Increased accumulation of hypoxia-inducible factor-1α with reduced transcriptional activity mediates the antitumor effect of triptolide

Molecular Cancer

Volumn 9, Issue , 2010, Pages

  Zhou, Zhao Li ^a,c   Luo, Zhi Guo ^b   Yu, Bing ^a   Jiang, Yi ^a   Chen, Yi ^a   Feng, Jian Ming ^a   Dai, Mei ^a   Tong, Lin Jiang ^a   Li, Zheng ^a   Li, Yuan Chao ^a   Ding, Jian ^a   Miao, Ze Hong ^a  

^a SHANGHAI INSTITUTE OF MATERIA MEDICA   (China)

^b FUDAN UNIVERSITY   (China)

^c SHENYANG PHARMACEUTICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; CARBONATE DEHYDRATASE IX; HYPOXIA INDUCIBLE FACTOR 1ALPHA; LUCIFERASE; MESSENGER RNA; PROTEIN BNIP3; TRIPTOLIDE; VASCULOTROPIN; ANTINEOPLASTIC AGENT; DITERPENE; EPOXIDE; PHENANTHRENE DERIVATIVE; SMALL INTERFERING RNA;

ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CELL PROLIFERATION; CONTROLLED STUDY; CYTOTOXICITY; DRUG INHIBITION; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; GENE TARGETING; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; NONHUMAN; OVARY CANCER; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEIN LOCALIZATION; PROTEIN SECRETION; RAT; REAL TIME POLYMERASE CHAIN REACTION; REPORTER GENE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING; CELL SURVIVAL; DRUG EFFECT; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; METABOLISM; NEOPLASM; PHYSIOLOGY; TUMOR CELL LINE;

RATTUS; TRIPTERYGIUM WILFORDII;

ANTINEOPLASTIC AGENTS; BLOTTING, WESTERN; CELL LINE, TUMOR; CELL SURVIVAL; DITERPENES; ENZYME-LINKED IMMUNOSORBENT ASSAY; EPOXY COMPOUNDS; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; IMMUNOPRECIPITATION; NEOPLASMS; PHENANTHRENES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, SMALL INTERFERING; VASCULAR ENDOTHELIAL GROWTH FACTORS;

EID: 77957674310     PISSN: None     EISSN: 14764598     Source Type: Journal    
DOI: 10.1186/1476-4598-9-268     Document Type: Article

References (49)

