The new iodoacetamidobenzofuran derivative TR120 decreases STAT5 expression and induces antitumor effects in imatinib-sensitive and imatinib-resistant BCR-ABL-expressing leukemia cells

Anti-Cancer Drugs

Volumn 24, Issue 4, 2013, Pages 384-393

  Grimaudo, Stefania ^a   Meli, Maria ^a   Di Cristina, Antonietta ^a   Ferro, Arianna ^a   Pipitone, Maria R ^a   Romagnoli, Romeo ^b   Simoni, Daniele ^b   Dieli, Francesco ^a   Tolomeo, Manlio ^a  

^a UNIVERSITY OF PALERMO   (Italy)

^b UNIVERSITY OF FERRARA   (Italy)

Author keywords

BCR ABL; chronic myeloid leukemia; imatinib resistance; STAT5; tyrosine kinase inhibitors

Indexed keywords

3 IODOACETYLAMINO 6 METHOXYBENZOFURAN 2 YL(3,5 TRIMETHOXYPHENYL)METHANONE; ANTINEOPLASTIC AGENT; BCR ABL PROTEIN; BENZOFURAN DERIVATIVE; CYCLIN D1; IMATINIB; PROTEIN BCL XL; STAT5 PROTEIN; TR 120; UNCLASSIFIED DRUG;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER INHIBITION; CELL CYCLE G0 PHASE; CELL CYCLE G1 PHASE; CELL STRAIN K 562; CHRONIC MYELOID LEUKEMIA; CONTROLLED STUDY; DRUG CYTOTOXICITY; HUMAN; HUMAN CELL; LEUKEMIA CELL; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANTINEOPLASTIC AGENTS; APOPTOSIS; BCL-X PROTEIN; BENZAMIDES; BENZOFURANS; BENZOPHENONES; BONE MARROW CELLS; CELL LINE, TUMOR; COLONY-FORMING UNITS ASSAY; CYCLIN D1; DOWN-REGULATION; DRUG RESISTANCE, NEOPLASM; DRUG SYNERGISM; FUSION PROTEINS, BCR-ABL; G0 PHASE; G1 PHASE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, BCL-1; GENES, BCL-2; HUMANS; K562 CELLS; LEUKEMIA, MYELOGENOUS, CHRONIC, BCR-ABL POSITIVE; NECROSIS; NEOPLASM PROTEINS; PIPERAZINES; PROTO-ONCOGENE PROTEINS C-BCL-2; PYRIMIDINES; STAT5 TRANSCRIPTION FACTOR;

EID: 84875056379     PISSN: 09594973     EISSN: 14735741     Source Type: Journal    
DOI: 10.1097/CAD.0b013e32835e64a0     Document Type: Article

References (46)

