Luteolin sensitises drug-resistant human breast cancer cells to tamoxifen via the inhibition of cyclin E2 expression

Food Chemistry

Volumn 141, Issue 2, 2013, Pages 1553-1561

  Tu, Shih Hsin ^a,b   Ho, Chi Tang ^c   Liu, Ming Fang ^a   Huang, Ching Shui ^a,b   Chang, Hui Wen ^d   Chang, Chien Hsi ^d   Wu, Chih Hsiung ^a,e   Ho, Yuan Soon ^a,d  

^a TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^b CATHAY GENERAL HOSPITAL   (Taiwan)

^c RUTGERS UNIVERSITY   (United States)

^d TAIPEI MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^e TAIPEI MEDICAL UNIVERSITY   (Taiwan)

Author keywords

Breast cancer; Cell cycle; Cyclin E2; Luteolin; Tamoxifen

Indexed keywords

CYTOLOGY; DISEASES; FLAVONOIDS; POLYMERASE CHAIN REACTION; PROTEINS; TISSUE;

BREAST CANCER; CELL CYCLE; CYCLIN E2; LUTEOLIN; TAMOXIFEN;

CELLS;

CYCLINE; LUTEOLIN; MESSENGER RNA; TAMOXIFEN;

ARTICLE; BREAST CANCER; CANCER CELL; CANCER INHIBITION; CANCER PATIENT; HUMAN; HUMAN CELL; MAJOR CLINICAL STUDY; PROTEIN ANALYSIS; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR CELL;

EID: 84878381514     PISSN: 03088146     EISSN: 18737072     Source Type: Journal    
DOI: 10.1016/j.foodchem.2013.04.077     Document Type: Article

References (51)

