Herbal compound triptolide synergistically enhanced antitumor activity of amino-terminal fragment of urokinase

Molecular Cancer

Volumn 12, Issue 1, 2013, Pages

  Lin, Yuli ^a   Peng, Nana ^a   Li, Jianping ^a   Zhuang, Hongqin ^a,b   Hua, Zi Chun ^a,b  

^a NANJING UNIVERSITY   (China)

^b Jiangsu TargetPharma Laboratories Inc   (China)

Author keywords

Amino terminal fragment of urokinase; Apoptosis; Cell cycle; Cell migration; Synergism; Triptolide; Xenograft

Indexed keywords

CASPASE 3; CASPASE 9; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; TRIPTOLIDE; UROKINASE; UROKINASE RECEPTOR;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CELL CYCLE; CELL CYCLE ARREST; CELL MIGRATION; CELL PROLIFERATION; COLON CANCER; CONTROLLED STUDY; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; SOLID TUMOR; TUMOR CELL; TUMOR XENOGRAFT;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; CELL CYCLE CHECKPOINTS; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; COLONIC NEOPLASMS; DITERPENES; DRUG SYNERGISM; EPOXY COMPOUNDS; HCT116 CELLS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; MALE; MICE; PEPTIDES; PHENANTHRENES; SIGNAL TRANSDUCTION; TUMOR BURDEN; UROKINASE-TYPE PLASMINOGEN ACTIVATOR; XENOGRAFT MODEL ANTITUMOR ASSAYS;

TRIPTERYGIUM WILFORDII;

EID: 84878640001     PISSN: None     EISSN: 14764598     Source Type: Journal    
DOI: 10.1186/1476-4598-12-54     Document Type: Article

References (72)

