Triptolide, a Chinese herbal extract, enhances drug sensitivity of resistant myeloid leukemia cell lines through downregulation of HIF-1α and Nrf2

Pharmacogenomics

Volumn 14, Issue 11, 2013, Pages 1305-1317

  Chen, Feili ^a   Liu, Yuejian ^a   Wang, Shiyun ^a   Guo, Xutao ^a   Shi, Pengcheng ^a   Wang, Weiguang ^b   Xu, Bing ^a  

^a SOUTHERN MEDICAL UNIVERSITY   (China)

^b UNIVERSITY OF WOLVERHAMPTON   (United Kingdom)

Author keywords

drug resistance; HIF 1 ; Nrf2; triptolide

Indexed keywords

CARBONATE DEHYDRATASE IX; CHEMOKINE RECEPTOR CXCR4; DOXORUBICIN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; IMATINIB; MESSENGER RNA; PROTEIN BNIP3; TRANSCRIPTION FACTOR NRF2; TRIPTOLIDE; VASCULOTROPIN; DITERPENE; EPOXIDE; HERBACEOUS AGENT; HIF1A PROTEIN, HUMAN; NFE2L2 PROTEIN, HUMAN; PHENANTHRENE DERIVATIVE;

APOPTOSIS; ARTICLE; CANCER RESISTANCE; CONTROLLED STUDY; DOWN REGULATION; DRUG CYTOTOXICITY; DRUG POTENTIATION; DRUG SENSITIVITY; GENE EXPRESSION; GSR GENE; HO 1 GENE; HUMAN; HUMAN CELL; LEUKEMIA CELL; NQO1 GENE; PROTEIN EXPRESSION; BIOSYNTHESIS; CHEMISTRY; DRUG EFFECTS; DRUG RESISTANCE; GENE EXPRESSION REGULATION; LEUKEMIA, MYELOID; PATHOLOGY; TUMOR CELL LINE;

CELL LINE, TUMOR; DITERPENES; DOWN-REGULATION; DRUG RESISTANCE, NEOPLASM; DRUGS, CHINESE HERBAL; EPOXY COMPOUNDS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; LEUKEMIA, MYELOID; NF-E2-RELATED FACTOR 2; PHENANTHRENES;

EID: 84882271464     PISSN: 14622416     EISSN: 17448042     Source Type: Journal    
DOI: 10.2217/pgs.13.122     Document Type: Article

References (47)

