Triptolide downregulates treg cells and the level of IL-10, TGF-β, and VEGF in melanoma-bearing mice

Planta Medica

Volumn 79, Issue 15, 2013, Pages 1401-1407

  Liu, Biao ^a   Zhang, Hongqi ^b   Li, Jian ^c   Lu, Cheng ^a   Chen, Gao ^d   Zhang, Ge ^b   Lu, Aiping ^a,e   He, Xiaojuan ^a  

^a INSTITUTE OF CHINESE MATERIA MEDICA   (China)

^b HONG KONG BAPTIST UNIVERSITY   (Hong Kong)

^c BEIJING UNIVERSITY OF CHINESE MEDICINE   (China)

^d HUBEI UNIVERSITY   (China)

^e SHANGHAI UNIVERSITY OF TRADITIONAL CHINESE MEDICINE   (China)

Author keywords

Celastraceae; cytokines; melanoma; regulatory T cells; Tripterygium wilfordii; triptolide

Indexed keywords

CYCLOPHOSPHAMIDE; INTERLEUKIN 10; MESSENGER RNA; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA; TRIPTOLIDE; VASCULOTROPIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AXILLARY LYMPH NODE; CANCER GROWTH; CANCER INHIBITION; CANCER TISSUE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DOWN REGULATION; DRUG MEGADOSE; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GENE EXPRESSION; HYPOTHESIS; LOW DRUG DOSE; MALE; MELANOMA; MOUSE; NONHUMAN; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY T LYMPHOCYTE; SPLEEN;

CELASTRACEAE; MUS; TRIPTERYGIUM WILFORDII;

ANIMALS; ANTINEOPLASTIC AGENTS, PHYTOGENIC; DISEASE MODELS, ANIMAL; DITERPENES; DOWN-REGULATION; DRUGS, CHINESE HERBAL; EPOXY COMPOUNDS; FORKHEAD TRANSCRIPTION FACTORS; INTERLEUKIN-10; LYMPH NODES; MALE; MELANOMA; MICE, INBRED C57BL; PHENANTHRENES; PHYTOTHERAPY; RNA, MESSENGER; SPLEEN; T-LYMPHOCYTES, REGULATORY; TRANSFORMING GROWTH FACTOR BETA; TRIPTERYGIUM; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84886096385     PISSN: 00320943     EISSN: 14390221     Source Type: Journal    
DOI: 10.1055/s-0033-1350708     Document Type: Article

References (50)

