Tanshinone IIA inhibits breast cancer stem cells growth in vitro and in vivo through attenuation of IL-6/STAT3/NF-kB signaling pathways

Journal of Cellular Biochemistry

Volumn 114, Issue 9, 2013, Pages 2061-2070

  Lin, Caiyu ^a   Wang, Li ^a   Wang, Hong ^a   Yang, Liuqi ^a   Guo, Huijie ^a   Wang, Xiujie ^a  

^a SICHUAN UNIVERSITY   (China)

Author keywords

BREAST CANCER; CANCER STEM CELLS; GROWTH INHIBITION; IL 6 STAT3 NF kB SIGNALING PATHWAYS; TANSHINONE IIA

Indexed keywords

CD44V ANTIGEN; CYCLIN D1; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; STAT3 PROTEIN; TANSHINONE IIA;

ANTINEOPLASTIC ACTIVITY; ARTICLE; BREAST CANCER; CANCER INHIBITION; CANCER STEM CELL; CARCINOGENICITY; CELL PROLIFERATION; CELL STRAIN MCF 7; CELL STRUCTURE; CYTOKINE RELEASE; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TUMOR MICROENVIRONMENT; WESTERN BLOTTING;

EID: 84881383785     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.24553     Document Type: Article

References (52)

1. Aalaoui-Jamali M, Bijian K, Batist G,. 2011. Emerging drug discovery approaches for selective targeting of "precursor" metastatic breast cancer cells: Highlights and perspectives. Am J Transl Res 3: 434-444.
2. Ao A, Morrison BJ, Wang H, Lõpez JA, Reynolds BA, Lu J,. 2011. Response of estrogen receptor-positive breast cancer tumorspheres to antiestrogen treatments. PLoS ONE 6: e18810.
3. Chen SF, Chang YC, Nieh S, Liu CL, Yang CY, Lin YS,. 2012a. Nonadhesive culture system as a model of rapid sphere formation with cancer stem cell properties. PLoS ONE 7: e31864.
4. Chen W, Tang F, Xie B, Chen S, Huang H, Liu P,. 2012b. Amelioration of atherosclerosis by tanshinone IIA in hyperlipidemic rabbits through attenuation of oxidative stress. Eur J Pharmacol 674: 359-364.
5. Cioce M, Gherardi S, Viglietto G, Strano S, Blandino G, Muti P, Ciliberto G,. 2010. Mammosphere-forming cells from breast cancer cell lines as a tool for the identification of CSC-like- and early progenitor-targeting drugs. Cell Cycle 9: 2878-2887.
6. Fan GW, Gao XM, Wang H, Zhu Y, Zhang J, Hu LM, Su YF, Kang LY, Zhang BL,. 2009. The anti-inflammatory activities of tanshinone IIA, an active component of TCM, are mediated by estrogen receptor activation and inhibition of iNOS. J Steroid Biochem Mol Biol 113: 275-280.
7. Gong Y, Li Y, Abdolmaleky HM, Li L, Zhou JR,. 2012. Tanshinones inhibit the growth of breast cancer cells through epigenetic modification of Aurora A expression and function. PLoS ONE 7: e33656.
8. Guo Y, Xu F, Lu T, Duan Z, Zhang Z,. 2012. Interleukin-6 signaling pathway in targeted therapy for cancer. Cancer Treat Rev 38: 904-910.
9. Hafeez BB, Jamal MS, Fischer JW, Mustafa A, Verma AK,. 2012. Plumbagin, a plant derived natural agent inhibits the growth of pancreatic cancer cells in in vitro and in vivo via targeting EGFR, Stat3 and NF-κB signaling pathways. Int J Cancer 131: 2175-2186.
10. Hinohara K, Gotoh N,. 2010. Inflammatory signaling pathways in self-renewing breast cancer stem cells. Curr Opin Pharmacol 10: 650-654.
11. Hu Y, Fu L,. 2012. Targeting cancer stem cells: A new therapy to cure cancer patients. Am J Cancer Res 2: 340-356.
12. Iliopoulos D, Hirsch HA, Struhl K,. 2009. An epigenetic switch involving NF-kappaB, Lin28, Let-7 MicroRNA, and IL6 links inflammation to cell transformation. Cell 139: 693-706.
13. Iliopoulos D, Hirsch HA, Wang G, Struhl K,. 2011. Inducible formation of breast cancer stem cells and their dynamic equilibrium with non-stem cancer cells via IL6 secretion. Proc Natl Acad Sci USA 108: 1397-1402.
14. Jang SI, Jeong SI, Kim KJ, Kim HJ, Yu HH, Park R, Kim HM, You YO,. 2003. Tanshinone IIA from Salvia miltiorrhiza inhibits inducible nitric oxide synthase expression and production of TNF-alpha, IL-1beta and IL-6 in activated RAW 264.7 cells. Planta Med 69: 1057-1059.
