Hsp90 inhibitor BIIB021 enhances triptolide-induced apoptosis of human T-celi acute lymphoblastic leukemia cells in vitro mainly by disrupting p53- MDM2 balance

Acta Pharmacologica Sinica

Volumn 34, Issue 12, 2013, Pages 1545-1553

  Li, Min ^a   Zhang, Xiang ^b   Zhou, Wen Jing ^a   Chen, Yue Hua ^c   Liu, Hui ^a   Liu, Lin ^a   Yang, Chun Mei ^a   Qian, Wen Bin ^a  

^a ZHEJIANG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b Chinese Traditional Medicine Hospital of Zhejiang Province   (China)

^c Shaoxing Second Hospital   (China)

Author keywords

Acute lymphoblastic leukemia; Anticancer drug; Apoptosis; Bcl 2; BIIB021; Hsp90; MDM2; P53; T cell; Triptolide

Indexed keywords

4 [5 (4 METHYL 1 PIPERAZINYL)[2,5' BI 1H BENZIMIDAZOL] 2' YL]PHENOL; ANTILEUKEMIC AGENT; BIIB 021; BIM PROTEIN; CASPASE; CYCLIN DEPENDENT KINASE 4; CYCLIN DEPENDENT KINASE 6; HEAT SHOCK PROTEIN 90; HEAT SHOCK PROTEIN 90 INHIBITOR; LIPOCORTIN 5; MESSENGER RNA; PROTEIN BAK; PROTEIN BCL 2; PROTEIN KINASE B; PROTEIN MDM2; PROTEIN P18; PROTEIN P53; SYNAPTOTAGMIN I; TRIPTOLIDE; UNCLASSIFIED DRUG; 6 CHLORO 9 (4 METHOXY 3,5 DIMETHYLPYRIDIN 2 YLMETHYL) 9H PURIN 2 YLAMINE; 6-CHLORO-9-(4-METHOXY-3,5-DIMETHYLPYRIDIN-2-YLMETHYL)-9H-PURIN-2-YLAMINE; ADENINE; DITERPENE; DRUG DERIVATIVE; EPOXIDE; MDM2 PROTEIN, HUMAN; PHENANTHRENE DERIVATIVE; PRIMER DNA; PYRIDINE DERIVATIVE; TP53 PROTEIN, HUMAN;

ACUTE LYMPHOBLASTIC LEUKEMIA; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; ASSAY; CANCER INHIBITION; CELL CYCLE; CELL CYCLE ARREST; CELL CYCLE G0 PHASE; CELL VIABILITY; CONTROLLED STUDY; DOSE RESPONSE; DRUG MECHANISM; DRUG POTENTIATION; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; FLOW CYTOMETRY; G1 PHASE CELL CYCLE CHECKPOINT; HUMAN; HUMAN CELL; IC 50; IN VITRO STUDY; LEUKEMIA CELL LINE; MONOTHERAPY; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STAINING; WESTERN BLOTTING; DRUG ANTAGONISM; DRUG EFFECT; METABOLISM; NUCLEOTIDE SEQUENCE; PATHOLOGY; REAL TIME POLYMERASE CHAIN REACTION; TUMOR CELL LINE;

ADENINE; APOPTOSIS; BASE SEQUENCE; CELL LINE, TUMOR; DITERPENES; DNA PRIMERS; EPOXY COMPOUNDS; FLOW CYTOMETRY; HSP90 HEAT-SHOCK PROTEINS; HUMANS; PHENANTHRENES; PRECURSOR T-CELL LYMPHOBLASTIC LEUKEMIA-LYMPHOMA; PROTO-ONCOGENE PROTEINS C-MDM2; PYRIDINES; REAL-TIME POLYMERASE CHAIN REACTION; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84901537155     PISSN: 16714083     EISSN: 17457254     Source Type: Journal    
DOI: 10.1038/aps.2013.124     Document Type: Article

References (39)

