Vorinostat synergistically potentiates MK-0457 lethality in chronic myelogenous leukemia cells sensitive and resistant to imatinib mesylate

Blood

Volumn 112, Issue 3, 2008, Pages 793-804

  Dai, Yun ^a   Chen, Shuang ^a   Venditti, Charis A ^a   Pei, Xin Yan ^a   Nguyen, Tri K ^a   Dent, Paul ^a   Grant, Steven ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AURORA A KINASE; AURORA B KINASE; BCR ABL PROTEIN; BIM PROTEIN; CYCLOPROPANECARBOXYLIC ACID [4 [4 (4 METHYL 1 PIPERAZINYL) 6 (5 METHYL 2H PYRAZOL 3 YLAMINO) 2 PYRIMIDINYLTHIO]PHENYL]AMIDE; IMATINIB; VORINOSTAT; ANTINEOPLASTIC AGENT; APOPTOSIS REGULATORY PROTEIN; AURORA KINASE; BCL 2 LIKE PROTEIN 11; BCL-2-LIKE PROTEIN 11; HYDROXAMIC ACID; MEMBRANE PROTEIN; ONCOPROTEIN; PIPERAZINE DERIVATIVE; PROTEIN SERINE THREONINE KINASE; PYRIMIDINE DERIVATIVE;

APOPTOSIS; ARTICLE; CANCER RESISTANCE; CELL CYCLE REGULATION; CHRONIC MYELOID LEUKEMIA; CONTROLLED STUDY; DOWN REGULATION; DRUG ACTIVITY; DRUG POTENTIATION; ENZYME INHIBITION; HUMAN; HUMAN CELL; LEUKEMIA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; ANIMAL; DRUG ANTAGONISM; DRUG RESISTANCE; TUMOR CELL LINE;

ANIMALS; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; APOPTOSIS REGULATORY PROTEINS; CELL LINE, TUMOR; DRUG RESISTANCE, NEOPLASM; DRUG SYNERGISM; FUSION PROTEINS, BCR-ABL; HUMANS; HYDROXAMIC ACIDS; LEUKEMIA, MYELOGENOUS, CHRONIC, BCR-ABL POSITIVE; MEMBRANE PROTEINS; PIPERAZINES; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS; PYRIMIDINES;

EID: 50949133899     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2007-10-116376     Document Type: Article

References (65)