1. 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. 10.2174/138955709788922610, 19689405.
2. Rankin EB, Giaccia AJ. The role of hypoxia-inducible factors in tumorigenesis. Cell Death Differ 2008, 15:678-685. 10.1038/cdd.2008.21, 18259193.
3. Harris AL. Hypoxia--a key regulatory factor in tumour growth. Nat Rev Cancer 2002, 2:38-47. 10.1038/nrc704, 11902584.
4. Zhong H, Chiles K, Feldser D, Laughner E, Hanrahan C, Georgescu MM, Simons JW, Semenza GL. Modulation of hypoxia-inducible factor 1alpha expression by the epidermal growth factor/phosphatidylinositol 3-kinase/PTEN/AKT/FRAP pathway in human prostate cancer cells: implications for tumor angiogenesis and therapeutics. Cancer Res 2000, 60:1541-1545.
5. Bos R, Zhong H, Hanrahan CF, Mommers EC, Semenza GL, Pinedo HM, Abeloff MD, Simons JW, van Diest PJ, van der Wall E. Levels of hypoxia-inducible factor-1 alpha during breast carcinogenesis. J Natl Cancer Inst 2001, 93:309-314. 10.1093/jnci/93.4.309, 11181778.
6. Poon E, Harris AL, Ashcroft M. Targeting the hypoxia-inducible factor (HIF) pathway in cancer. Expert Rev Mol Med 2009, 11:e26. 10.1017/S1462399409001173, 19709449.
7. Carmeliet P, Dor Y, Herbert JM, Fukumura D, Brusselmans K, Dewerchin M, Neeman M, Bono F, Abramovitch R, Maxwell P, Koch CJ, Ratcliffe P, Moons L, Jain RK, Collen D, Keshert E. Role of HIF-1alpha in hypoxia-mediated apoptosis, cell proliferation and tumour angiogenesis. Nature 1998, 394:485-490. 10.1038/28867, 9697772.
8. Su D, Song Y, Li R. [Comparative clinical study of rheumatoid arthritis treated by triptolide and an ethyl acetate extract of Tripterygium wilfordii]. Zhong Xi Yi Jie He Za Zhi 1990, 10:144-146. 131.
9. Yang SX, Gao HL, Xie SS, Zhang WR, Long ZZ. Immunosuppression of triptolide and its effect on skin allograft survival. Int J Immunopharmacol 1992, 14:963-969. 10.1016/0192-0561(92)90139-C, 1428369.
10. He MF, Huang YH, Wu LW, Ge W, Shaw PC, But PP. Triptolide functions as a potent angiogenesis inhibitor. Int J Cancer 126:266-278. 10.1002/ijc.24694, 19569053.
11. Zhu W, Ou Y, Li Y, Xiao R, Shu M, Zhou Y, Xie J, He S, Qiu P, Yan G. A small-molecule triptolide suppresses angiogenesis and invasion of human anaplastic thyroid carcinoma cells via down-regulation of the nuclear factor-kappa B pathway. Mol Pharmacol 2009, 75:812-819. 10.1124/mol.108.052605, 19158360.
12. Yang S, Chen J, Guo Z, Xu XM, Wang L, Pei XF, Yang J, Underhill CB, Zhang L. Triptolide inhibits the growth and metastasis of solid tumors. Mol Cancer Ther 2003, 2:65-72.
13. Shi X, Jin Y, Cheng C, Zhang H, Zou W, Zheng Q, Lu Z, Chen Q, Lai Y, Pan J. Triptolide inhibits Bcr-Abl transcription and induces apoptosis in STI571-resistant chronic myelogenous leukemia cells harboring T315I mutation. Clin Cancer Res 2009, 15:1686-1697. 10.1158/1078-0432.CCR-08-2141, 19240172.
14. Li Z, Zhou ZL, Miao ZH, Lin LP, Feng HJ, Tong LJ, Ding J, Li YC. Design and Synthesis of Novel C14-Hydroxyl Substituted Triptolide Derivatives as Potential Selective Antitumor Agents. J Med Chem 2009, 52:5115-5123. 10.1021/jm900342g, 19637874.
15. Lou YJ, Jin J. Triptolide down-regulates bcr-abl expression and induces apoptosis in chronic myelogenous leukemia cells. Leuk Lymphoma 2004, 45:373-376. 10.1080/1042819031000139710, 15101726.
16. Phillips PA, Dudeja V, McCarroll JA, Borja-Cacho D, Dawra RK, Grizzle WE, Vickers SM, Saluja AK. Triptolide induces pancreatic cancer cell death via inhibition of heat shock protein 70. Cancer Res 2007, 67:9407-9416. 10.1158/0008-5472.CAN-07-1077, 17909050.
17. Lee KY, Park JS, Jee YK, Rosen GD. Triptolide sensitizes lung cancer cells to TNF-related apoptosis-inducing ligand (TRAIL)-induced apoptosis by inhibition of NF-kappaB activation. Exp Mol Med 2002, 34:462-468.