1. Damiani D, Tiribelli M, Raspadori D et al. The role of MDR-related proteins in the prognosis of adult acute myeloid leukaemia (AML) with normal karyotype. Hematol. Oncol. 25(1), 38-43 (2007).
2. Graziose R, Lila MA, Raskin I. Merging traditional Chinese medicine with modern drug discovery technologies to find novel drugs and functional foods. Curr. Drug Discov. Technol. 7(1), 2-12 (2010).
3. Liu Q. Triptolide and its expanding multiple pharmacological functions. Int. Immunopharmacol. 11(3), 377-383 (2011).
4. 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. 32(4), 503-511 (2011).
5. Pigneux A, Mahon FX, Uhalde M et al. Triptolide cooperates with chemotherapy to induce apoptosis in acute myeloid leukemia cells. Exp. Hematol. 36(12), 1648-1659 (2008).
6. Wang W, Li X, Sun W et al. Triptolide triggers the apoptosis of pancreatic cancer cells via the downregulation of decoy receptor 3 expression. J. Cancer Res. Clin. Oncol. 138(9), 1597-1605 (2012).
7. Wu PP, Liu KC, Huang WW et al. Triptolide induces apoptosis in human adrenal cancer NCI-H295 cells through a mitochondrial-dependent pathway. Oncol. Rep. 25(2), 551-557 (2010).
8. Tengchaisri T, Chawengkirttikul R, Rachaphaew N, Reutrakul V, Sangsuwan R, Sirisinha S. Antitumor activity of triptolide against cholangiocarcinoma growth in vitro and in hamsters. Cancer Lett. 133(2), 169-175 (1998).
9. Xu B, Guo X, Mathew S et al. Triptolide simultaneously induces reactive oxygen species, inhibits NF-kB activity and sensitizes 5-fluorouracil in colorectal cancer cell lines. Cancer Lett. 291(2), 200-208 (2009).
10. Shamon LA, Pezzuto JM, Graves JM et al. Evaluation of the mutagenic, cytotoxic, and antitumor potential of triptolide, a highly oxygenated diterpene isolated from Tripterygium wilfordii. Cancer Lett. 112(1), 113-117 (1997).
11. Xiaowen H, Yi S. Triptolide sensitizes TRAIL-induced apoptosis in prostate cancer cells via p53-mediated DR5 up-regulation. Mol. Biol. Rep. 39(9), 8763-8770 (2012).
12. Zhu W, Li J, Wu S et al. Triptolide cooperates with cisplatin to induce apoptosis in gemcitabine-resistant pancreatic cancer. Pancreas 41(7), 1029-1038 (2012).
13. Huang X, Yang M, Jin J. Triptolide enhances the sensitivity of multiple myeloma cells to dexamethasone via microRNAs. Leuk. Lymphoma 53(6), 1188-1195 (2012).
14. Sporn MB, Liby KT. NRF2 and cancer: the good, the bad and the importance of context. Nat. Rev. Cancer 12(8), 564-571 (2012).
15. Higgins LG, Kelleher MO, Eggleston IM, Itoh K, Yamamoto M, Hayes JD. Transcription factor Nrf2 mediates an adaptive response to sulforaphane that protects fibroblasts in vitro against the cytotoxic effects of electrophiles, peroxides and redox-cycling agents. Toxicol. Appl. Pharmacol. 237(3), 267-280 (2009).
16. Rushworth SA, Zaitseva L, Murray MY, Shah NM, Bowles KM, Macewan DJ. The high Nrf2 expression in human acute myeloid leukemia is driven by NF-kB and underlies its chemo-resistance. Blood 120(26), 5188-5198 (2012).
17. Zhong Y, Zhang F, Sun Z et al. Drug resistance associates with activation of Nrf2 in MCF-7/DOX cells, and wogonin reverses it by down-regulating Nrf2-mediated cellular defense response. Mol. Carcinog. doi:10.1002/mc.21921 (2012) (Epub ahead of print).
18. Chowdhry S, Zhang Y, McMahon M, Sutherland C, Cuadrado A, Hayes JD. Nrf2 is controlled by two distinct b-TrCP recognition motifs in its Neh6 domain, one of which can be modulated by GSK-3 activity. Oncogene doi:10.1038/onc.2012.388 (2012) (Epub ahead of print).
19. Marin-Hernandez A, Gallardo-Perez JC, Ralph SJ, Rodriguez-Enriquez S, Moreno-Sanchez R. HIF-1a modulates energy metabolism in cancer cells by inducing over-expression of specific glycolytic isoforms. Mini Rev. Med. Chem. 9(9), 1084-1101 (2009).
20. Rankin EB, Giaccia AJ. The role of hypoxia-inducible factors in tumorigenesis. Cell Death Differ. 15(4), 678-685 (2008).
21. Harris AL. Hypoxia-a key regulatory factor in tumour growth. Nat. Rev. Cancer 2(1), 38-47 (2002).
22. Matsunaga T, Imataki O, Torii E 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. 36(6), e122-e124 (2012).
23. Deeb G, Vaughan MM, McInnis I et al. Hypoxia-inducible factor-1a protein expression is associated with poor survival in normal karyotype adult acute myeloid leukemia. Leuk. Res. 35(5), 579-584 (2011).
24. Escherich G, Zimmermann M, Janka-Schaub G. Doxorubicin or daunorubicin given upfront in a therapeutic window are equally effective in children with newly diagnosed acute lymphoblastic leukemia. A randomized comparison in trial CoALL 07-03. Pediatr. Blood Cancer 60(2), 254-257 (2012).