1. Ferrando AA, Neuberg DS, Staunton J, Loh ML, Huard C, Raimondi SC, et al. Gene expression signatures define novel oncogenic pathways in T cell acute lymphoblastic leukemia. Cancer Cell 2002; 1: 75-87.
2. Pui CH, Robison LL, Look AT. Acute lymphoblastic leukaemia. Lancet 2008; 371:1030-43.
3. Xiao K, Liu W, Qu S, Sun H, Tang J. Study of heat shock protein HSP90 alpha, HSP70, HSP27 mRNA expression in human acute leukemia cells. J Tongji Med Univ 1996; 16: 212-6.
4. Lauten M, Beger C, Gerdes K, Asgedom G, Kardinal C, Welte K, et al. Expression of heat-shock protein 90 in glucocorticoid-sensitive and -resistant childhood acute lymphoblastic leukaemia. Leukaemia 2003; 17:1551-6.
5. Hacihanefioglu A, Gonullu E, Mehtap O, Keski H, Yavuz M, Ercin C. Effect of heat shock protein-90 (HSP90) and vascular endothelial growth factor (VEGF) on survival in acute lymphoblastic leukemia: An immunohistochemical study. Med Oncol 2011; 28:846-51.
6. Tong WG, Estrov Z, Wang Y, O'Brien S, Faderl S, Harris DM, et al. The synthetic heat shock protein 90 (Hsp90) inhibitor EC141 induces degradation of Bcr-Abl p190 protein and apoptosis of Ph-positive acute lymphoblastic leukemia cells. Invest New Drugs 2011; 29: 1206-12.
7. Tavernier E, Flandrin-Gresta P, Solly F, Rigollet L, Cornillon J, Augeul-Meunier K, et al. HSP90 inhibition results in apoptosis of Philadelphia acute lymphoblastic leukaemia cells: An attractive prospect of new targeted agents. J Cancer Res Clin Oncol 2012; 138:1753-8.
8. Peng C, Li D, Li S. Heat shock protein 90: A potential therapeutic target in leukemic progenitor and stem cells harboring mutant BCR- ABL resistant to kinase inhibitors. Ceil Cycle 2007; 6:2227-31.
9. Taldone T, Gozman A, Maharaj R, Chiosis G. Targeting Hsp90: small-molecule inhibitors and their clinical development. Curr Opin Pharmacol 2008; 8:370-4.
10. Lundgren K, Zhang H, Brekken J, Huser N, Powell RE, Timple N, et al. BIIB021, an orally available, fully synthetic small-molecule inhibitor of the heat shock protein Hsp90. Mol Cancer Ther 2009; 8: 921-9.
11. Boll B, Eltaib F, Reiners KS, von Tresckow B, Tawadros S, Simhadri VR, et al. Heat shock protein 90 inhibitor BIIB021 (CNF2024) depletes NF-kappaB and sensitizes Hodgkin's lymphoma cells for natural killer cell-mediated cytotoxicity. Clin Cancer Res 2009; 15: 5108-16.
12. Yin X, Zhang H, Lundgren K, Wilson L, Burrows F, Shores CG. BIIB021, a novel Hsp90 inhibitor, sensitizes head and neck squamous cell carcinoma to radiotherapy. Int J Cancer 2010; 126:1216-25.
13. Zhang H, Neely L, Lundgren K, Yang YC, Lough R, Timple N, et al. BIIB021, a synthetic Hsp90 inhibitor, has broad application against tumors with acquired multidrug resistance. Int J Cancer 2010; 126: 1226-34.
14. Dickson MA, Okuno SH, Keohan ML, Maki RG, D'Adamo DR, Akhurst TJ, et al. Phase II study of the HSP90-inhibitor BIIB021 in gastrointestinal stromal tumors. Ann Oncol 2013; 24:252-7.
15. Luo Y, Shi C, Liao M. Advance in the anti-tumor mechanism of triptolide. Chin J Chin Mater Med 2009; 34: 2024-6.
16. Carter BZ, Mak DH, Schober WD, McQueen T, Harris D, Estrov Z, et al. Triptolide induces caspase-dependent cell death mediated via the mitochondrial pathway in leukemic cells. Blood 2006; 108:630-7.
17. Carter BZ, Mak DH, Schober WD, Dietrich MF, Pinilla C, Vassilev LT, et al. Triptolide sensitizes AML cells to TRAIL-induced apoptosis via decrease of XIAP and P53-mediated increase of DR5. Blood 2008; 111: 3742-50.
18. Park B, Sung B, Yadav VR, Chaturvedi MM, Aggarwal BB. Triptolide, histone acetyltransferase inhibitor, suppresses growth and chemo- sensitizes leukemic cells through inhibition of gene expression regulated by TNF-TNFR1-TRADD-TRAF2- NIK-TAK1-IKK pathway. Biochem Pharmacol 2011; 82:1134-44.
19. Li H, Hui L, Xu W, Shen H, Chen Q, Long L, et al. Triptolide modulates the sensitivity of K562/A02 cells to adriamycin by regulating miR-21 expression. Pharm Biol 2012; 50:1233-40.
