Low-dose triptolide in combination with idarubicin induces apoptosis in AML leukemic stem-like KG1a cell line by modulation of the intrinsic and extrinsic factors

Cell Death and Disease

Volumn 4, Issue 12, 2013, Pages

  Liu, Y ^a   Chen, F ^a   Wang, S ^a   Guo, X ^a   Shi, P ^a   Wang, W ^b   Xu, B ^a  

^a SOUTHERN MEDICAL UNIVERSITY   (China)

^b UNIVERSITY OF WOLVERHAMPTON   (United Kingdom)

Author keywords

HIF 1 ; idarubicin; Nrf2; reactive oxygen species; triptolide

Indexed keywords

CYANOCOBALAMIN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; IDARUBICIN; INTRINSIC FACTOR; REACTIVE OXYGEN METABOLITE; TRANSCRIPTION FACTOR NRF2; TRIPTOLIDE;

ACUTE GRANULOCYTIC LEUKEMIA; APOPTOSIS; ARTICLE; CELL CYCLE; CELL SELECTION; CELL VIABILITY; COLONY FORMING UNIT; CONTROLLED STUDY; CYTOTOXICITY; CYTOTOXICITY ASSAY; ENZYME INHIBITION; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IMMUNOPHENOTYPING; IN VITRO STUDY; LEUKEMIA CELL; LOW DRUG DOSE; MTT ASSAY; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

APOPTOSIS; BLOTTING, WESTERN; CELL CYCLE; CELL LINE; CELL SURVIVAL; DITERPENES; EPOXY COMPOUNDS; FLOW CYTOMETRY; HUMANS; IDARUBICIN; IMMUNOPHENOTYPING; LEUKEMIA, MYELOID, ACUTE; NEOPLASTIC STEM CELLS; NF-E2-RELATED FACTOR 2; PHENANTHRENES; REACTIVE OXYGEN SPECIES; REAL-TIME POLYMERASE CHAIN REACTION;

EID: 84891798669     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2013.467     Document Type: Article

References (45)