15. Jiang XP, Yang DC, Elliott RL, Head JF,. 2011. Down-regulation of expression of interleukin-6 and its receptor results in growth inhibition of MCF-7 breast cancer cells. Anticancer Res 31: 2899-2906.
16. Kapoor S,. 2009. Tanshinone IIA: A potent, natural anti-carcinogenic agent for the management of systemic malignancies. Chin J Integr Med 15: 153.
17. Kim MJ, Kim YJ, Park HJ, Chung JH, Leem KH, Kim HK,. 2006. Apoptotic effect of red wine polyphenols on human colon cancer SNU-C4 cells. Food Chem Toxicol 44: 898-902.
18. Korkaya H, Liu S, Wicha MS,. 2011a. Breast cancer stem cells, cytokine networks, and the tumor microenvironment. J Clin Invest 121: 3804-3809.
19. Korkaya H, Liu S, Wicha MS,. 2011b. Regulation of cancer stem cells by cytokine networks: Attacking cancer's inflammatory roots. Clin Cancer Res 17: 6125-6129.
20. Leslie K, Gao SP, Berishaj M, Podsypanina K, Ho H, Ivashkiv L, Bromberg J,. 2010. Differential interleukin-6/Stat3 signaling as a function of cellular context mediates Ras-induced transformation. Breast Cancer Res 12: R80.
21. Li N, Grivennikov SI, Karin M,. 2011. The unholy trinity: Inflammation, cytokines, and STAT3 shape the cancer microenvironment. Cancer Cell 19: 429-431.
22. Liu M, Sakamaki T, Casimiro MC, Willmarth NE, Quong AA, Ju X, Ojeifo J, Jiao X, Yeow WS, Katiyar S, Shirley LA, Joyce D, Lisanti MP, Albanese C, Pestell RG,. 2010. The canonical NF-kappaB pathway governs mammary tumorigenesis in transgenic mice and tumor stem cell expansion. Cancer Res 70: 10464-10473.
23. - stem cell-like breast cancer cells in human tumors. J Clin Invest 121: 2723-2735.
24. Mather JP,. 2012. In vitro models. Stem Cells 30: 95-99.
25. Mitra AK, Faruque FS,. 2004. Breast cancer incidence and exposure to environmental chemicals in 82 counties in Mississippi. South Med J 97: 259-263.
26. Mitra I,. 2011. Breast cancer screening in developing countries. Prev Med 53: 121-122.
27. Murohashi M, Hinohara K, Kuroda M, Isagawa T, Tsuji S, Kobayashi S, Umezawa K, Tojo A, Aburatani H, Gotoh N,. 2010. Gene set enrichment analysis provides insight into novel signalling pathways in breast cancer stem cells. Br J Cancer 102: 206-212.
28. Omene CO, Wu J, Frenkel K,. 2012. Caffeic acid phenethyl ester (CAPE) derived from propolis, a honeybee product, inhibits growth of breast cancer stem cells. Invest New Drugs 30: 1279-1288.
29. Papi A, Guarnieri T, Storci G, Santini D, Ceccarelli C, Taffurelli M, De Carolis S, Avenia N, Sanguinetti A, Sidoni A, Orlandi M, Bonafé M,. 2012. Nuclear receptors agonists exert opposing effects on the inflammation dependent survival of breast cancer stem cells. Cell Death Differ 19: 1208-1219.
30. Ray RB, Raychoudhuri A, Steele R, Nerurkar P,. 2010. Bitter melon (Momordica charantia) extract inhibits breast cancer cell proliferation by modulating cell cycle regulatory genes and promotes apoptosis. Cancer Res 70: 1925-1931.
31. Ren ZH, Tong YH, Xu W, Ma J, Chen Y,. 2010. Tanshinone II A attenuates inflammatory responses of rats with myocardial infarction by reducing MCP-1 expression. Phytomedicine 17: 212-218.
32. Sansone P, Storci G, Tavolari S, Guarnieri T, Giovannini C, Taffurelli M, Ceccarelli C, Santini D, Paterini P, Marcu KB, Chieco P, Bonafè M,. 2007. IL-6 triggers malignant features in mammospheres from human ductal breast carcinoma and normal mammary gland. J Clin Invest 117: 3988-4002.
33. Shostak K, Chariot A,. 2011. NF-κB, stem cells and breast cancer: The links get stronger. Breast Cancer Res 13: 214.
34. Su CC, Chien SY, Kuo SJ, Chen YL, Cheng CY, Chen DR,. 2012. Tanshinone IIA inhibits human breast cancer MDA-MB-231 cells by decreasing LC3-II, Erb-B2 and NF-κBp65. Mol Med Rep 5: 1019-1022.