1. Antonoff M. B., Chugh R., Borja-Cacho D., Dudeja V., Clawson K. A., Skube S. J., Sorenson B. S., Saltzman D. A., Vickers S. M., Saluja A. K. Triptolide therapy for neuroblastoma decreases cell viability in vitro and inhibits tumor growth in vivo. Surgery: 2009; 146 282 290
2. Liu J., Jiang Z., Xiao J., Zhang Y., Lin S., Duan W., Yao J., Liu C., Huang X., Wang T., Liang Z., Wang R., Zhang S., Zhang L. Effects of triptolide from Tripterygium wilfordii on ERalpha and p 53 expression in two human breast cancer cell lines. Phytomedicine: 2009; 16 1006 1013
3. Chugh R., Sangwan V., Patil S. P., Dudeja V., Dawra R. K., Banerjee S., Schumacher R. J., Blazar B. R., Georg G. I., Vickers S. M., Saluja A. K. A preclinical evaluation of Minnelide as a therapeutic agent against pancreatic cancer. Sci Transl Med: 2012; 4 156ra139
4. Kiviharju T. M., Lecane P. S., Sellers R. G., Peehl D. M. 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 (Pubitemid 34856355)
5. 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
6. He M. F., Huang Y. H., Wu L. W., Ge W., Shaw P. C., But P. P. Triptolide functions as a potent angiogenesis inhibitor. Int J Cancer: 2010; 126 266 278
7. Zhao H., Yang Z., Wang X., Zhang X., Wang M., Wang Y., Mei Q., Wang Z. 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
8. Yinjun L., Jie J., Yungui W. Triptolide inhibits transcription factor NF-kappaB and induces apoptosis of multiple myeloma cells. Leuk Res: 2005; 29 99 105 (Pubitemid 39487915)
9. Qiu D., Zhao G., Aoki Y., Shi L., Uyei A., Nazarian S., Ng J. C., Kao P. N. Immunosuppressant PG490 (triptolide) inhibits T-cell interleukin-2 expression at the level of purine-box/nuclear factor of activated T-cells and NF-kappaB transcriptional activation. J Biol Chem: 1999; 274 13443 13450
10. Wang Y., Lu J. J., He L., Yu Q. Triptolide (TPL) inhibits global transcription by inducing proteasome-dependent degradation of RNA polymerase II (Pol II). PloS One: 2011; 6 e23993
11. Ménétrier-Caux C., Gobert M., Caux C. Differences in tumor regulatory T-cell localization and activation status impact patient outcome. Cancer Res: 2009; 69 7895 7898
12. Lindau D., Gielen P., Kroesen M., Wesseling P., Adema G. J. The immunosuppressive tumour network: myeloid-derived suppressor cells, regulatory T cells and natural killer T cells. Immunology: 2013; 138 105 115
13. Miller A. M., Lundberg K., Ozenci V., Banham A. H., Hellstrom M., Egevad L., Pisa P. CD4+CD25high T cells are enriched in the tumor and peripheral blood of prostate cancer patients. J Immunol: 2006; 177 7398 7405 (Pubitemid 44715110)
14. Petersen R. P., Campa M. J., Sperlazza J., Conlon D., Joshi M. B., Harpole D. H. jr., Patz E. F. jr. Tumor infiltrating Foxp3+ regulatory T-cells are associated with recurrence in pathologic stage I NSCLC patients. Cancer: 2006; 107 2866 2872 (Pubitemid 44937041)
15. Huang Y., Wang F. M., Wang T., Wang Y. J., Zhu Z. Y., Gao Y. T., Du Z. Tumor-infiltrating FoxP3+ regs and CD8+ T cells affect the prognosis of hepatocellular carcinoma patients. Digestion: 2012; 86 329 337
16. Wang Y., Ma Y., Fang Y., Wu S., Liu L., Fu D., Shen X. Regulatory T cell: a protection for tumour cells. J Cell Mol Med: 2012; 16 425 436
17. Beyer M., Schultze J. L. Regulatory T cells in cancer. Blood: 2006; 108 804 811 (Pubitemid 44154611)
18. Liu Y., Chen Y., Liu F. Q., Lamb J. R., Tam P. K. Combined treatment with triptolide and rapamycin prolongs graft survival in a mouse model of cardiac transplantation. Transpl Int: 2008; 21 483 494 (Pubitemid 351490170)
19. Zhang G., Liu Y., Guo H., Sun Z., Zhou Y. H. Triptolide promotes generation of FoxP3+ T regulatory cells in rats. J Ethnopharmacol: 2009; 125 41 46
20. Facciabene A., Motz G. T., Coukos G. T-regulatory cells: key players in tumor immune escape and angiogenesis. Cancer Res: 2012; 72 2162 2171
21. Cohen A. D., Diab A., Perales M. A., Wolchok J. D., Rizzuto G., Merghoub T., Huggins D., Liu C., Turk M. J., Restifo N. P., Sakaguchi S., Houghton A. N. Agonist anti-GITR antibody enhances vaccine-induced CD8(+) T-cell responses and tumor immunity. Cancer Res: 2006; 66 4904 4912
22. Ghiringhelli F., Menard C., Puig P. E., Ladoire S., Roux S., Martin F., Solary E., Le Cesne A., Zitvogel L., Chauffert B. Metronomic cyclophosphamide regimen selectively depletes CD4+CD25+ regulatory T cells and restores T and NK effector functions in end stage cancer patients. Cancer Immunol Immunother: 2007; 56 641 648 (Pubitemid 46348738)
23. Sutmuller R. P., van Duivenvoorde L. M., van Elsas A., Schumacher T. N., Wildenberg M. E., Allison J. P., Toes R. E., Offringa R., Melief C. J. Synergism of cytotoxic T lymphocyte-associated antigen 4 blockade and depletion of CD25(+) regulatory T cells in antitumor therapy reveals alternative pathways for suppression of autoreactive cytotoxic T lymphocyte responses. J Exp Med: 2001; 194 823 832 (Pubitemid 32983017)
24. Rasku M. A., Clem A. L., Telang S., Taft B., Gettings K., Gragg H., Cramer D., Lear S. C., McMasters K. M., Miller D. M., Chesney J. Transient T cell depletion causes regression of melanoma metastases. J Transl Med: 2008; 6 12