18. Jiang XH, Wong BC, Lin MC, Zhu GH, Kung HF, Jiang SH, Yang D, Lam SK. Functional p53 is required for triptolide-induced apoptosis and AP-1 and nuclear factor-kappaB activation in gastric cancer cells. Oncogene 2001, 20:8009-8018. 10.1038/sj.onc.1204981, 11753684.
19. 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, 8:2666-2674.
20. Chang WT, Kang JJ, Lee KY, Wei K, Anderson E, Gotmare S, Ross JA, Rosen GD. Triptolide and chemotherapy cooperate in tumor cell apoptosis. A role for the p53 pathway. J Biol Chem 2001, 276:2221-2227.
21. Zhu W, He S, Li Y, Qiu P, Shu M, Ou Y, Zhou Y, Leng T, Xie J, Zheng X, Xu D, Su X, Yan G. Anti-angiogenic activity of triptolide in anaplastic thyroid carcinoma is mediated by targeting vascular endothelial and tumor cells. Vascul Pharmacol 2010, 52:46-54. 10.1016/j.vph.2009.10.006, 19854299.
22. Otrock ZK, Hatoum HA, Awada AH, Ishak RS, Shamseddine AI. Hypoxia-inducible factor in cancer angiogenesis: structure, regulation and clinical perspectives. Crit Rev Oncol Hematol 2009, 70:93-102. 10.1016/j.critrevonc.2009.01.001, 19186072.
23. Guo M, Song LP, Jiang Y, Liu W, Yu Y, Chen GQ. Hypoxia-mimetic agents desferrioxamine and cobalt chloride induce leukemic cell apoptosis through different hypoxia-inducible factor-1alpha independent mechanisms. Apoptosis 2006, 11:67-77. 10.1007/s10495-005-3085-3, 16374551.
24. Qing G, Simon MC. Hypoxia inducible factor-2alpha: a critical mediator of aggressive tumor phenotypes. Curr Opin Genet Dev 2009, 19:60-66. 10.1016/j.gde.2008.12.001, 19167211.
25. D'Angelo G, Duplan E, Boyer N, Vigne P, Frelin C. Hypoxia up-regulates prolyl hydroxylase activity: a feedback mechanism that limits HIF-1 responses during reoxygenation. J Biol Chem 2003, 278:38183-38187. 10.1074/jbc.M302244200, 12876291.
26. Luo W, Zhong J, Chang R, Hu H, Pandey A, Semenza GL. HSP70 and CHIP selectively mediate Ubiquitination and degradation of hypoxia-inducible factor (HIF)-1{alpha} but not HIF-2{alpha}. J Biol Chem 2010, 285:3651-3663. 10.1074/jbc.M109.068577, 19940151.
27. Yu B, Miao ZH, Jiang Y, Li MH, Yang N, Li T, Ding J. c-Jun protects hypoxia-inducible factor-1alpha from degradation via its oxygen-dependent degradation domain in a nontranscriptional manner. Cancer Res 2009, 69:7704-7712. 10.1158/0008-5472.CAN-09-0808, 19738058.
28. Triantafyllou A, Mylonis I, Simos G, Bonanou S, Tsakalof A. Flavonoids induce HIF-1alpha but impair its nuclear accumulation and activity. Free Radic Biol Med 2008, 44:657-670. 10.1016/j.freeradbiomed.2007.10.050, 18061585.
29. Liu YV, Semenza GL. RACK1 vs. HSP90: competition for HIF-1 alpha degradation vs. stabilization. Cell Cycle 2007, 6:656-659. 10.4161/cc.6.13.4435, 17361105.
30. Wang XH, Cavell BE, Syed Alwi SS, Packham G. Inhibition of hypoxia inducible factor by phenethyl isothiocyanate. Biochem Pharmacol 2009, 78:261-272. 10.1016/j.bcp.2009.04.010, 19376091.
31. Jones DT, Pugh CW, Wigfield S, Stevens MF, Harris AL. Novel thioredoxin inhibitors paradoxically increase hypoxia-inducible factor-alpha expression but decrease functional transcriptional activity, DNA binding, and degradation. Clin Cancer Res 2006, 12:5384-5394. 10.1158/1078-0432.CCR-05-2380, 17000671.
32. Maynard MA, Ohh M. The role of hypoxia-inducible factors in cancer. Cell Mol Life Sci 2007, 64:2170-2180. 10.1007/s00018-007-7082-2, 17514355.
33. Onnis B, Rapisarda A, Melillo G. Development of HIF-1 Inhibitors for Cancer Therapy. J Cell Mol Med 2009, 13:2780-2786. 10.1111/j.1582-4934.2009.00876.x, 2832082, 19674190.