20. Li H, Hui L, Xu W, Shen H, Chen Q, Long L, et al. Modulation of P-glycoprotein expression by triptolide in adriamycin-resistant K562/A02 cells. Oncol Lett 2012; 3:485-9.
21. Zhou GS, Hu Z, Fang HT, Zhang FX, Pan XF, Chen XQ, et al. Biologic activity of triptolide in t(8;21) acute myeloid leukemia cells. Leuk Res 2011; 35: 214-8.
22. Huang M, Zhang H, Liu T, Tian D, Gu L, Zhou M. Triptolide inhibits MDM2 and induces apoptosis in acute lymphoblastic leukemia cells through a P53-independent pathway. Mol Cancer Ther 2013; 12: 184-94.
23. Meng HT, Zhu L, Ni WM, You LS, Jin J, Qian WB. Triptolide inhibits the proliferation of cells from lymphocytic leukemic cell lines in association with downregulation of NF-kB activity and miR-16-1*. Acta Pharmacol Sin 2011; 32:503-11.
24. Bai F, Pei XH, Godfrey VL, Xiong Y. Haptoinsufficiency of p18 (INK4c) sensitizes mice to carcinogen-induced tumorigenesis. Mol Cell Biol 2003; 23:1269-77.
25. Powers MV, Workman P. Targeting of multiple signalling pathways by heat shock protein 90 molecular chaperone inhibitors. Endocr Relat Cancer 2006; 13: S125-35.
26. Palomero T, Sulis ML, Cortina M, Real PJ, Barnes K, Ciofani M, et al. Mutational loss of PTEN induces resistance to NOTCHl inhibition in T-cell leukemia. Nat Med 2007; 13:1203-10.
27. Chang WT, Kang JJ, Lee KY, Wei K, Anderson E, Gotmare S, et al. Triptolideand chemotherapy cooperate in tumor cell apoptosis. A role for the p53 pathway. J Biol Chem 2001; 276:2221-7.
28. Jiang XH, Wong BC, Lin MC, Zhu GH, Kung HF, Jiang SH, et al. Functional p53 is required for triptolide-induced apoptosis and AP-1 and nuclear factor-kappaB activation in gastric cancer cells. Oncogene 2001; 20: 8009-18.
29. Agirre X, Novo FJ, Calasanz MJ, LarrSyoz MJ, Lahortiga I, Valganon M, et al. TP53 is frequently altered by methylation, mutation, and/or deletion in acute lymphoblastic leukaemia. Mol Carcinog 2003; 38: 201-8.
30. Jonveaux P, Berger R. Infrequent mutations in the P53 gene in primary human T-cell acute lymphoblastic leukemia. Leukemia 1991; 5:839-40.
31. Yeargin J, Cheng J, Haas M. Role of the p53 tumor suppressor gene in the pathogenesis and in the suppression of acute lymphoblastic T-cell leukemia. Leukemia 1992; 6:85S-91S.
32. Diccianni MB, Yu J, Hsiao M, Mukherjee S, Shao LE, Yu AL. Clinical significance of p53 mutations in relapsed T-cell acute lymphoblastic leukemia. Blood 1994; 84:3105-12.
33. Hsiao MH, Yu AL, Yeargin J, Ku D, Haas M. Nonhereditary p53 mutations in T-cell acute lymphoblastic leukemia are associated with the relapse phase. Blood 1994; 83:2922-30.
34. Kawamura M, Ohnishi H, Guo SX, Sheng XM, Minegishi M, Hanada R, et al. Alterations of the p53, p21, p16, p15, and RAS genes in childhood T-cell acute lymphoblastic leukemia. Leuk Res 1999; 23: 115-26.
35. Vilas-Zornoza A, Agirre X, Martin-Palanco V, Martfn-Subero Jl, San Jose-Eneriz E, Garate L, et al. Frequent and simultaneous epigenetic inactivation of TP53 pathway genes in acute lymphoblastic leukemia. PLoS One 2011; 6: e17012.
36. Hendy OM, Elghannam DM, El-Sharnouby JA, Goda EF, El-Ashry R, Al-Tonbary Y. Frequency and prognostic significance of murine double minute protein-2 overexpression and p53 gene mutations in childhood acute lymphoblastic leukemia. Hematology 2009; 14:335-40.
37. Wade M, Li YC, Wahl GM. MDM2, MDMX and p53 in oncogenesis and cancer therapy. Nat Rev Cancer 2012; 13:83-96.
38. Li Q, Lozano G. Molecular pathways: Targeting Mdm2 and Mdm4 in cancer therapy. Clin Cancer Res 2013; 19:34-41.
39. Lamottke B, Kaiser M, Mieth M, Heider U, Gao Z, Nikolova Z, et al. The novel, orally bioavailable HSP90 inhibitor NVP-HSP990 induces cell cycle arrest and apoptosis in multiple myeloma cells and acts synergistically with melphalan by increased cleavage of caspases. Eur J Haematol 2012; 88:406-15.