1. Groffen J, Stephenson JR, Heisterkamp N, de Klein A, Bartram CR, Grosveld G. Philadelphia chromosomal breakpoints are clustered within a limited region, BCR, on chromosome 22. Cell 1984; 36:93-99
2. Li S, Ilaria RL Jr, Million RP, Daley GQ, Van Etten RA. The P190, P210, and P230 forms of the BCR/ABL oncogene induce a similar chronic myeloid leukemia-like syndrome in mice but have different lymphoid leukemogenic activity. J Exp Med 1999; 189:1399-1412
3. Sirard C, Laneuville P, Dick JE. Expression of BCR-ABL abrogates factordependent growth of human hematopoietic M07E cells by an autocrine mechanism. Blood 1994; 83:1575-1585
4. Skorski T, Nieborowska-Skorska M, Wlodarski P, Wasik M, Trotta R, Kanakaraj P, et al. The SH3 domain contributes to BCR/ABL-dependent leukemogenesis in vivo: Role in adhesion, invasion, and homing. Blood 1998; 91:406-418
5. Bedi A, Zehnbauer BA, Barber JP, Sharkis SJ, Jones RJ. Inhibition of apoptosis by BCR-ABL in chronic myeloid leukemia. Blood 1994; 83:2038-2044
6. Druker BJ, Talpaz M, Resta DJ, Peng B, Buchdunger E, Ford JM, et al. Efficacy and safety of a specific inhibitor of the BCR-ABL tyrosine kinase in chronic myeloid leukemia. N Engl J Med 2001; 344:1031-1037
7. Gorre ME, Mohammed M, Ellwood K, Hsu N, Paquette R, Rao PN, Sawyers CL. Clinical resistance to STI-571 cancer therapy caused by BCR-ABL gene mutation or amplification. Science 2001; 293:876-880
8. Quintas-Cardama A, Kantarjian H, Cortes J. Flying under the radar: The new wave of BCR-ABL inhibitors. Nat Rev Drug Discov 2007; 6:834-848
9. Fava C, Kantarjian H, Cortes J. Molecular resistance: An early indicator for treatment change? Clin Lymphoma Myeloma Leuk 2012; 12:79-87
10. Roychowdhury S, Talpaz M. Managing resistance in chronic myeloid leukemia. Blood Rev 2011; 25:279-290
11. Chu S, Li L, Singh H, Bhatia R. BCR-Tyrosine 177 plays an essential role in Ras and Akt activation and in human hematopoietic progenitor transformation in chronic myelogenous leukemia. Cancer Res 2007; 67:7045-7053
12. Horita M, Andreu EJ, Benito A, Arbona C, Sanz C, Benet I, et al. Blockade of the BCR-ABL kinase activity induces apoptosis of chronic myelogenous leukemia cells by suppressing signal transducer and activator of transcription 5-dependent expression of Bcl-xL. J Exp Med 2000; 191: 977-984
13. Cirinna M, Trotta R, Salomoni P, Kossev P,Wasik M, Perrotti D, Calabretta B. Bcl-2 expression restores the leukemogenic potential of a BCR/ABL mutant defective in transformation. Blood 2000; 96:3915-3921
14. Hoover RR, Gerlach MJ, Koh EY, Daley GQ. Cooperative and redundant effects of STAT5 and Ras signaling in BCR/ABL transformed hematopoietic cells. Oncogene 2001; 20:5826-5835
15. Ilaria RL Jr, Van Etten RA. P210 and P190 (BCR/ABL) induce the tyrosine phosphorylation and DNA binding activity of multiple specific STAT family members. J Biol Chem 1996; 271:31704-31710
16. Carlesso N, Frank DA, Griffin JD. Tyrosyl phosphorylation and DNA binding activity of signal transducers and activators of transcription (STAT) proteins in hematopoietic cell lines transformed by BCR/ABL. J Exp Med 1996; 183:811-820
17. Frank DA, Varticovski L. BCR/ABL leads to the constitutive activation of STAT proteins, and shares an epitope with tyrosine phosphorylated stats. Leukemia 1996; 10:1724-1730
18. Shuai K, Halpern J, ten Hoeve J, Rao X, Sawyers CL. Constitutive activation of STAT5 by the BCR-ABL oncogene in chronic myelogenous leukemia. Oncogene 1996; 13:247-254
19. Gesbert F, Griffin JD. BCR/ABL activates transcription of the Bcl-X gene through STAT5. Blood 2000; 96:2269-2276
20. Magne S, Caron S, Charon M, Rouyez MC, Dusanter-Fourt I. STAT5 and Oct-1 form a stable complex that modulates cyclin D1 expression. Mol Cell Biol 2003; 23:8934-8945
21. De Groot RP, Raaijmakers JA, Lammers JW, Koenderman L. STAT5- dependent CyclinD1 and Bcl-xL expression in BCR-ABL-Transformed cells. Mol Cell Biol Res Commun 2000; 3:299-305
22. Romagnoli R, Baraldi PG, Sarkar T, Carrion MD, Cruz-Lopez O, Lopez CaraC, et al. Synthesis and biological evaluation of 2-(30,40,50-Trimethoxybenzoyl)-3- N,N-dimethylamino benzo[b]furan derivatives as inhibitors of tubulin polymerization. Bioorg Med Chem 2008; 16:8419-8426
23. Webb JL. Effect of more than one inhibitor. Enzymes and Metabolic Inhibitors. New York, NY: Academic Press; 1963. pp. 66-79
24. Sanchez-Garcia I, Grutz G. Tumorigenic activity of the BCR-ABL oncogenes is mediated by BCL2. Proc Natl Acad Sci USA 1995; 92:5287-5291