34. Brinker AM, Ma J, Lipsky PE, Raskin I. Medicinal chemistry and pharmacology of genus Tripterygium (Celastraceae). Phytochemistry 2007, 68:732-766. 10.1016/j.phytochem.2006.11.029, 17250858.
35. Manolescu B, Oprea E, Busu C, Cercasov C. Natural compounds and the hypoxia-inducible factor (HIF) signalling pathway. Biochimie 2009, 91:1347-1358. 10.1016/j.biochi.2009.08.005, 19703512.
36. Tang XD, Zhou X, Zhou KY. Dauricine inhibits insulin-like growth factor-I-induced hypoxia inducible factor 1alpha protein accumulation and vascular endothelial growth factor expression in human breast cancer cells. Acta Pharmacol Sin 2009, 30:605-616. 10.1038/aps.2009.8, 19349962.
37. Vispe S, DeVries L, Creancier L, Besse J, Breand S, Hobson DJ, Svejstrup JQ, Annereau JP, Cussac D, Dumontet C, Guilbaud N, Barret JM, Bailly C. Triptolide is an inhibitor of RNA polymerase I and II-dependent transcription leading predominantly to down-regulation of short-lived mRNA. Mol Cancer Ther 2009, 8:2780-2790. 10.1158/1535-7163.MCT-09-0549, 19808979.
38. Leuenroth SJ, Crews CM. Triptolide-induced transcriptional arrest is associated with changes in nuclear substructure. Cancer Res 2008, 68:5257-5266. 10.1158/0008-5472.CAN-07-6207, 2587069, 18593926.
39. Demidenko ZN, Rapisarda A, Garayoa M, Giannakakou P, Melillo G, Blagosklonny MV. Accumulation of hypoxia-inducible factor-1alpha is limited by transcription-dependent depletion. Oncogene 2005, 24:4829-4838. 10.1038/sj.onc.1208636, 15897903.
40. Weidemann A, Johnson RS. Biology of HIF-1alpha. Cell Death Differ 2008, 15:621-627. 10.1038/cdd.2008.12, 18259201.
41. Aoyagi Y, Hitotsuyanagi Y, Hasuda T, Matsuyama S, Fukaya H, Takeya K, Aiyama R, Matsuzaki T, Hashimoto S. Fluorination of triptolide and its analogues and their cytotoxicity. Bioorg Med Chem Lett 2008, 18:2459-2463. 10.1016/j.bmcl.2008.02.039, 18321701.
42. Li W, Shao Y, Hu L, Zhang X, Chen Y, Tong L, Li C, Shen X, Ding J. BM6, a new semi-synthetic vinca alkaloid, exhibits its potent in vivo anti-tumor activities via its high binding affinity for tubulin and improved pharmacokinetic profiles. Cancer Biol Ther 2007, 6:787-794. 10.4161/cbt.6.5.4006, 17387272.
43. Tao Z, Zhou Y, Lu J, Duan W, Qin Y, He X, Lin L, Ding J. Caspase-8 preferentially senses the apoptosis-inducing action of NG-18, a Gambogic acid derivative, in human leukemia HL-60 cells. Cancer Biol Ther 2007, 6:691-696. 10.4161/cbt.6.5.3960, 17426447.
44. Hong SH, Kim J, Kim JM, Lee SY, Shin DS, Son KH, Han DC, Sung YK, Kwon BM. Apoptosis induction of 2'-hydroxycinnamaldehyde as a proteasome inhibitor is associated with ER stress and mitochondrial perturbation in cancer cells. Biochem Pharmacol 2007, 74:557-565. 10.1016/j.bcp.2007.05.016, 17606223.
45. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001, 25:402-408. 10.1006/meth.2001.1262, 11846609.
46. Dai M, Miao ZH, Ren X, Tong LJ, Yang N, Li T, Lin LP, Shen YM, Ding J. MFTZ-1 reduces constitutive and inducible HIF-1alpha accumulation and VEGF secretion independent of its topoisomerase II inhibition. J Cell Mol Med 2009,
47. Sowter HM, Raval RR, Moore JW, Ratcliffe PJ, Harris AL. Predominant role of hypoxia-inducible transcription factor (Hif)-1alpha versus Hif-2alpha in regulation of the transcriptional response to hypoxia. Cancer Res 2003, 63:6130-6134.
48. Feng JM, Zhu H, Zhang XW, Ding J, Miao ZH. Proteasome-dependent degradation of Chk1 kinase induced by the topoisomerase II inhibitor R16 contributes to its anticancer activity. Cancer Biol Ther 2008, 7:1726-1731.
49. Sun QM, Miao ZH, Lin LP, Gui M, Zhu CH, Xie H, Duan WH, Ding J. BB, a new EGFR inhibitor, exhibits prominent anti-angiogenesis and antitumor activities. Cancer Biol Ther 2009, 8:1640-1647. 10.4161/cbt.8.17.9205, 19625781.