1. Damiani D, Tiribelli M, Raspadori D, Michelutti A, Gozzetti A, Calistri E et al. The role of MDR-related proteins in the prognosis of adult acute myeloid leukaemia (AML) with normal karyotype. Hematol Oncol 2007; 25: 38-43
2. Lapidot T, Grunberger T, Vormoor J, Estrov Z, Kollet O, Bunin N et al. Identification of human juvenile chronic myelogenous leukemia stem cells capable of initiating the disease in primary and secondary SCID mice. Blood 1996; 88: 2655-2664
3. de Figueiredo-Pontes LL, Pintao MC, Oliveira LC, Dalmazzo LF, Jacomo RH, Garcia AB et al. Determination of P-glycoprotein, MDR-related protein 1, breast cancer resistance protein, and lung-resistance protein expression in leukemic stem cells of acute myeloid leukemia. Cytometry B Clin Cytom 2008; 74: 163-168
4. Fardel O, Payen L, Courtois A, Drenou B, Fauchet R, Rault B. Differential expression and activity of P-glycoprotein and multidrug resistance-Associated protein in CD34-positive KG1a leukemic cells. Int J Oncol 1998; 12: 315-319
5. She M, Niu X, Chen X, Li J, Zhou M, He Y et al. Resistance of leukemic stem-like cells in AML cell line KG1a to natural killer cell-mediated cytotoxicity. Cancer Letters 2012; 318: 173-179
6. Konopleva MY, Jordan CT. Leukemia stem cells and microenvironment: Biology and therapeutic targeting. J Clin Oncol 2011; 29: 591-599
7. Mortensen BT, Jensen PO, Helledie N, Iversen PO, Ralfkiaer E, Larsen JK et al. Changing bone marrow micro-environment during development of acute myeloid leukaemia in rats. Br J Haematol 1998; 102: 458-464
8. Marin-Hernandez A, Gallardo-Perez JC, Ralph SJ, Rodriguez-Enriquez S, Moreno-Sanchez R. HIF-1alpha modulates energy metabolism in cancer cells by inducing over-expression of specific glycolytic isoforms. Mini Rev Med Chem 2009; 9: 1084-1101
9. Deeb G, Vaughan MM, McInnis I, Ford LA, Sait SNJ, Starostik P et al. Hypoxia-inducible factor-1a protein expression is associated with poor survival in normal karyotype adult acute myeloid leukemia. Leuk Res 2011; 35: 579-584
10. Wang Y, Liu Y, Malek SN, Zheng P. Targeting HIF1alpha eliminates cancer stem cells in hematological malignancies. Cell Stem Cell 2011; 8: 399-411
11. Staller P, Sulitkova J, Lisztwan J, Moch H, Oakeley EJ, Krek W. Chemokine receptor CXCR4 downregulated by von Hippel-Lindau tumour suppressor pVHL. Nature 2003; 425: 307-311
12. Ceradini DJ, Kulkarni AR, Callaghan MJ, Tepper OM, Bastidas N, Kleinman ME et al. Progenitor cell trafficking is regulated by hypoxic gradients through HIF-1 induction of SDF-1. Nat Med 2004; 10: 858-864
13. Sporn MB, Liby KT. NRF2 and cancer: The good, the bad and the importance of context. Nature Rev Cancer 2012; 12: 564-571
14. Achuthan S, Santhoshkumar TR, Prabhakar J, Nair SA, Pillai MR. Drug-induced senescence generates chemoresistant stemlike cells with low reactive oxygen species. J Biol Chem 2011; 286: 37813-37829
15. Zhou ZL, Yang YX, Ding J, Li YC, Miao ZH. Triptolide: Structural modifications, structureactivity relationships, bioactivities, clinical development and mechanisms. Nat Prod Rep 2012; 29: 457-475
16. 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: 81-87
17. Zhao H, Yang Z, Wang X, Zhang X, Wang M, Wang Y et al. Triptolide inhibits ovarian cancer cell invasion by repression of matrix metalloproteinase 7 and 19 and upregulation of E-cadherin. Exp Mol Med 2012; 44: 633-641
18. Xu B, Guo X, Mathew S, Armesilla AL, Cassidy J, Darling JL et al. Triptolide simultaneously induces reactive oxygen species, inhibits NF-kappaB activity and sensitizes 5-fluorouracil in colorectal cancer cell lines. Cancer Lett 2010; 291: 200-208
19. Ding X, Zhou X, Zhang H, Qing J, Qiang H, Zhou G. Triptolide augments the effects of 5-lipoxygenase RNA interference in suppressing pancreatic tumor growth in a xenograft mouse model. Cancer Chemother Pharmacol 2012; 69: 253-261
20. Huang X, Yang M, Jin J. Triptolide enhances the sensitivity of multiple myeloma cells to dexamethasone via microRNAs. Leuk Lymphoma 2012; 53: 1-8
21. Chen F, Liu Y, Wang S, Guo X, Shi P, Wang W et al. Triptolide, a Chinese herbal extract, enhances drug sensitivity of resistant myeloid leukemia cell lines through downregulation of HIF-1alpha and Nrf2. Pharmacogenomics 2013; 14: 1305-1317
22. Mak DH, Schober WD, Chen W, Konopleva M, Cortes J, Kantarjian HM et al. Triptolide induces cell death independent of cellular responses to imatinib in blast crisis chronic myelogenous leukemia cells including quiescent CD34+ primitive progenitor cells. Mol Cancer Ther 2009; 8: 2509-2516