25. Fontenot J. D., Gavin M. A., Rudensky A. Y. Foxp3 programs the development and function of CD4+CD25+ regulatory T cells. Nat Immunol: 2003; 4 330 336 (Pubitemid 36432314)
26. Liang J., Chen H., Pan W., Xu C. Puerarin inhibits caspase-3 expression in osteoblasts of diabetic rats. Mol Med Rep: 2012; 5 1419 1422
27. Yu Z., Li W. Induction of apoptosis by puerarin in colon cancer HT-29 cells. Cancer Lett: 2006; 238 53 60 (Pubitemid 43851146)
28. Tao Y., Zhang M. L., Ma P. C., Sun J. F., Zhou W. Q., Cao Y. P., Li L. J. Triptolide inhibits proliferation and induces apoptosis of human melanoma A375 cells. Asian Pac J Cancer Prev: 2012; 13 1611 1615
29. Lu N., Liu J., Liu J., Zhang C., Jiang F., Wu H., Chen L., Zeng W., Cao X., Yan T., Wang G., Zhou H., Lin B., Yan X., Zhang X. K., Zeng J. Z. Antagonist effect of triptolide on AKT activation by truncated retinoid X receptor-alpha. PLoS One: 2012; 7 e35722
30. Manzo S. G., Zhou Z. L., Wang Y. Q., Marinello J., He J. X., Li Y. C., Ding J., Capranico G., Miao Z. H. Natural product triptolide mediates cancer cell death by triggering CDK7-dependent degradation of RNA polymerase II. Cancer Res: 2012; 72 5363 5373
31. Lu L., Kanwar J., Schmitt S., Cui Q. C., Zhang C., Zhao C., Dou Q. P. Inhibition of tumor cellular proteasome activity by triptolide extracted from the Chinese medicinal plant thunder god vine Anticancer Res: 2011; 31 1 10
32. Miyara M., Sakaguchi S. Natural regulatory T cells: mechanisms of suppression. Trends Mol Med: 2007; 13 108 116 (Pubitemid 46341958)
33. Jankovic D., Kullberg M. C., Feng C. G., Goldszmid R. S., Collazo C. M., Wilson M., Wynn T. A., Kamanaka M., Flavell R. A., Sher A. Conventional T-bet(+)Foxp3(-) Th1 cells are the major source of host-protective regulatory IL-10 during intracellular protozoan infection. J Exp Med: 2007; 204 273 283 (Pubitemid 46294544)
34. Dercamp C., Chemin K., Caux C., Trinchieri G., Vicari A. P. Distinct and overlapping roles of interleukin-10 and CD25+ regulatory T cells in the inhibition of antitumor CD8 T-cell responses. Cancer Res: 2005; 65 8479 8486 (Pubitemid 41330616)
35. Strauss L., Bergmann C., Szczepanski M., Gooding W., Johnson J. T., Whiteside T. L. A unique subset of CD4+CD25highFoxp3+ T cells secreting interleukin-10 and transforming growth factor-beta1 mediates suppression in the tumor microenvironment. Clin Cancer Res: 2007; 13 4345 4354 (Pubitemid 47219698)
36. Powrie F., Carlino J., Leach M. W., Mauze S., Coffman R. L. A critical role for transforming growth factor-beta but not interleukin 4 in the suppression of T helper type 1-mediated colitis by CD45RB(low) CD4+ T cells. J Exp Med: 1996; 183 2669 2674
37. Massague J. TGFbeta in cancer. Cell: 2008; 134 215 230
38. Javelaud D., Alexaki V. I., Mauviel A. Transforming growth factor-beta in cutaneous melanoma. Pigment Cell Melanoma Res: 2008; 21 123 132 (Pubitemid 351551229)
39. Meulmeester E., Ten Dijke P. The dynamic roles of TGF- β in cancer. J Pathol: 2011; 223 205 218
40. Guise T. Examining the metastatic niche: targeting the microenvironment. Semin Oncol: 2010; 37 S2 S14
41. Yamagiwa S., Gray J. D., Hashimoto S., Horwitz D. A. A role for TGF-beta in the generation and expansion of CD4+CD25+ regulatory T cells from human peripheral blood. J Immunol: 2001; 166 7282 7289 (Pubitemid 32525603)
42. Chen W., Jin W., Hardegen N., Lei K. J., Li L., Marinos N., McGrady G., Wahl S. M. Conversion of peripheral CD4+CD25- naive T cells to CD4+CD25+ regulatory T cells by TGF-beta induction of transcription factor Foxp3. J Exp Med: 2003; 198 1875 1886 (Pubitemid 38032120)
43. Beck C., Schreiber H., Rowley D. Role of TGF-beta in immune-evasion of cancer. Microsc Res Tech: 2001; 52 387 395
44. Leek R. D. The prognostic role of angiogenesis in breast cancer. Anticancer Res: 2001; 21 4325 4331 (Pubitemid 34240962)
45. Grothey A., Allegra C. Antiangiogenesis therapy in the treatment of metastatic colorectal cancer. Ther Adv Med Oncol: 2012; 4 301 319
46. Ferrara N., Gerber H. P., LeCouter J. The biology of VEGF and its receptors. Nat Med: 2003; 9 669 676 (Pubitemid 36749215)
47. Ning H., Shao Q. Q., Ding K. J., Gao D. X., Lu Q. L., Cao Q. W., Niu Z. H., Fu Q., Zhang C. H., Qu X., Lü J. J. Tumor-infiltrating regulatory T cells are positively correlated with angiogenic status in renal cell carcinoma. Chin Med J (Engl): 2012; 125 2120 2125
48. Terme M., Pernot S., Marcheteau E., Sandoval F., Benhamouda N., Colussi O., Dubreuil O., Carpentier A. F., Tartour E., Taieb J. VEGFA-VEGFR pathway blockade inhibits tumor-induced regulatory T-cell proliferation in colorectal cancer. Cancer Res: 2013; 73 539 549
49. Hu K. B., Liu Z. H., Guo X. H., Liu D., Li L. S. Triptolide inhibits vascular endothelial growth factor expression and production in endothelial cells. Acta Pharmacol Sin: 2001; 22 651 656 (Pubitemid 32656496)
50. Johnson S. M., Wang X., Evers B. M. Triptolide inhibits proliferation and migration of colon cancer cells by inhibition of cell cycle regulators and cytokine receptors. J Surg Res: 2011; 168 197 205