1. Druker BJ, O'Brien SG, Cortes J, Radich J. Chronic myelogenous leukemia. Hematology Am Soc Hematol Educ Program. 2002;111-135.
2. 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.
3. Druker BJ, Guilhot F, O'Brien SG, et al. Five-year follow-up of patients receiving imatinib for chronic myeloid leukemia. N Engl J Med. 2006;355:2408-2417.
4. Mughal TI, Goldman JM. Chronic myeloid leukemia: current status and controversies. Oncology (Williston Park). 2004;18:837-844, 847.
5. Ritchie E, Nichols G. Mechanisms of resistance to imatinib in CML patients: a paradigm for the advantages and pitfalls of molecularly targeted therapy. Curr Cancer Drug Targets. 2006;6:645-657.
6. O'Hare T, Eide CA, Deininger MW. Bcr-Abl kinase domain mutations, drug resistance and the road to a cure of chronic myeloid leukemia. Blood. 2007:110:2242-2249.
7. 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;7:345-356.
8. O'Hare T, Walters DK, Stoffregen EP, et al. In vitro activity of Bcr-Abl inhibitors AMN107 and BMS-354825 against clinically relevant imatinibresistant Abl kinase domain mutants. Cancer Res. 2005;65:4500-4505.
9. Harrington EA, Bebbington D, Moore J, et al. VX-680, a potent and selective small-molecule inhibitor of the Aurora kinases, suppresses tumor growth in vivo. Nat Med. 2004;10:262-267.
10. Fu J, Bian M, Jiang Q, Zhang C. Roles of Aurora kinases in mitosis and tumorigenesis. Mol Cancer Res. 2007;5:1-10.
11. Cheetham GM, Charlton PA, Golee JM, Pollard JR. Structural basis for potent inhibition of the Aurora kinases and aT315I multi-drug resistant mutant form of Abl kinase by VX-680. Cancer Lett. 2007:251:323-329.
12. Young MA, Shah NP, Chao LH, et al. Structure of the kinase domain of an imatinib-resistant Abl mutant in complex with the Aurora kinase inhibitor VX-680. Cancer Res. 2006;66:1007-1014.
13. Carter TA, Wodicka LM, Shah NP, et al. Inhibition of drug-resistant mutants of ABL, KIT, and EGF receptor kinases. Proc Natl Acad Sci USA. 2005; 102:11011-11016.
14. Lee EC, FrolovA, Li R, Ayala G, Greenberg NM. Targeting Aurora kinases for the treatment of prostate cancer. Cancer Res. 2006:66:4996-5002.
15. Gizatullin F, Yao Y, Kung V, et al. The Aurora kinase inhibitor VX-680 induces endoreduplication and apoptosis preferentially in cells with compromised p53-dependent postmitotic checkpoint function. Cancer Res. 2006;66:7668-7677. 16. Tuma RS. With targeted drugs, chronic
16. myelogenous leukemia therapy may follow HIVs model. J Natl Cancer Inst. 2007;99:192-194.
17. Shah NP, Skaggs BJ, Branford S, et al. Sequential ABL kinase inhibitor therapy selects for compound drug-resistant BCR-ABL mutations with altered oncogenic potency. J Glin Invest. 2007; 117:2562-2569.
18. Giles FJ, Cortes J, Jones D, et al. MK-0457, a novel kinase inhibitor is active in patients with chronic myeloid leukemia or acute lymphocytic leukemia with the T315I BCR-ABL mutation. Blood. 2007;109:500-502.
19. Soverini S, lacobucci I, Baccarani M, Martinelli G. Targeted therapy and the T3151 mutation in Philadelphia-positive leukemias. Haematologica. 2007:92:437-439.
20. Marks PA. Discovery and development of SAHA as an anticancer agent. Oncogene. 2007;26: 1351-1356.
21. Grant S, Easley C, Kirkpatrick P. Vorinostat. Nat Rev Drug Discov. 2007;6:21-22.
22. Xu WS, Parmigiani RB, Marks PA. Histone deacetylase inhibitors: molecular mechanisms of action. Oncogene. 2007;26:5541-5552.
23. Lindemann RK, Newbold A, Whitecross KF, et al. Analysis of the apoptotic and therapeutic activities of histone deacetylase inhibitors by using a mouse model of B cell lymphoma. Proc Natl Acad Sci U S A. 2007;104:8071-8076.
24. Insinga A, Monestiroli S, Ronzoni S, et al. Inhibitors of histone deacetylases induce tumor-selective apoptosis through activation of the death receptor pathway. Nat Med. 2005;11:71-76.
25. Rosato RR, Almenara JA, Grant S. The histone deacetylase inhibitor MS-275 promotes differentiation or apoptosis in human leukemia cells through a process regulated by generation of reactive oxygen species and induction of p21 CIP1/WAF1 1. Cancer Res. 2003;63:3637-3645.