23. Berman E, Heller G, Santorsa J, McKenzie S, Gee T, Kempin S et al. Results of a randomized trial comparing idarubicin and cytosine arabinoside with daunorubicin and cytosine arabinoside in adult patients with newly diagnosed acute myelogenous leukemia. Blood 1991; 77: 1666-1674
24. Shi P, Zha J, Guo X, Chen F, Fan Z, Huang F et al. Idarubicin is superior to daunorubicin in remission induction of de novo acute myeloid leukemia patients with high MDR1 expression. Pharmacogenomics 2013; 14: 17-23
25. Fukushima T, Inoue H, Takemura H, Kishi S, Yamauchi T, Inai K et al. Idarubicin and idarubicinol are less affected by topoisomerase II-related multidrug resistance than is daunorubicin. Leuk Res 1998; 22: 625-629
26. Tang X, Wang H, Fan L, Wu X, Xin A, Ren H et al. Luteolin inhibits Nrf2 leading to negative regulation of the Nrf2/ARE pathway and sensitization of human lung carcinoma A549 cells to therapeutic drugs. Free Radic Biol Med 2011; 50: 1599-1609
27. 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: 3742-3750
28. Pigneux A, Mahon FX, Uhalde M, Jeanneteau M, Lacombe F, Milpied N et al. Triptolide cooperates with chemotherapy to induce apoptosis in acute myeloid leukemia cells. Exp Hematol 2008; 36: 1648-1659
29. Ioannou M, Pyrpasopoulou A, Simos G, Paraskeva E, Nikolaidou C, Venizelos I et al. Upregulation of VEGF expression is associated with accumulation of HIF-1alpha in the skin of naive scleroderma patients. Mod Rheumatol 2013; 23: 1245-1248
30. Oh YS, Kim HY, Song IC, Yun HJ, Jo DY, Kim S et al. Hypoxia induces CXCR4 expression and biological activity in gastric cancer cells through activation of hypoxia-inducible factor-1alpha. Oncol Rep 2012; 28: 2239-2246
31. Zhou Z-L, Luo Z-G, Yu B, Jiang Y, Chen Y, Feng J-M et al. Increased accumulation of hypoxia-inducible factor-1a with reduced transcriptional activity mediates the antitumor effect of triptolide. Mol Cancer 2010; 9: 268
32. Wilczynski J, Duechler M, Czyz M. Targeting NF-kappaB and HIF-1 pathways for the treatment of cancer: Part I. Arch Immunol Ther Exp (Warsz) 2011; 59: 289-299
33. Wilczynski J, Duechler M, Czyz M. Targeting NF-kappaB and HIF-1 pathways for the treatment of cancer: Part II. Arch Immunol Ther Exp (Warsz) 2011; 59: 301-307
34. Matsunaga T, Imataki O, Torii E, Kameda T, Shide K, Shimoda H et al. Elevated HIF-1a expression of acute myelogenous leukemia stem cells in the endosteal hypoxic zone may be a cause of minimal residual disease in bone marrow after chemotherapy. Leuk Res 2012; 36: E122-e124
35. Dong-Feng Z, Ting L, Cheng C, Xi Z, Xue L, Xing-Hua C et al. Silencing HIF-1a reduces the adhesion and secretion functions of acute leukemia hBMSCs. Braz J Med Biol Res 2012; 45: 906-912
36. Tavor S, Petit I. Can inhibition of the SDF-1/CXCR4 axis eradicate acute leukemiäSemin Cancer Biol 2010; 20: 178-185
37. Matsunaga T, Takemoto N, Sato T, Takimoto R, Tanaka I, Fujimi A et al. Interaction between leukemic-cell VLA-4 and stromal fibronectin is a decisive factor for minimal residual disease of acute myelogenous leukemia. Nat Med 2003; 9: 1158-1165
38. Nervi B, Ramirez P, Rettig MP, Uy GL, Holt MS, Ritchey JK et al. Chemosensitization of acute myeloid leukemia (AML) following mobilization by the CXCR4 antagonist AMD3100. Blood 2009; 113: 6206-6214
39. Reuter S, Gupta SC, Chaturvedi MM, Aggarwal BB. Oxidative stress, inflammation, and cancer: How are they linked? Free Rad Biol Med 2010; 49: 1603-1616
40. Toyokuni S. Novel aspects of oxidative stress-Associated carcinogenesis. Antioxid Redox Signal 2006; 8: 1373-1377
41. Jin Y, Lu Z, Ding K, Li J, Du X, Chen C et al. Antineoplastic mechanisms of niclosamide in acute myelogenous leukemia stem cells: Inactivation of the NF-kappaB pathway and generation of reactive oxygen species. Cancer Res 2010; 70: 2516-2527
42. Guzman ML, Rossi RM, Karnischky L, Li X, Peterson DR, Howard DS et al. The sesquiterpene lactone parthenolide induces apoptosis of human acute myelogenous leukemia stem and progenitor cells. Blood 2005; 105: 4163-4169
43. Baird L, Dinkova-Kostova AT. The cytoprotective role of the Keap1-Nrf2 pathway. Arch Toxicol 2011; 85: 241-272
44. Rushworth SA, Bowles KM, MacEwan DJ. High basal nuclear levels of Nrf2 in acute myeloid leukemia reduces sensitivity to proteasome inhibitors. Cancer Res 2011; 71: 1999-2009
45. Yip NC, Fombon IS, Liu P, Brown S, Kannappan V, Armesilla AL et al. Disulfiram modulated ROS-MAPK and NFkB pathways and targeted breast cancer cells with cancer stem cell-like properties. Br J Cancer 2011; 104: 1564-1574