Triptolide inhibits Bcr-Abl transcription and induces apoptosis in STI571-resistant chronic myelogenous leukemia cells harboring T315I mutation

Clinical Cancer Research

Volumn 15, Issue 5, 2009, Pages 1686-1697

  Shi, Xianping ^a   Jin, Yanli ^a   Cheng, Chao ^b   Zhang, Hui ^d   Zou, Waiyi ^b   Zheng, Qin ^a   Lu, Zhongzheng ^a   Chen, Qi ^a   Lai, Yingrong ^c   Pan, Jingxuan ^a  

^a SUN YAT SEN UNIVERSITY   (China)

^b Department of Surgery ^*  (China)

^c SUN YAT SEN UNIVERSITY   (China)

^d UNIVERSITY OF TEXAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BCR ABL PROTEIN; CASPASE; IMATINIB; MESSENGER RNA; PROTEIN KINASE B; PROTEIN MCL 1; SURVIVIN; TRIPTOLIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CANCER GROWTH; CANCER RESISTANCE; CELL SURVIVAL; CHRONIC MYELOID LEUKEMIA; CONTROLLED STUDY; DOWN REGULATION; DRUG POTENCY; FEMALE; GENE MUTATION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; LEUKEMIA CELL; MALE; MOUSE; NONHUMAN; NUDE MOUSE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TUMOR XENOGRAFT;

ADOLESCENT; ADULT; AGED; ANIMALS; ANTINEOPLASTIC AGENTS, ALKYLATING; APOPTOSIS; BLOTTING, WESTERN; CELL CYCLE; CELL PROLIFERATION; DITERPENES; DRUG RESISTANCE, NEOPLASM; EPOXY COMPOUNDS; FEMALE; FLOW CYTOMETRY; FUSION PROTEINS, BCR-ABL; HUMANS; IMMUNOENZYME TECHNIQUES; LEUKEMIA, MYELOGENOUS, CHRONIC, BCR-ABL POSITIVE; MALE; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; MICE, INBRED BALB C; MICE, NUDE; MIDDLE AGED; MUTATION; PHENANTHRENES; PIPERAZINES; PROTEIN KINASE INHIBITORS; PROTEIN-TYROSINE KINASES; PROTO-ONCOGENE PROTEINS C-AKT; PROTO-ONCOGENE PROTEINS C-BCL-2; PYRIMIDINES; REACTIVE OXYGEN SPECIES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC; TRIPTERYGIUM; TUMOR CELLS, CULTURED; TUMOR STEM CELL ASSAY; XENOGRAFT MODEL ANTITUMOR ASSAYS; YOUNG ADULT;

EID: 63549123206     PISSN: 10780432     EISSN: None     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-08-2141     Document Type: Article

References (55)