26. Shao Y, Gao Z, Marks PA, Jiang X. Apoptotic and autophagic cell death induced by histone deacetylase inhibitors. Proc Natl Acad Sci U S A. 2004;101:18030-18035.
27. Carew JS, Nawrocki ST Kahue CN, et al. Targeting autophagy augments the anticancer activity of the histone deacetylase inhibitor SAHAto overcome Bcr-Abl-mediated drug resistance. Blood. 2007;110:313-322.
28. Xu WS, Perez G, Ngo L, Gui CY, Marks PA. Induction of polyploidy by histone deacetylase inhibitor: a pathway for antitumor effects. Cancer Res. 2005;65:7832-7839.
29. Scroggins BT Robzyk K, Wang D, et al. An acetylation site in the middle domain of Hsp90 regulates chaperone function. Mol Cell. 2007;25:151-159.
30. Bali P, Pranpat M, Bradner J, et al. Inhibition of histone deacetylase 6 acetylates and disrupts the chaperone function of heat shock protein 90: a novel basis of antileukemia activity of histone deacetylase inhibitors. J Biol Chem. 2005;280: 26729-26734.31. Rahmani M, Yu C, Dai Y, et al. Coadministration of the heat shock protein 90 antagonist
31. 17-allylamino-17-demethoxygeldanamycin with sub-eroylanilide hydroxamic acid or sodium butyrate synergistically induces apoptosis in human leukemia cells. Cancer Res. 2003;63:8420-8427.
32. Workman P, Burrows F, Neckers L, Rosen N. Drugging the cancer chaperone HSP90: Combinatorial therapeutic exploitation of oncogene addiction and tumor stress. Ann N Y Acad Sci. 2007; 1113:202-216.
33. Yu C, Rahmani M, Almenara J, et al. Histone deacetylase inhibitors promote STI571-mediated apoptosis in STI571-sensitive and -resistant Bcr/Abl+ human myeloid leukemia cells. Gancer Res. 2003;63:2118-2126.
34. Fiskus W, Pranpat M, Balasis M, et al. Cotreatment with vorinostat (suberoylanilide hydroxamic acid) enhances activity of dasatinib (BMS-354825) against imatinib mesylate-sensitive or imatinib mesylate-resistant chronic myelogenous leukemia cells. Clin Cancer Res. 2006;12:5869-5878.
35. Nimmanapalli R, Fuino L, Bali P, et al. Histone deacetylase inhibitor LAQ824 both lowers expression and promotes proteasomal degradation of Bcr-Abl and induces apoptosis of imatinib mesylate-sensitive or -refractory chronic myelogenous leukemia-blast crisis cells. Cancer Res. 2003;63:5126-5135.
36. Qiu L, Burgess A, Fairlie DP, et al. Histone deacetylase inhibitors trigger a G2 checkpoint in normal cells that is defective in tumor cells. Mol Biol Cell. 2000;11:2069-2083.
37. Lozzio CB, Lozzio BB. Human chronic myelogenous leukemia cell-line with positive Philadelphia chromosome. Blood. 1975;45:321-334.
38. Dai Y, Rahmani M, Corey SJ, Dent P, Grant S. A Bcr/Abl-independent, Lyn-dependent form of imatinib mesylate (STI-571 ) resistance is associated with altered expression of Bcl-2. J Biol Ghem. 2004;279:34227-34239.
39. Nguyen TK, Rahmani M, Harada H, Dent P, Grant S. MEK1/2 inhibitors sensitize Bcr/Abl+ human leukemia cells to the dual Abl/Src inhibitor BMS-354/825. Blood. 2007;109:4006-4015.
40. O'Hare T, Druker BJ. BIRB-796 is not an effective ABL(T315I) inhibitor. Nat Biotechnol. 2005;23: 1209-1210.
41. Daley GQ, Baltimore D. Transformation of an interleukin 3-dependent hematopoietic cell line by the chronic myelogenous leukemia-specific P210bcr/abl protein. Proc Natl Acad Sci U S A. 1988;85:9312-9316.
42. Nguyen TK, Rahmani M, Gao N, et al. Synergistic interactions between DMAG and mitogen-activated protein kinase kinase 1/2 inhibitors in Bcr/abl+ leukemia cells sensitive and resistant to imatinib mesylate. Clin Cancer Res. 2006;12: 2239-2247.
43. Dai Y, Rahmani M, Dent P, Grant S. Blockade of histone deacetylase inhibitor-induced RelA/p65 acetylation and NF-{kappa}B activation potentiates apoptosis in leukemia cells through a process mediated by oxidative damage, XIAP downregulation, and c-Jun N-terminal kinase 1 activation. Mol Cell Biol. 2005;25:5429-5444.
44. Dai Y, Rahmani M, Grant S. An intact NF-kappaB pathway is required for histone deacetylase inhibitor-induced G1 arrest and maturation in U937 human myeloid leukemia cells. Cell Cycle. 2003; 2:467-472.