25. Amarante-Mendes GP, McGahon AJ, Nishioka WK, Afar DE, Witte ON, Green DR. Bcl-2-independent BCR-ABL-mediated resistance to apoptosis:Protection is correlated with up regulation of Bcl-xL. Oncogene 1998; 16:1383-1390
26. Tauchi T, Sumi M, Nakajima A, Sashida G, Shimamoto T, Ohyashiki K. BCL-2 antisense oligonucleotide genasense is active against imatinib-resistant BCR-ABL-positive cells. Clin Cancer Res 2003; 9:4267-4273
27. Goff DA, Abrahamsson-Schairer A, Shih A, Black JM, Chuang R, Tesi RJ, et al. The broad spectrum Bcl-2 inhibitor apogossypol induces apoptosis and differentiation of blast crisis chronic myeloid leukemia stem cells. ASH Ann Meeting Abs 2009; 114:3275
28. Mak DH, Schober WD, Konopleva M, Cortes J, Kantarjian HM, Andreeff M, et al. Inhibition of Bcl-2/Bcl-xL promotes apoptosis in blast crisis CML including quiescent primitive progenitor cells regardless of cellular responses to tyrosine kinase inhibitors. ASH Ann Meeting Abs 2009; 114:646
29. Smith S. Anti-Bcl2 therapy in chronic myelogenous leukemia. Leuk Lymphoma 2008; 49:1232-1233
30. Tolomeo M, Dieli F, Gebbia N, Simoni D. Tyrosine kinase inhibitors for the treatment of chronic myeloid leukemia. Anticancer Agents Med Chem 2009; 9:853-863
31. Ye D,Wolff N, Li L, Zhang S, Ilaria RL Jr. STAT5 signaling is required for the efficient induction and maintenance of CML in mice. Blood 2006; 107:4917-4925
32. Nieborowska-Skorska M, Wasik MA, Slupianek A, Salomoni P, Kitamura T, Calabretta B, Skorski T. Signal transducer and activator of transcription (STAT)5 activation by BCR/ABL is dependent on intact Src homology (SH)3 and SH2 domains of BCR/ABL and is required for leukemogenesis. J Exp Med 1999; 189:1229-1242
33. Hoelbl A, Schuster C, Kovacic B, Zhu B,Wickre M, Hoelzl MA, et al. STAT5 is indispensable for the maintenance of BCR/ABL-positive leukaemia. EMBO Mol Med 2010; 2:98-110
34. Birkenkamp KU, Geugien M, Lemmink HH, KruijerW, Vellenga E. Regulation of constitutive STAT5 phosphorylation in acute myeloid leukemia blasts. Leukemia 2001; 15:1923-1931
35. Gouilleux-Gruart V, Gouilleux F, Desaint C, Claisse JF, Capiod JC, Delobel J, et al. STAT-related transcription factors are constitutively activated in peripheral blood cells from acute leukemia patients. Blood 1996; 87: 1692-1697
36. Spiekermann K, Pau M, Schwab R, Schmieja K, Franzrahe S, HiddemannW. Constitutive activation of STAT3 and STAT5 is induced by leukemic fusion proteins with protein tyrosine kinase activity and is sufficient for transformation of hematopoietic precursor cells. Exp Hematol 2002; 30:262-271
37. Lacout C, Pisani DF, Tulliez M, Gachelin FM, Vainchenker W, Villeval JL. JAK2V617F expression in murine hematopoietic cells leads to MPD mimicking human PV with secondary myelofibrosis. Blood 2006; 108:1652-1660
38. Wernig G, Mercher T, Okabe R, Levine RL, Lee BH, Gilliland DG. Expression of Jak2V617F causes a polycythemia vera-like disease with associated myelofibrosis in a murine bone marrow transplant model. Blood 2006; 107:4274-4281
39. Ihle JN. The STAT family in cytokine signaling. Curr Opin Cell Biol 2001; 13:211-217
40. Schindler C, Darnell JE Jr. Transcriptional responses to polypeptide ligands: The JAK-STAT pathway. Annu Rev Biochem 1995; 64:621-651
41. Warsch W, Kollmann K, Eckelhart E, Fajmann S, Cerny-Reiterer S, Holbl A, et al. High STAT5 levels mediate imatinib resistance and indicate disease progression in chronic myeloid leukemia. Blood 2011; 117:3409-3420
42. Nelson EA, Walker SR, Weisberg E, Bar-Natan M, Barrett R, Gashin LB, et al. The STAT5 inhibitor pimozide decreases survival of chronic myelogenous leukemia cells resistant to kinase inhibitors. Blood 2011; 117:3421-3429
43. 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; 121:396-409
44. Lopez-Perez M, Salazar EP. A role for the cytoskeleton in STAT5 activation in MCF7 human breast cancer cells stimulated with EGF. Int J Biochem Cell Biol 2006; 38:1716-1728
45. Gleason EL, Hogan JC, Stephens JM. Stabilization, not polymerization, of microtubules inhibits the nuclear translocation of STATs in adipocytes. Biochem Biophys Res Commun 2004; 325:716-718
46. Moser C, Lang SA, Mori A, Hellerbrand C, Schlitt HJ, Geissler EK, et al. ENMD-1198, a novel tubulin-binding agent reduces HIF-1alpha and STAT3 activity in human hepatocellular carcinoma (HCC) cells, and inhibits growth and vascularization in vivo. BMC Cancer 2008; 8:206-217