1. Foekens JA, Schmitt M, Van Putten WL, Peters HA, Bontenbal M, Janicke F, Klijn JG. Prognostic value of urokinase-type plasminogen activator in 671 primary breast cancer patients. Cancer Res 1992, 52:6101-6105.
2. Laufs S, Schumacher J, Allgayer H. Urokinase-receptor (u-PAR): an essential player in multiple games of cancer: a review on its role in tumour progression, invasion, metastasis, proliferation/dormancy, clinical outcome and minimal residual disease. Cell Cycle 2006, 5:1760-1771. 10.4161/cc.5.16.2994, 16931909.
3. Choong PF, Nadesapillai AP. Urokinase plasminogen activator system: a multifunctional role in tumour progression and metastasis. Clin Orthop Relat Res 2003, (415):S46-S58.
4. Reuning U, Magdolen V, Wilhelm O, Fischer K, Lutz V, Graeff H, Schmitt M. Multifunctional potential of the plasminogen activation system in tumour invasion and metastasis (review). Int J Oncol 1998, 13:893-906.
5. Dano K, Andreasen PA, Grondahl-Hansen J, Kristensen P, Nielsen LS, Skriver L. Plasminogen activators, tissue degradation, and cancer. Adv Cancer Res 1985, 44:139-266.
6. Andreasen PA, Egelund R, Petersen HH. The plasminogen activation system in tumour growth, invasion, and metastasis. Cell Mol Life Sci 2000, 57:25-40. 10.1007/s000180050497, 10949579.
7. Liu D, Aguirre GJ, Estrada Y, Ossowski L. EGFR is a transducer of the urokinase receptor initiated signal that is required for in vivo growth of a human carcinoma. Cancer Cell 2002, 1:445-457. 10.1016/S1535-6108(02)00072-7, 12124174.
8. Wei Y, Lukashev M, Simon DI, Bodary SC, Rosenberg S, Doyle MV, Chapman HA. Regulation of integrin function by the urokinase receptor. Science 1996, 273:1551-1555. 10.1126/science.273.5281.1551, 8703217.
9. Mars WM, Jo M, Gonias SL. Activation of hepatocyte growth factor by urokinase-type plasminogen activator is ionic strength-dependent. Biochem J 2005, 390:311-315. 10.1042/BJ20042028, 1184584, 15869463.
10. Koolwijk P, Van Erck MG, De Vree WJ, Vermeer MA, Weich HA, Hanemaaijer R, Van HV. Cooperative effect of TNFalpha, bFGF, and VEGF on the formation of tubular structures of human microvascular endothelial cells in a fibrin matrix. Role of urokinase activity. J Cell Biol 1996, 132:1177-1188. 10.1083/jcb.132.6.1177, 2120755, 8601593.
11. Rabbani SA, Gladu J. Urokinase receptor antibody can reduce tumour volume and detect the presence of occult tumour metastases in vivo. Cancer Res 2002, 62:2390-2397.
12. Kobayashi H, Gotoh J, Shinohara H, Moniwa N, Terao T. Inhibition of the metastasis of Lewis lung carcinoma by antibody against urokinase-type plasminogen activator in the experimental and spontaneous metastasis model. Thromb Haemost 1994, 71:474-480.
13. Li H, Soria C, Griscelli F, Opolon P, Soria J, Yeh P, Legrand C, Vannier JP, Belin D, Perricaudet M, Lu H. Amino-terminal fragment of urokinase inhibits tumour cell invasion in vitro and in vivo: respective contribution of the urokinase plasminogen activator receptor-dependent or -independent pathway. Hum Gene Ther 2005, 16:1157-1167. 10.1089/hum.2005.16.1157, 16218777.
14. Li H, Griscelli F, Lindenmeyer F, Opolon P, Sun LQ, Connault E, Soria J, Soria C, Perricaudet M, Yeh P, Lu H. Systemic delivery of antiangiogenic adenovirus AdmATF induces liver resistance to metastasis and prolongs survival of mice. Hum Gene Ther 1999, 10:3045-3053. 10.1089/10430349950016438, 10609663.
15. Mohanam S, Chandrasekar N, Yanamandra N, Khawar S, Mirza F, Dinh DH, Olivero WC, Rao JS. Modulation of invasive properties of human glioblastoma cells stably expressing amino-terminal fragment of urokinase-type plasminogen activator. Oncogene 2002, 21:7824-7830. 10.1038/sj.onc.1205893, 12420219.
16. Tao X, Younger J, Fan FZ, Wang B, Lipsky PE. Benefit of an extract of Tripterygium Wilfordii Hook F in patients with rheumatoid arthritis: a double-blind, placebo-controlled study. Arthritis Rheum 2002, 46:1735-1743. 10.1002/art.10411, 12124856.