25. Lee HJ, Thompson JE, Wang ES, Wetzler M. Philadelphia chromosome-positive acute lymphoblastic leukemia. Cancer 117(8), 1583-1594 (2011).
26. Baran Y, Gur B, Kaya P, Ural AU, Avcu F, Gunduz U. Upregulation of multi drug resistance genes in doxorubicin resistant human acute myelogeneous leukemia cells and reversal of the resistance. Hematology 12(6), 511-517 (2007).
27. Qi J, Peng H, Gu ZL, Liang ZQ, Yang CZ. Establishment of an imatinib resistant cell line K562/G01 and its characterization. Zhonghua Xue Ye Xue Za Zhi 25(6), 337-341 (2004).
28. Chou TC, Talalay P. Quantitative analysis of dose-effect relationships: the combined effects of multiple drugs or enzyme inhibitors. Adv. Enzyme Regul. 22, 27-55 (1984).
29. Tang X, Wang H, Fan L 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. 50(11), 1599-1609 (2011).
30. Jung CW, Jo JR, Lee SH et al. Anti-cancer properties of glucosamine-hydrochloride in YD-8 human oral cancer cells: induction of the caspase-dependent apoptosis and down-regulation of HIF-1a. Toxicol. In vitro 26(1), 42-50 (2012).
31. Ioannou M, Pyrpasopoulou A, Simos G et al. Upregulation of VEGF expression is associated with accumulation of HIF-1a in the skin of naive scleroderma patients. Mod. Rheumatol. doi:10.1007/s10165-012-0787-6 (2012) (Epub ahead of print).
32. Oh YS, Kim HY, Song IC et al. Hypoxia induces CXCR4 expression and biological activity in gastric cancer cells through activation of hypoxia-inducible factor-1a. Oncol. Rep. 28(6), 2239-2246 (2012).
33. Zhou ZL, Luo ZG, Yu B et al. Increased accumulation of hypoxia-inducible factor-1a with reduced transcriptional activity mediates the antitumor effect of triptolide. Mol. Cancer 9(1), 268 (2010).
34. Wilczynski J, Duechler M, Czyz M. Targeting NF-aB and HIF-1 pathways for the treatment of cancer: part I. Arch. Immunol. Ther. Exp. (Warsz.) 59(4), 289-299 (2011).
35. Wilczynski J, Duechler M, Czyz M. Targeting NF-kB and HIF-1 pathways for the treatment of cancer: part II. Arch. Immunol. Ther. Exp. (Warsz.) 59(4), 301-307 (2011).
36. Zhao F, Mancuso A, Bui TV et al. Imatinib resistance associated with BCR-ABL upregulation is dependent on HIF-1a-induced metabolic reprograming. Oncogene 29(20), 2962-2972 (2010).
37. Zhong H, Mabjeesh N, Willard M, Simons J. Nuclear expression of hypoxia-inducible factor 1a protein is heterogeneous in human malignant cells under normoxic conditions. Cancer Lett. 181(2), 233-238 (2002).
38. Wang Y, Liu Y, Malek SN, Zheng P. Targeting HIF1a eliminates cancer stem cells in hematological malignancies. Cell Stem Cell 8(4), 399-411 (2011).
39. Doublier S, Belisario DC, Polimeni M et al. HIF-1 activation induces doxorubicin resistance in MCF7 3-D spheroids via P-glycoprotein expression: a potential model of the chemo-resistance of invasive micropapillary carcinoma of the breast. BMC Cancer 12, 4 (2012).
40. Lang L, Tang K, Li Y, Liu X, Wang C, Chen X. Identification of two small molecule inhibitors of hypoxia-inducible factor 1 with different cell-based screening model. Zhongguo Zhong Yao Za Zhi 37(14), 2151-2155 (2012).
41. Rushworth SA, Bowles KM, Macewan DJ. High basal nuclear levels of Nrf2 in acute myeloid leukemia reduces sensitivity to proteasome inhibitors. Cancer Res. 71(5), 1999-2009 (2011).
42. Tarumoto T, Nagai T, Ohmine K et al. Ascorbic acid restores sensitivity to imatinib via suppression of Nrf2-dependent gene expression in the imatinib-resistant cell line. Exp. Hematol. 32(4), 375-381 (2004).
43. Nagai T, Kikuchi S, Ohmine K et al. Hemin reduces cellular sensitivity to imatinib and anthracyclins via Nrf2. J. Cell Biochem. 104(2), 680-691 (2008).
44. Ren D, Villeneuve NF, Jiang T et al. Brusatol enhances the efficacy of chemotherapy by inhibiting the Nrf2-mediated defense mechanism. Proc. Natl Acad. Sci. USA 108(4), 1433-1438 (2011).
45. Li J, Jin J, Li M et al. Role of Nrf2 in protection against triptolide-induced toxicity in rat kidney cells. Toxicol. Lett. 213(2), 194-202 (2012).
46. Baird L, Dinkova-Kostova AT. The cytoprotective role of the Keap1-Nrf2 pathway. Arch. Toxicol. 85(4), 241-272 (2011).
47. Chapple SJ, Siow RC, Mann GE. Crosstalk between Nrf2 and the proteasome: therapeutic potential of Nrf2 inducers in vascular disease and aging. Int. J. Biochem. Cell Biol. 44(8), 1315-1320 (2012).