dual inhibitor of JAK2V617F and BCRABLT315I kinases: elucidation of a novel therapeutic spectrum based on substrate competitive inhibition. Genes Cancer. 2010;1(4):[IN PRESS].
43. Pardanani A, Hood J, Lasho T, Levine RL, Martin MB, Noronha G, et al. TG101209, a small molecule JAK2-selective kinase inhibitor potently inhibits myeloproliferative disorder-associated JAK2V617F and MPLW515L/K mutations. Leukemia. 2007;21(8):1658-68.
44. Sandberg EM, Ma X, He K, Frank SJ, Ostrov DA, Sayeski PP. Identification of 1,2,3,4,5,6-hexabromocyclohexane as a small molecule inhibitor of jak2 tyrosine kinase autophosphorylation [correction of autophophorylation]. J Med Chem. 2005;48(7):2526-33.
45. Shiotsu Y, Soga S, Akinaga S. Heat shock protein 90-antagonist destabilizes Bcr-Abl/HSP90 chaperone complex. Leuk Lymphoma.2002;43(5):961-8.
46. Wu LX, Xu JH, Zhang KZ, Lin Q, Huang XW, Wen CX, et al. Disruption of the Bcr-Abl/Hsp90 protein complex: a possible mechanism to inhibit Bcr-Abl-positive human leukemic blasts by novobiocin. Leukemia.2008;22(7):1402-1409.
47. Kamal A, Boehm MF, Burrows FJ. Therapeutic and diagnostic implications of Hsp90 activation. Trends Mol Med. 2004;10(6): 283-90.
48. Zuehlke A, Johnson JL. Hsp90 and co-chaperones twist the functions of diverse client proteins. Biopolymers. 2010;93(3):211-7.
49. Tsuruma R, Ohbayashi N, Kamitani S, Ikeda O, Sato N, Muromoto R, et al. Physical and functional interactions between STAT3 and KAP1. Oncogene. 2008;27(21):3054-9.
50. Bhattacharya S, Ray RM, Johnson LR. STAT3-mediated transcription of Bcl-2, Mcl-1 and c-IAP2 prevents apoptosis in polyamine-depleted cells. Biochem J. 2005;392(pt 2):335-44.
51. Samanta AK, Huang HJ, Bast RC Jr, Liao WS. Overexpression of MEKK3 confers resistance to apoptosis through activation of NFkappaB. J Biol Chem. 2004;279(9):7576-83.
52. Solit DB, Scher HI, Rosen N. Hsp90 as a therapeutic target in prostate cancer. Semin Oncol. 2003;30(5):709-16.
53. Csermely P, Schnaider T, Soti C, Prohaszka Z, Nardai G. The 90-kDa molecular chaperone family: structure, function, and clinical applications. A comprehensive review. Pharmacol Ther. 1998;79(2):129-68.
54. Usmani SZ, Bona R, Li Z. 17 AAG for HSP90 inhibition in cancer: from bench to bedside. Curr Mol Med. 2009;9(5):654-64.
55. Scheibel T, Buchner J. The Hsp90 complex: a super-chaperone machine as a novel drug target. Biochem Pharmacol. 1998;56(6):675-82.
56. Kamal A, Thao L, Sensintaffar J, Zhang L, Boehm MF, Fritz LC, et al. A high-affinity conformation of Hsp90 confers tumour selectivity on Hsp90 inhibitors. Nature. 2003;425(6956):407-10.
57. Kaneko Y, Ohno H, Imamura Y, Kohno S, Miyazaki Y. The effects of an hsp90 inhibitor on the paradoxical effect. Jpn J Infect Dis.2009;62(5):392-3.
58. Johnson BD, Chadli A, Felts SJ, Bouhouche I, Catelli MG, Toft DO. Hsp90 chaperone activity requires the full-length protein and interaction among its multiple domains. J Biol Chem. 2000;275(42): 32499-507.
59. Isaacs JS, Xu W, Neckers L. Heat shock protein 90 as a molecular target for cancer therapeutics. Cancer Cell. 2003;3(3):213-7.
60. Eustace BK, Jay DG. Extracellular roles for the molecular chaperone, hsp90. Cell Cycle. 2004;3(9):1098-100.
61. Ammirante M, Rosati A, Gentilella A, Festa M, Petrella A, Marzullo L, et al. The activity of hsp90 alpha promoter is regulated by NFkappa B transcription factors. Oncogene. 2008;27(8):1175-8.
62. George P, Bali P, Annavarapu S, Scuto A, Fiskus W, Guo F, et al. Combination of the histone deacetylase inhibitor LBH589 and the hsp90 inhibitor 17-AAG is highly active against human CMLBC cells and AML cells with activating mutation of FLT-3. Blood.2005;105(4):1768-76.
63. Bartholomeusz GA, Talpaz M, Kapuria V, Kong LY, Wang S, Estrov Z, et al. Activation of a novel Bcr/Abl destruction pathway by WP1130 induces apoptosis of chronic myelogenous leukemia cells. Blood. 2007;109(8):3470-8.