17. Matta R, Wang X, Ge H, Ray W, Nelin LD, Liu Y. Triptolide induces anti-inflammatory cellular responses. Am J Transl Res 2009, 1:267-282. 2776323, 19956437.
18. Chen BJ. Triptolide, a novel immunosuppressive and anti-inflammatory agent purified from a Chinese herb Tripterygium wilfordii Hook F. Leuk Lymphoma 2001, 42:253-265. 10.3109/10428190109064582, 11699390.
19. 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.
20. Kupchan SM, Court WA, Dailey RG, Gilmore CJ, Bryan RF. Triptolide and tripdiolide, novel antileukemic diterpenoid triepoxides from Tripterygium wilfordii. J Am Chem Soc 1972, 94:7194-7195. 10.1021/ja00775a078, 5072337.
21. Liu Q. Triptolide and its expanding multiple pharmacological functions. Int Immunopharmacol 2011, 11:377-383. 10.1016/j.intimp.2011.01.012, 21255694.
22. 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 1998, 133:169-175. 10.1016/S0304-3835(98)00222-5, 10072166.
23. 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 tumours. Mol Cancer Ther 2003, 2:65-72.
24. Tang XY, Zhu YQ, Tao WH, Wei B, Lin XL. Synergistic effect of triptolide combined with 5-fluorouracil on colon carcinoma. Postgrad Med J 2007, 83:338-343. 10.1136/pgmj.2006.055426, 2600066, 17488865.
25. Xu B, Guo X, Mathew S, Armesilla AL, Cassidy J, Darling JL, Wang W. 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. 10.1016/j.canlet.2009.10.013, 19903580.
26. Westfall SD, Nilsson EE, Skinner MK. Role of triptolide as an adjunct chemotherapy for ovarian cancer. Chemotherapy 2008, 54:67-76. 10.1159/000112419, 18073474.
27. Huynh PN, Hikim AP, Wang C, Stefonovic K, Lue YH, Leung A, Atienza V, Baravarian S, Reutrakul V, Swerdloff RS. Long-term effects of triptolide on spermatogenesis, epididymal sperm function, and fertility in male rats. J Androl 2000, 21:689-699.
28. Ye X, Li W, Yan Y, Mao C, Cai R, Xu H, Yang X. Effects of cytochrome P4503A inducer dexamethasone on the metabolism and toxicity of triptolide in rat. Toxicol Lett 2010, 192:212-220. 10.1016/j.toxlet.2009.10.028, 19879934.
29. Fidler JM, Li K, Chung C, Wei K, Ross JA, Gao M, Rosen GD. PG490-88, a derivative of triptolide, causes tumour regression and sensitizes tumours to chemotherapy. Mol Cancer Ther 2003, 2:855-862.
30. 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. 10.1038/emm.2002.64, 12526088.
31. Dan HC, Cooper MJ, Cogswell PC, Duncan JA, Ting JP, Baldwin AS. Akt-dependent regulation of NF-{kappa}B is controlled by mTOR and Raptor in association with IKK. Genes Dev 2008, 22:1490-1500. 10.1101/gad.1662308, 2418585, 18519641.
32. Rogers R, Ouellet G, Brown C, Moyer B, Rasoulpour T, Hixon M. Cross-talk between the Akt and NF-kappaB signalling pathways inhibits MEHP-induced germ cell apoptosis. Toxicol Sci 2008, 106:497-508. 10.1093/toxsci/kfn186, 2581679, 18755736.
33. Ouyang DY, Wang YY, Zheng YT. Activation of c-Jun N-terminal kinases by ribotoxic stresses. Cell Mol Immunol 2005, 2:419-425.
34. Dhanasekaran DN, Reddy EP. JNK signalling in apoptosis. Oncogene 2008, 27:6245-6251. 10.1038/onc.2008.301, 3063296, 18931691.
35. Blasi F, Carmeliet P. uPAR: a versatile signalling orchestrator. Nat Rev Mol Cell Biol 2002, 3:932-943. 10.1038/nrm977, 12461559.
36. Zhou H, Tang Y, Liang X, Yang X, Yang J, Zhu G, Zheng M, Zhang C. RNAi targeting urokinase-type plasminogen activator receptor inhibits metastasis and progression of oral squamous cell carcinoma in vivo. Int J Cancer 2009, 125:453-462. 10.1002/ijc.24360, 19391133.
37. Greenlee RT, Hill-Harmon MB, Murray T, Thun M. Cancer statistics, 2001. CA Cancer J Clin 2001, 51:15-36. 10.3322/canjclin.51.1.15, 11577478.