1. Faderl S, Talpaz M, Estrov Z, O'Brien S, Kurzrock R, Kantarjian HM. The biology of chronic myeloid leukemia. N Engl J Med 1999;341:164-72.
2. Ren R. Mechanisms of BCR-ABL in the pathogenesis of chronic myelogenous leukaemia. Nat Rev Cancer 2005;5:172-83.
3. Melo JV, Barnes DJ. Chronic myeloid leukaemia as a model of disease evolution in human cancer. Nat Rev Cancer 2007;7:441 -53.
4. Quintas-Cardama A, Kantarjian H, Cortes J. Flying under the radar: the new wave of BCR-ABL inhibitors. Nat Rev Drug Discov2007;6:834-48.
5. Baselga J, Arribas J. Treating cancer's kinase 'addiction'. NatMed2004;10:786-7.
6. Druker BJ. Circumventing resistance to kinase-inhibitor therapy. N Engl J Med 2006;354:2594-6.
7. Druker BGF, O'Brien S, Larson R. Long-term benefits of imatinib (IM) for patients newly diagnosed with chronic myelogenous leukemia in chronic phase (CML-CP): the 5-year update from the IRIS study [Abstract]. J Clin Oncol 2006;24:18S.
8. Donato NJ, Wu JY, Stapley J, et al. BCR-ABL independence and LYN kinase overexpression in chronic myelogenous leukemia cells selected for resistance to
9. STI571. Blood2003;101:690-8.
10. Gambacorti-Passerini C, le Coutre P, Zucchetti M, D'Incalci M. Binding of imatinib by α (1)-acid glycoprotein. Blood2002;100:367-8;authorreply8-9.
11. Thomas J, Wang L, Clark RE, Pirmohamed M. Active transport of imatinib into and out of cells: implications fordrugresistance. Blood2004;104:3739-45.
12. Gorre ME, Mohammed M, Ellwood K, et al. Clinical resistance to STI-571 cancer therapy caused by BCR- ABL gene mutation or amplification. Science 2001; 293:876-80.
13. Hochhaus A, Kreil S, CorbinAS, etal.Molecularand chromosomal mechanisms of resistance to imatinib (STI571) therapy. Leukemia2002;16:2190-6.
14. Kantarjian HM, Talpaz M, Giles F, O'Brien S, Cortes J. New insights into the pathophysiology of chronic myeloid leukemia and imatinib resistance. Ann Intern Med 2006;145:913-23.
15. Morinaga K, Yamauchi T, Kimura S, Maekawa T, Ueda T. Overcoming imatinib resistance using Src inhibitor CGP76030, Abl inhibitor nilotinib and Abl/Lyn inhibitor INNO-406 in newly established K562 variants with BCR-ABL gene amplification. Int J Cancer 2008; 122:2621 -7.
16. Talpaz M, ShahN P, Kantarjian H, et al. Dasatinibin imatinib-resistant Philadelphia chromosome-positive leukemias. N Engl J Med 2006;354:2531 -41.
17. Chen R, Gandhi V, Plunkett W. A sequential blockade strategy for the design of combination therapies to overcome oncogene addiction in chronic myelogenous leukemia. Cancer Res 2006;66:10959-66.
18. Nimmanapalli R, Fuino L, Bali P, et al. Histone deacetylaseinhibitorLAQ824bothlowersexpression 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 -35.
19. Corson TW, Crews CM. Molecular understanding and modern application of traditional medicines: triumphs and trials. Cell 2007;130:769 -74.
20. Tao XL, Sun Y, Dong Y, et al. A prospective, controlled, double-blind, cross-over study of tripterygium wilfodii hook F in treatment of rheumatoid arthritis. Chin Med J (Engl) 1989;102:327-32.
21. Jiang X. Clinical observations on the use of the Chinese herb Tripterygium wilfordii Hook for the treatment of nephrotic syndrome. Pediatr Nephrol 1994;8:343-4.
22. Efferth T, Li PC, KonkimallaVS, Kaina B. From traditional Chinese medicine to rational cancer therapy. TrendsMol Med2007;13:353-61.
23. 22.Tao X, Schulze-Koops H, Ma L, Cai J, Mao Y, Lipsky PE. Effects of Tripterygium wilfordii hook F extractson induction of cyclooxygenase 2 activity and prostaglandin E2 production. Arthritis Rheum 1998;41: 130-8.
24. Fidler JM, Li K, Chung C, et al.PG490-88, aderivative of triptolide, causes tumor regression and sensitizes tumors to chemotherapy. Mol CancerTher 2003; 2:855-62.
25. Jiang XH, Wong BC, Lin MC, et al.Functional p53 is required for triptolide-induced apoptosis and AP-1and nuclear factor-κB activation in gastric cancer cells. Oncogene 2001;20:8009 -18.
26. Kupchan SM, Court WA, Dailey RG, Jr., Gilmore CJ, Bryan RF. Triptolide and tripdiolide, novel antileukemic diterpenoid triepoxides from Tripterygium wilfordii. J Am Chem Soc 1972;94:7194-5.
27. Carter BZ, Mak DH, SchoberWD, et al. Triptolide induces caspase-dependent cell death mediated via the mitochondrial pathway in leukemic cells. Blood 2006;108:630-7.
28. Yang S, Chen J, Guo Z, et al. Triptolide inhibits the growth and metastasis of solid tumors. Mol Cancer Ther 2003;2:65-72.