1. Akli, S., Zheng, P. J., Multani, A. S., Wingate, H. F., Pathak, S., Zhang, N., et al. (2004). Tumour-specific low molecular weight forms of cyclin E induce genomic instability and resistance (Pubitemid 38581423)
2. Amin, A. R., Wang, D., Zhang, H., Peng, S., Shin, H. J., Brandes, J. C., et al. (2010). Enhanced anti-tumour activity by the combination of the natural compounds (-)-epigallocatechin-3-gallate and luteolin: Potential role of p53. The Journal of Biological Chemistry, 285(45), 34557-34565.
3. Bagli, E., Stefaniotou, M., Morbidelli, L., Ziche, M., Psillas, K., Murphy, C., et al. (2004). Luteolin inhibits vascular endothelial growth factor-induced angiogenesis; inhibition of endothelial cell survival and proliferation by targeting phosphatidylinositol 30-kinase activity. Cancer Research, 64(21), 7936-7946. (Pubitemid 39446927)
4. Bai, L., Xu, X., Wang, Q., Xu, S., Ju, W., Wang, X., et al. (2012). A superoxide-mediated mitogen-activated protein kinase phosphatase-1 degradation and c-Jun NH(2)- terminal kinase activation pathway for luteolin-induced lung cancer cytotoxicity. Molecular Pharmacology, 81(4), 549-555.
5. Baskar, A. A., Ignacimuthu, S., Michael, G. P., & Al Numair, K. S. (2011). Cancer chemopreventive potential of luteolin-7-O-glucoside isolated from Ophiorrhiza mungos Linn. Nutrition and Cancer, 63(1), 130-138.
6. Bortner, D. M., & Rosenberg, M. P. (1997). Induction of mammary gland hyperplasia and carcinomas in transgenic mice expressing human cyclin E. Molecular and Cellular Biology, 17(1), 453-459. (Pubitemid 26425635)
7. Butt, A. J., Caldon, C. E., McNeil, C. M., Swarbrick, A., Musgrove, E. A., & Sutherland, R. L. (2008). Cell cycle machinery: Links with genesis and treatment of breast cancer. Advances in Experimental Medicine and Biology, 630, 189-205.
8. Byun, S., Lee, K. W., Jung, S. K., Lee, E. J., Hwang, M. K., Lim, S. H., et al. (2010). Luteolin inhibits protein kinase C(epsilon) and c-Src activities and UVB-induced skin cancer. Cancer Research, 70(6), 2415-2423.
9. Caldon, C. E., Sergio, C. M., Kang, J., Muthukaruppan, A., Boersma, M. N., Stone, A., et al. (2012). Cyclin E2 overexpression is associated with endocrine resistance but not insensitivity to CDK2 inhibition in human breast cancer cells. Molecular Cancer Therapeutics, 11(7), 1488-1499.
10. Caldon, C. E., Sergio, C. M., Schutte, J., Boersma, M. N., Sutherland, R. L., Carroll, J. S., et al. (2009). Estrogen regulation of cyclin E2 requires cyclin D1 but not c-Myc. Molecular and Cellular Biology, 29(17), 4623-4639.
11. Chen, L. C., Liu, Y. C., Liang, Y. C., Ho, Y. S., & Lee, W. S. (2009). Magnolol inhibits human glioblastoma cell proliferation through upregulation of p21/Cip1. Journal of Agricultural and Food Chemistry, 57(16), 7331-7337.
12. Chiang, C. T., Way, T. D., & Lin, J. K. (2007). Sensitising HER2-overexpressing cancer cells to luteolin-induced apoptosis through suppressing p21(WAF1/CIP1) expression with rapamycin. Molecular Cancer Therapeutics, 6(7), 2127-2138.
13. Chiu, F. L., & Lin, J. K. (2008). Downregulation of androgen receptor expression by luteolin causes inhibition of cell proliferation and induction of apoptosis in human prostate cancer cells and xenografts. The Prostate, 68(1), 61-71.
14. Coser, K. R., Chesnes, J., Hur, J., Ray, S., Isselbacher, K. J., & Shioda, T. (2003). Global analysis of ligand sensitivity of estrogen inducible and suppressible genes in MCF7/BUS breast cancer cells by DNA microarray. Proceedings of the National Academy of Sciences of the United States of America, 100(24), 13994-13999. (Pubitemid 37499179)
15. DeFriend, D. J., Howell, A., Nicholson, R. I., Anderson, E., Dowsett, M., Mansel, R. E., et al. (1994). Investigation of a new pure antiestrogen (ICI 182780) in women with primary breast cancer. Cancer Research, 54(2), 408-414. (Pubitemid 24053178)
16. Desmedt, C., Ouriaghli, F. E., Durbecq, V., Soree, A., Colozza, M. A., Azambuja, E., et al. (2006). Impact of cyclins E, neutrophil elastase and proteinase 3 expression levels on clinical outcome in primary breast cancer patients. International Journal of Cancer (Journal International du Cancer), 119(11), 2539-2545. (Pubitemid 44691306)
17. Dhillon, N. K., & Mudryj, M. (2002). Ectopic expression of cyclin E in estrogen responsive cells abrogates antiestrogen mediated growth arrest. Oncogene, 21(30), 4626-4634. (Pubitemid 34833140)