38. Sohma I, Fujiwara Y, Sugita Y, Yoshioka A, Shirakawa M, Moon JH, Takiguchi S, Miyata H, Yamasaki M, Mori M, Doki Y. Parthenolide, an NF-kappaB inhibitor, suppresses tumour growth and enhances response to chemotherapy in gastric cancer. CANCER GENOMICS PROTEOMICS 2011, 8:39-47.
39. Friedberg JW, Vose JM, Kelly JL, Young F, Bernstein SH, Peterson D, Rich L, Blumel S, Proia NK, Liesveld J, Fisher RI, Armitage JO, Grant S, Leonard JP. The combination of bendamustine, bortezomib, and rituximab for patients with relapsed/refractory indolent and mantle cell non-Hodgkin lymphoma. Blood 2011, 117:2807-2812. 10.1182/blood-2010-11-314708, 3062293, 21239695.
40. Duffy MJ. Proteases as prognostic markers in cancer. Clin Cancer Res 1996, 2:613-618.
41. Shimizu M, Cohen B, Goldvasser P, Berman H, Virtanen C, Reedijk M. Plasminogen activator uPA is a direct transcriptional target of the JAG1-Notch receptor signalling pathway in breast cancer. Cancer Res 2011, 71:277-286. 10.1158/0008-5472.CAN-10-2523, 21199807.
42. Dear AE, Medcalf RL. The urokinase-type-plasminogen-activator receptor (CD87) is a pleiotropic molecule. Eur J Biochem 1998, 252:185-193. 10.1046/j.1432-1327.1998.2520185.x, 9523687.
43. Zhu F, Jia S, Xing G, Gao L, Zhang L, He F. cDNA transfection of amino-terminal fragment of urokinase efficiently inhibits cancer cell invasion and metastasis. DNA Cell Biol 2001, 20:297-305. 10.1089/104454901750232490, 11410166.
44. Li H, Lu H, Griscelli F, Opolon P, Sun LQ, Ragot T, Legrand Y, Belin D, Soria J, Soria C, Perricaudet M, Yeh P. Adenovirus-mediated delivery of a uPA/uPAR antagonist suppresses angiogenesis-dependent tumour growth and dissemination in mice. Gene Ther 1998, 5:1105-1113. 10.1038/sj.gt.3300742, 10326034.
45. Lue Y, Sinha Hikim AP, Wang C, Leung A, Baravarian S, Reutrakul V, Sangsawan R, Chaichana S, Swerdloff RS. Triptolide: a potential male contraceptive. J Androl 1998, 19:479-486.
46. Qiu D, Kao PN. Immunosuppressive and anti-inflammatory mechanisms of triptolide, the principal active diterpenoid from the Chinese medicinal herb Tripterygium wilfordii Hook. f. Drugs R&D 2003, 4:1-18.
47. Liu Q, Chen T, Chen G, Shu X, Sun A, Ma P, Lu L, Cao X. Triptolide impairs dendritic cell migration by inhibiting CCR7 and COX-2 expression through PI3-K/Akt and NF-kappaB pathways. Mol Immunol 2007, 44:2686-2696. 10.1016/j.molimm.2006.12.003, 17223196.
48. Zhou B, Miao Z, Deng G, Ding J, Yang Y, Feng H, Li Y. Synthesis and biological evaluation of novel triptolide analogues for anticancer activity. Bioorg Med Chem Lett 2010, 20:6217-6221. 10.1016/j.bmcl.2010.08.106, 20833543.
49. Shamon LA, Pezzuto JM, Graves JM, Mehta RR, Wangcharoentrakul S, Sangsuwan R, Chaichana S, Tuchinda P, Cleason P, Reutrakul V. Evaluation of the mutagenic, cytotoxic, and antitumor potential of triptolide, a highly oxygenated diterpene isolated from Tripterygium wilfordii. Cancer Lett 1997, 112:113-117. 10.1016/S0304-3835(96)04554-5, 9029176.
50. Kitzen JJ, De Jonge MJ, Lamers CH, Eskens FA, Van Der BD, Van DL, Ter SJ, Brandely M, Puozzo C, Verweij J. Phase I dose-escalation study of F60008, a novel apoptosis inducer, in patients with advanced solid tumours. Eur J Cancer 2009, 45:1764-1772. 10.1016/j.ejca.2009.01.026, 19251409.
51. Lee KY, Chang W, Qiu D, Kao PN, Rosen GD. PG490 (triptolide) cooperates with tumour necrosis factor-alpha to induce apoptosis in tumour cells. J Biol Chem 1999, 274:13451-13455. 10.1074/jbc.274.19.13451, 10224110.
52. Chang WT, Kang JJ, Lee KY, Wei K, Anderson E, Gotmare S, Ross JA, Rosen GD. Triptolide and chemotherapy cooperate in tumour cell apoptosis. A role for the p53 pathway. J Biol Chem 2001, 276:2221-2227.
53. Yang M, Huang J, Pan HZ, Jin J. Triptolide overcomes dexamethasone resistance and enhanced PS-341-induced apoptosis via PI3k/Akt/NF-kappaB pathways in human multiple myeloma cells. Int J Mol Med 2008, 22:489-496.