45. Dai Y, Rahmani M, Pei XY, Dent P, Grant S. Bortezomib and flavopiridol interact synergistically to induce apoptosis in chronic myeloid leukemia cells resistant to imatinib mesylate through both Bcr/Abl-dependent and -independent mechanisms. Blood. 2004;104:509-518.
46. Donato NJ, Wu JY, Stapley J, et al. BCR-ABL independence and LYN kinase overexpression in chronic myelogenous leukemia cells selected for resistance to STI571. Blood. 2003;101:690-698.
47. Ito T, Tanaka H, Kimura A. Establishment and characterization of a novel imatinib-sensitive chronic myeloid leukemia cell line MYL, and an imatinib-resistant subline MYL-R showing overexpression of Lyn. Eur J Haematol. 2007;78:417-431.
48. Sattler M, Mohi MG, Pride YB, et al. Critical role for Gab2 in transformation by BCR/ABL. Cancer Cell. 2002;1:479-492.
49. Mortlock AA, Keen NJ, Jung FH, et al. Progress in the development of selective inhibitors of aurora kinases. Curr Top Med Chem. 2005;5:807-821.
50. Zhao Y, Tan J, Zhuang L, et al. Inhibitors of histone deacetylases target the Rb-E2F1 pathway for apoptosis induction through activation of proapoptotic protein Bim. Proc Natl Acad Sci U S A. 2005:102:16090-16095.51. O'Connor QA, Heaney ML, Schwartz L, et al. Clinical experience with intravenous and oral formulations of the novel histone deacetylase
51. inhibitor suberoylanilide hydroxamic acid in patients with advanced hematologic malignancies. J Clin Oncol. 2006;24:166-173.
52. 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;100:3041-3044.
53. Grbovic OM, Basso AD, Sawai A, et al. V600E B-Raf requires the Hsp90 chaperone for stability and is degraded in response to Hsp90 inhibitors. Proc Natl Acad Sci U S A. 2006;103:57-62.
54. Ptasznik A, Nakata Y, Kalota A, Emerson SG, Gewirtz AM. Short interfering RNA (siRNA) targeting the Lyn kinase induces apoptosis in primary, and drug-resistant, BCR-ABL1 (+) leukemia cells. Nat Med. 2004;10:1187-1189.
55. Hirota T, Lipp JJ, Toh BH, Peters JM. Histone H3 serine 10 phosphorylation by Aurora B causes HP1 dissociation from heterochromatin. Nature. 2005;438:1176-1180.
56. Warrener R, Beamish H, Burgess A, et al. Tumor cell-selective cytotoxicity by targeting cell cycle checkpoints. FASEB J. 2003;17:1550-1552.
57. Magnaghi-Jaulin L, Eot-Houllier G, Fulcrand G, Jaulin C. Histone deacetylase inhibitors induce premature sister chromatid separation and override the mitotic spindle assembly checkpoint. Cancer Res. 2007;67:6360-6367.
58. Li Y, Kao GD, Garcia BA, et al. A novel histone deacetylase pathway regulates mitosis by modulating Aurora B kinase activity. Genes Dev. 2006; 20:2566-2579.59. Zhang XD, Gillespie SK, Borrow JM, Hersey P.
59. The histone deacetylase inhibitor suberic bishydroxamate regulates the expression of multiple apoptotic mediators and induces mitochondria-dependent apoptosis of melanoma cells. Mol Cancer Ther. 2004;3:425-435.
60. Tan J. Zhuang L. Jiang X, et al. Apoptosis signal-regulating kinase 1 is a direct target of E2F1 and contributes to histone deacetylase inhibitor-induced apoptosis through positive feedback regulation of E2F1 apoptotic activity. J Biol Chem. 2006;281:10508-10515.
61. Inoue S, Riley J, Gant TW, Dyer MJ, Cohen GM. Apoptosis induced by histone deacetylase inhibitors in leukemic cells is mediated by Bim and Noxa. Leukemia. 2007;21:1773-1782.
62. Fiskus W, Pranpat M, Bali P, et al. Combined effects of novel tyrosine kinase inhibitor AMN107 and histone deacetylase inhibitor LBH589 against Bcr-Abl-expressing human leukemia cells. Blood. 2006;108:645-652.
63. Leao M, Anderton E, Wade M, Meekings K, Allday MJ. Epstein-barr virus-induced resistance to drugs that activate the mitotic spindle assembly checkpoint in Burkitt's lymphoma cells. J Virol. 2007;81:248-260.
64. Aichberger KJ; Mayerhofer M; Krauth MT et al. Low-level expression of proapoptotic Bcl-2-interacting mediator in leukemic cells in patients with chronic myeloid leukemia: role of BCRZABL, characterization of underlying signaling pathways, and reexpression by novel pharmacologic compounds. Cancer Res. 2005;65:9436-9444.
65. Kuribara R, Honda H, Matsui H, et al. Roles of Bim in apoptosis of normal and Bcr-Abl-expressing hematopoietic progenitors. Mol Cell Biol. 2004;24:6172-6183.