18. Du, G. J., Song, Z. H., Lin, H. H., Han, X. F., Zhang, S., & Yang, Y. M. (2008). Luteolin as a glycolysis inhibitor offers superior efficacy and lesser toxicity of doxorubicin in breast cancer cells. Biochemical and Biophysical Research Communications, 372(3), 497-502.
19. Fan, P., Wang, J., Santen, R. J., & Yue, W. (2007). Long-term treatment with tamoxifen facilitates translocation of estrogen receptor alpha out of the nucleus and enhances its interaction with EGFR in MCF-7 breast cancer cells. Cancer Research, 67(3), 1352-1360.
20. Gudas, J. M., Payton, M., Thukral, S., Chen, E., Bass, M., Robinson, M. O., et al. (1999). Cyclin E2, a novel G1 cyclin that binds Cdk2 and is aberrantly expressed in human cancers. Molecular and Cellular Biology, 19(1), 612-622. (Pubitemid 29018463)
21. Han, D. H., Denison, M. S., Tachibana, H., & Yamada, K. (2002). Relationship between estrogen receptor-binding and estrogenic activities of environmental estrogens and suppression by flavonoids. Bioscience, Biotechnology, and Biochemistry, 66(7), 1479-1487. (Pubitemid 39246853)
22. Han, D., Tachibana, H., & Yamada, K. (2001). Inhibition of environmental estrogeninduced proliferation of human breast carcinoma MCF-7 cells by flavonoids. In Vitro Cellular & Developmental Biology - Animal, 37(5), 275-282. (Pubitemid 32751427)
23. Huang, L., Zhao, S., Frasor, J. M., & Dai, Y. (2011). An integrated bioinformatics approach identifies elevated cyclin E2 expression and E2F activity as distinct features of tamoxifen resistant breast tumours. PLoS One, 6(7), e22274.
24. Jeon, Y. W., & Suh, Y. J. (2013). Synergistic apoptotic effect of celecoxib and luteolin on breast cancer cells. Oncology Reports, 29(2), 819-825.
25. Katzenellenbogen, B. S., Miller, M. A., Mullick, A., & Sheen, Y. Y. (1985). Antiestrogen action in breast cancer cells: Modulation of proliferation and protein synthesis, and interaction with estrogen receptors and additional antiestrogen binding sites. Breast Cancer Research and Treatment, 5(3), 231-243. (Pubitemid 15054666)
26. Lee, E. J., Oh, S. Y., & Sung, M. K. (2012). Luteolin exerts anti-tumour activity through the suppression of epidermal growth factor receptor-mediated pathway in MDA-MB-231 ER-negative breast cancer cells. Food and Chemical Toxicology: An International Journal Published for the British Industrial Biological Research Association, 50(11), 4136-4143.
27. Lim do, Y., Cho, H. J., Kim, J., Nho, C. W., Lee, K. W., & Park, J. H. (2012). Luteolin decreases IGF-II production and downregulates insulin-like growth factor-I receptor signalling in HT-29 human colon cancer cells. BMC Gastroenterology, 12, 9.
28. Lin, Y. S., Tsai, P. H., Kandaswami, C. C., Cheng, C. H., Ke, F. C., Lee, P. P., et al. (2011). Effects of dietary flavonoids, luteolin, and quercetin on the reversal of epithelial-mesenchymal transition in A431 epidermal cancer cells. Cancer Science, 102(10), 1829-1839.
29. Markaverich, B. M., Shoulars, K., & Rodriguez, M. A. (2011). Luteolin regulation of estrogen signalling and cell cycle pathway genes in MCF-7 human breast cancer cells. International Journal of Biomedical Science: IJBS, 7(2), 101-111.
30. Musgrove, E. A., Sergio, C. M., Loi, S., Inman, C. K., Anderson, L. R., Alles, M. C., et al. (2008). Identification of functional networks of estrogen- and c-Myc-responsive genes and their relationship to response to tamoxifen therapy in breast cancer. PLoS One, 3(8), e2987.
31. Pan, M. H., Huang, M. C., Wang, Y. J., Lin, J. K., & Lin, C. H. (2003). Induction of apoptosis by hydroxydibenzoylmethane through coordinative modulation of cyclin D3, Bcl-X(L), and Bax, release of cytochrome c, and sequential activation of caspases in human colorectal carcinoma cells. Journal of Agricultural and Food Chemistry, 51(14), 3977-3984.
32. Pratheeshkumar, P., Son, Y. O., Budhraja, A., Wang, X., Ding, S., Wang, L., et al. (2012). Luteolin inhibits human prostate tumour growth by suppressing vascular endothelial growth factor receptor 2-mediated angiogenesis. PLoS One, 7(12), e52279.
33. Rao, P. S., Satelli, A., Moridani, M., Jenkins, M., & Rao, U. S. (2012). Luteolin induces apoptosis in multidrug resistant cancer cells without affecting the drug transporter function: Involvement of cell line-specific apoptotic mechanisms. International Journal of Cancer (Journal International du Cancer), 130(11), 2703-2714.
34. Ruan, J., Zhang, L., Yan, L., Liu, Y., Yue, Z., Chen, L., et al. (2012). Inhibition of hypoxiainduced epithelial-mesenchymal transition by luteolin in non-small cell lung cancer cells. Molecular Medicine Reports, 6(1), 232-238.