54. Kang DW, Lee JY, Oh DH, Park SY, Woo TM, Kim MK, Park MH, Jang YH, Min DS. Triptolide-induced suppression of phospholipase D expression inhibits proliferation of MDA-MB-231 breast cancer cells. Exp Mol Med 2009, 41:678-685. 10.3858/emm.2009.41.9.074, 2753661, 19478552.
55. Li-Weber M. Targeting apoptosis pathways in cancer by Chinese medicine. Cancer Lett 2010, 332:304-312.
56. Papa S, Zazzeroni F, Pham CG, Bubici C, Franzoso G. Linking JNK signalling to NF-kappaB: a key to survival. J Cell Sci 2004, 117:5197-5208. 10.1242/jcs.01483, 15483317.
57. Chang L, Kamata H, Solinas G, Luo JL, Maeda S, Venuprasad K, Liu YC, Karin M. The E3 ubiquitin ligase itch couples JNK activation to TNFalpha-induced cell death by inducing c-FLIP(L) turnover. Cell 2006, 124:601-613. 10.1016/j.cell.2006.01.021, 16469705.
58. Freedman DA, Wu L, Levine AJ. Functions of the MDM2 oncoprotein. Cell Mol Life Sci 1999, 55:96-107. 10.1007/s000180050273, 10065155.
59. Zhao F, Chen Y, Li R, Liu Y, Wen L, Zhang C. Triptolide alters histone H3K9 and H3K27 methylation state and induces G0/G1 arrest and caspase-dependent apoptosis in multiple myeloma in vitro. Toxicology 2010, 267:70-79. 10.1016/j.tox.2009.10.023, 19879315.
60. Barre B, Perkins ND. A cell cycle regulatory network controlling NF-kappaB subunit activity and function. EMBO J 2007, 26:4841-4855. 10.1038/sj.emboj.7601899, 2099464, 17962807.
61. 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.
62. Zhang C, Cui GH, Liu F, Wu QL, Chen Y. Inhibitory effect of triptolide on lymph node metastasis in patients with non-Hodgkin lymphoma by regulating SDF-1/CXCR4 axis in vitro. Acta Pharmacol Sin 2006, 27:1438-1446. 10.1111/j.1745-7254.2006.00415.x, 17049119.
63. Chang HJ, Kim MH, Baek MK, Park JS, Chung IJ, Shin BA, Ahn BW, Jung YD. Triptolide inhibits tumour promoter-induced uPAR expression via blocking NF-kappaB signalling in human gastric AGS cells. Anticancer Res 2007, 27:3411-3417.
64. Carriero MV, Del VS, Franco P, Potena MI, Chiaradonna F, Botti G, Stoppelli MP, Salvatore M. Vitronectin binding to urokinase receptor in human breast cancer. Clin Cancer Res 1997, 3:1299-1308.
65. Kanse SM, Kost C, Wilhelm OG, Andreasen PA, Preissner KT. The urokinase receptor is a major vitronectin-binding protein on endothelial cells. Exp Cell Res 1996, 224:344-353. 10.1006/excr.1996.0144, 8612711.
66. Nykjaer A, Conese M, Christensen EI, Olson D, Cremona O, Gliemann J, Blasi F. Recycling of the urokinase receptor upon internalization of the uPA:serpin complexes. EMBO J 1997, 16:2610-2620. 10.1093/emboj/16.10.2610, 1169872, 9184208.
67. Li Y, Knisely JM, Lu W, McCormick LM, Wang J, Henkin J, Schwartz AL, Bu G. Low density lipoprotein (LDL) receptor-related protein 1B impairs urokinase receptor regeneration on the cell surface and inhibits cell migration. J Biol Chem 2002, 277:42366-42371. 10.1074/jbc.M207705200, 12194987.
68. 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.
69. Ossowski L, Guirre-Ghiso JA. Urokinase receptor and integrin partnership: coordination of signalling for cell adhesion, migration and growth. Curr Opin Cell Biol 2000, 12:613-620. 10.1016/S0955-0674(00)00140-X, 10978898.
70. Yan C, Boyd DD. Regulation of matrix metalloproteinase gene expression. J Cell Physiol 2007, 211:19-26. 10.1002/jcp.20948, 17167774.
71. Li S, Dong W, Zong Y, Yin W, Jin G, Hu Q, Huang X, Jiang W, Hua ZC. Polyethylenimine-complexed plasmid particles targeting focal adhesion kinase function as melanoma tumour therapeutics. Mol Ther 2007, 15:515-523. 10.1038/sj.mt.6300072, 17285141.
72. Chou TC. Theoretical basis, experimental design, and computerized simulation of synergism and antagonism in drug combination studies. Pharmacol Rev 2006, 58:621-681. 10.1124/pr.58.3.10, 16968952.