35. Su CC, Lin YH,. 2008. Tanshinone IIA inhibits human breast cancer cells through increased Bax to Bcl-xL ratios. Int J Mol Med 22: 357-361.
36. Sun S, Yin Y, Yin X, Cao F, Luo D, Zhang T, Li Y, Ni L,. 2012. Anti-nociceptive effects of Tanshinone IIA (TIIA) in a rat model of complete Freund's adjuvant (CFA)-induced inflammatory pain. Brain Res Bull 88: 581-588.
37. Tang C, Xue HL, Bai CL, Fu R,. 2011. Regulation of adhesion molecules expression in TNF-α-stimulated brain microvascular endothelial cells by tanshinone IIA: Involvement of NF-κB and ROS generation. Phytother Res 25: 376-380.
38. Tirino V, Desiderio V, Paino F, Papaccio G, De Rosa M,. 2012. Methods for cancer stem cell detection and isolation. Methods Mol Biol 879: 513-529.
39. Tsai CH, Lin FM, Yang YC, Lee MT, Cha TL, Wu GJ, Hsieh SC, Hsiao PW,. 2009. Herbal extract of Wedelia chinensis attenuates androgen receptor activity and orthotopic growth of prostate cancer in nude mice. Clin Cancer Res 15: 5435-5444.
40. van Meerloo J, Kaspers GJ, Cloos J,. 2011. Cell sensitivity assays: The MTT assay. Methods Mol Biol 731: 237-245.
41. Wang L, Zhang X, Liu L, Cui L, Yang R, Li M, Du W,. 2010. Tanshinone II A down-regulates HMGB1, RAGE, TLR4, NF-kappaB expression, ameliorates BBB permeability and endothelial cell function, and protects rat brains against focal ischemia. Brain Res 1321: 143-145.
42. Wang X, Wei Y, Yuan S, Liu G, Lu Y, Zhang J, Wang W,. 2005. Potential anticancer activity of tanshinone IIA against human breast cancer. Int J Cancer 116: 799-807.
43. Wu X, Liu L, Xie H, Liao J, Zhou X, Wan J, Yu K, Li J, Zhang Y,. 2012. Tanshinone IIA prevents uric acid nephropathy in rats through NF-κB inhibition. Planta Med 78: 866-873.
44. Xie G, Yao Q, Liu Y, Du S, Liu A, Guo Z, Sun A, Ruan J, Chen L, Ye C, Yuan Y,. 2012. IL-6-induced epithelial-mesenchymal transition promotes the generation of breast cancer stem-like cells analogous to mammosphere cultures. Int J Oncol 40: 1171-1179.
45. Xu S, Liu Z, Huang Y, Le K, Tang F, Huang H, Ogura S, Little PJ, Shen X, Liu P,. 2012. Tanshinone II-A inhibits oxidized LDL-induced LOX-1 expression in macrophages by reducing intracellular superoxide radical generation and NF-κB activation. Transl Res 160: 114-124.
46. Xu W, Lin H, Zhang Y, Chen X, Hua B, Hou W, Qi X, Pei Y, Zhu X, Zhao Z, Yang L,. 2011. Compound Kushen injection suppresses human breast cancer stem-like cells by down-regulating the canonical Wnt/β-catenin pathway. J Exp Clin Cancer Res 30: 103.
47. Yan MY, Chien SY, Kuo SJ, Chen DR, Su CC,. 2012. Tanshinone IIA inhibits BT-20 human breast cancer cell proliferation through increasing caspase 12, GADD153 and phospho-p38 protein expression. Int J Mol Med 29: 855-863.
48. Yin X, Yin Y, Cao FL, Chen YF, Peng Y, Hou WG, Sun SK, Luo ZJ,. 2012. Tanshinone IIA attenuates the inflammatory response and apoptosis after traumatic injury of the spinal cord in adult rats. PLoS ONE 7: e38381.
49. Yip NC, Fombon IS, Liu P, Brown S, Kannappan V, Armesilla AL, Xu B, Cassidy J, Darling JL, Wang W,. 2011. Disulfiram modulated ROS-MAPK and NFκB pathways and targeted breast cancer cells with cancer stem cell-like properties. Br J Cancer 104: 1564-1574.
50. Yoon S, Woo SU, Kang JH, Kim K, Shin HJ, Gwak HS, Park S, Chwae YJ,. 2012. NF-κB and STAT3 cooperatively induce IL6 in starved cancer cells. Oncogene 31: 3467-3481.
51. Zhou J, Wulfkuhle J, Zhang H, Gu P, Yang Y, Deng J, Margolick JB, Liotta LA, Petricoin E III, Zhang Y,. 2007. Activation of the PTEN/mTOR/STAT3 pathway in breast cancer stem-like cells is required for viability and maintenance. Proc Natl Acad Sci USA 104: 16158-16163.
52. Zhu C, Cheng KW, Ouyang N, Huang L, Sun Y, Constantinides P, Rigas B,. 2012. Phosphosulindac (OXT-328) selectively targets breast cancer stem cells in vitro and in human breast cancer xenografts. Stem Cells 30: 2065-2075.