35. Shi, R., Huang, Q., Zhu, X., Ong, Y. B., Zhao, B., Lu, J., et al. (2007). Luteolin sensitises the anticancer effect of cisplatin via c-Jun NH2-terminal kinase-mediated p53 phosphorylation and stabilization. Molecular Cancer Therapeutics, 6(4), 1338-1347. (Pubitemid 46711997)
36. Shih, Y. L., Liu, H. C., Chen, C. S., Hsu, C. H., Pan, M. H., Chang, H. W., et al. (2010). Combination treatment with luteolin and quercetin enhances antiproliferative effects in nicotine-treated MDA-MB-231 cells by down-regulating nicotinic acetylcholine receptors. Journal of Agricultural and Food Chemistry, 58(1), 235-241.
37. Shoulars, K., Rodriguez, M. A., Thompson, T., & Markaverich, B. M. (2010). Regulation of cell cycle and RNA transcription genes identified by microarray analysis of PC-3 human prostate cancer cells treated with luteolin. The Journal of Steroid Biochemistry and Molecular Biology, 118(1-2), 41-50.
38. Sieuwerts, A. M., Look, M. P., Meijer-van Gelder, M. E., Timmermans, M., Trapman, A. M., Garcia, R. R., et al. (2006). Which cyclin E prevails as prognostic marker for breast cancer? Results from a retrospective study involving 635 lymph nodenegative breast cancer patients. Clinical Cancer Research: An Official Journal of the American Association for Cancer Research, 12(11 Pt 1), 3319-3328.
39. Tam, K. W., Ho, C. T., Lee, W. J., Tu, S. H., Huang, C. S., Chen, C. S., et al. (2013). Alteration of alpha-tocopherol-associated protein (TAP) expression in human breast epithelial cells during breast cancer development. Food Chemistry, 138(2-3), 1015-1021.
40. Taneja, P., Maglic, D., Kai, F., Zhu, S., Kendig, R. D., Fry, E. A., et al. (2010). Classical and novel prognostic markers for breast cancer and their clinical significance. Clinical Medicine Insights - Oncology, 4, 15-34.
41. Tang, X., Wang, H., Fan, L., Wu, X., Xin, A., Ren, H., et al. (2011). Luteolin inhibits Nrf2 leading to negative regulation of the Nrf2/ARE pathway and sensitisation of human lung carcinoma A549 cells to therapeutic drugs. Free Radical Biology & Medicine, 50(11), 1599-1609.
42. Tsui, K. H., Chung, L. C., Feng, T. H., Chang, P. L., & Juang, H. H. (2012). Upregulation of prostate-derived Ets factor by luteolin causes inhibition of cell proliferation and cell invasion in prostate carcinoma cells. International Journal of Cancer. Journal International du Cancer, 130(12), 2812-2823.
43. Tu, S. H., Chang, C. C., Chen, C. S., Tam, K. W., Wang, Y. J., Lee, C. H., et al. (2010). Increased expression of enolase alpha in human breast cancer confers tamoxifen resistance in human breast cancer cells. Breast Cancer Research and Treatment, 121(3), 539-553.
44. Tu, S. H., Chang, C. C., Chen, C. S., Tam, K. W., Wang, Y. J., Lee, C. H., et al. (2010). Increased expression of enolase alpha in human breast cancer confers tamoxifen resistance in human breast cancer cells. Breast Cancer Research and Treatment, 121(3), 539-553.
45. Varma, H., Skildum, A. J., & Conrad, S. E. (2007). Functional ablation of pRb activates Cdk2 and causes antiestrogen resistance in human breast cancer cells. PLoS One, 2(12), e1256.
46. Wang, L. M., Xie, K. P., Huo, H. N., Shang, F., Zou, W., & Xie, M. J. (2012). Luteolin inhibits proliferation induced by IGF-1 pathway dependent ERalpha in human breast cancer MCF-7 cells. Asian Pacific Journal of Cancer Prevention: APJCP, 13(4), 1431-1437.
47. Xavier, C. P., Lima, C. F., Rohde, M., & Pereira-Wilson, C. (2011). Quercetin enhances 5-fluorouracil-induced apoptosis in MSI colorectal cancer cells through p53 modulation. Cancer Chemotherapy and Pharmacology, 68(6), 1449-1457.
48. Xie, F., Lang, Q., Zhou, M., Zhang, H., Zhang, Z., Zhang, Y., et al. (2012). The dietary flavonoid luteolin inhibits Aurora B kinase activity and blocks proliferation of cancer cells. European Journal of Pharmaceutical Sciences: Official Journal of the European Federation for Pharmaceutical Sciences, 46(5), 388-396.
49. Yan, J., Wang, Q., Zheng, X., Sun, H., Zhou, Y., Li, D., et al. (2012). Luteolin enhances TNF-related apoptosis-inducing ligand's anticancer activity in a lung cancer xenograft mouse model. Biochemical and Biophysical Research Communications, 417(2), 842-846.
50. Zhao, Y., Yang, G., Ren, D., Zhang, X., Yin, Q., & Sun, X. (2011). Luteolin suppresses growth and migration of human lung cancer cells. Molecular Biology Reports, 38(2), 1115-1119.
51. Zhou, Q., Yan, B., Hu, X., Li, X. B., Zhang, J., & Fang, J. (2009). Luteolin inhibits invasion of prostate cancer PC3 cells through E-cadherin. Molecular Cancer Therapeutics, 8(6), 1684-1691.