29. Phillips PA, Dudeja V, McCarroll JA, et al. Triptolide induces pancreatic cancer cell death via inhibition of heat shock protein 70. Cancer Res 2007;67:
30. 9407-16.
31. Lee KY, Chang W, Qiu D, Kao PN, Rosen GD. PG490 (triptolide) cooperates with tumor necrosis factor-α to induce apoptosis in tumor cells. J Biol
32. Chem1999;274:13451 -5.
33. Frese S, Pirnia F, Miescher D, et al. PG490-mediated sensitization of lung cancer cells to Apo2L/TRAIL- induced apoptosis requires activation of ERK2. Oncogene 2003;22:5427-35.
34. Kiviharju TM, Lecane PS, Sellers RG, Peehl DM. Antiproliferative and proapoptotic activities of triptolide (PG490), a natural product entering clinical trials, on primary cultures of human prostatic epithelial cells. Clin Cancer Res 2002;8:2666-74.
35. Chan EW, Cheng SC, Sin FW, Xie Y. Triptolide induced cytotoxic effects on human promyelocytic leukemia, T cell lymphoma and human hepatocellular carcinoma cell lines. Toxicol Lett 2001;122:81 -7.
36. Lou YJ, Jin J. Triptolide down-regulates bcr-abl expression and induces apoptosis in chronic myelogenous leukemia cells. Leuk Lymphoma 2004;45: 373 -6.
37. Zhang H, Trachootham D, Lu W, et al. Effective killing of Gleevec-resistant CML cells with T315I mutation by a natural compound PEITC through redox-mediated mechanism. Leukemia 2008;22:1191 -9.
38. Ricci C, Scappini B, Divoky V, et al. Mutation in the ATP-binding pocket of the ABL kinase domain in an STI571-resistant BCR/ABL-positive cell line. Cancer Res 2002;62:5995-8.
39. Beran M, Pisa P, O'Brien S, et al. Biological properties and growth in SCID mice of a new myelogenous leukemia cell line (KBM-5) derived from chronic myelogenous leukemia cells in the blastic phase. Cancer Res1993;53:3603 -10.
40. Orsolic N, Golemovic M, Quintas-Cardama A, et al. Adaphostin has significant and selective activity against chronic and acute myeloid leukemia cells.Cancer Sci 2006;97:952 -60.
41. Pan J, Quintas-Cardama A, Kantarjian HM, et al. EXEL-0862, a novel tyrosine kinase inhibitor, induces apoptosis in vitro and ex vivo in human mast cells expressing the KIT D816V mutation. Blood 2007; 109:315-22.
42. Pan J, Quintas-Cardama A, Manshouri T, et al. The novel tyrosine kinase inhibitor EXEL-0862 induces apoptosis in human FIP1L1-PDGFR-α-expressing cells through caspase-3-mediated cleavage of Mcl-1. Leukemia 2007;21:1395 -404.
43. Pan J, Xu G, Yeung SC. Cytochrome c release isup- stream to activation of caspase-9, caspase-8, and caspase-3 in the enhanced apoptosis of anaplastic thyroid cancer cells induced by manumycin and paclitaxel. J Clin Endocrinol Metab 2001;86:4731 -40.
44. Westerheide SD, Kawahara TL, Orton K, Morimoto RI. Triptolide, an inhibitor of the human heat shock response that enhances stress-induced cell death. J Biol Chem 2006;281:9616 -22.
45. Bao X, Cui J, Wu Y, et al.Therolesofendogenous reactive oxygen species and nitric oxide in triptolide- induced apoptotic cell death in macrophages. J Mol Med 2007;85:85-98.
46. Gumireddy K, Baker SJ, Cosenza SC, et al. A non- ATP-competitive inhibitor of BCR-ABL overrides imatinib resistance. Proc Natl Acad Sci U S A 2005;102: 1992-7.
47. Cheetham GM, Charlton PA, Golec 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: 323-9.
48. Kuma Y, Sabio G, Bain J, ShpiroN, MarquezR, Cuenda A. BIRB796 inhibits all p38 MAPK isoforms in vitro and in vivo. J Biol Chem 2005; 280:19472-9.
49. Chandra J, Tracy J, Loegering D, et al. Adaphostin- induced oxidative stress overcomes BCR/ABL mutation-dependent and -independent imatinib resistance. Blood 2006;107:2501 -6.
50. 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 -14.
51. Giles FJ, Cortes J, JonesD, Bergstrom D, Kantarjian H, Freedman SJ. MK-0457, a novel kinase inhibitor, is active in patients with chronic myeloid leukemia or acute lymphocytic leukemia with theT315I BCR-ABL mutation. Blood 2007;109:500-2.
52. Peng C, Brain J, Hu Y, et al. Inhibition ofheat shock protein 90 prolongs survival of mice with BCR-ABL- T315I-induced leukemia and suppresses leukemic stem cells. Blood 2007;110:678-85.
53. Leuenroth SJ, Crews CM. Triptolide-induced transcriptional arrestis associated with changesin nuclear substructure. Cancer Res 2008;68:5257 -66.
54. Bedi A, Zehnbauer BA, BarberJP, Sharkis SJ, Jones RJ. Inhibition ofapoptosis by BCR-ABL in chronicmyeloid leukemia. Blood1994;83:2038-44.
55. Rowley PT, Keng PC, Kosciolek BA. The effect of bcr-abl antisense oligonucleotide on DNA synthesis and apoptosis in K562 chronic myeloid leukemia cells. Leuk Res1996;20:473 -80.