Tectorigenin sensitizes paclitaxel-resistant human ovarian cancer cells through downregulation of the Akt and NFκB pathway

Carcinogenesis

Volumn 33, Issue 12, 2012, Pages 2488-2498

  Yang, Yeong In ^a   Lee, Kyung Tae ^a   Park, Hee Juhn ^b   Kim, Tae Jin ^c   Choi, Youn Seok ^d   Shih, Ie Ming ^e   Choi, Jung Hye ^a  

^a Kyung Hee University   (South Korea)

^b Sangji University   (South Korea)

^c Kwandong University College of Medicine   (South Korea)

^d Catholic University of Daegu   (South Korea)

^e DEPARTMENT OF PATHOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; CASPASE 3; CASPASE 8; CASPASE 9; CYCLOOXYGENASE 2; FLICE INHIBITORY PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PACLITAXEL; PROTEIN BCL 2; PROTEIN BCL XL; PROTEIN KINASE B; TECTORIGENIN; X LINKED INHIBITOR OF APOPTOSIS;

APOPTOSIS; ARTICLE; CANCER CELL; CANCER GROWTH; CANCER INHIBITION; CANCER RESISTANCE; ENZYME ACTIVATION; FEMALE; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; INTRACELLULAR SIGNALING; OVARY CANCER; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RECEPTOR DOWN REGULATION;

ANTINEOPLASTIC AGENTS, PHYTOGENIC; APOPTOSIS; CELL LINE, TUMOR; DOWN-REGULATION; DRUG RESISTANCE, NEOPLASM; DRUG SYNERGISM; FEMALE; HUMANS; ISOFLAVONES; NF-KAPPA B; OVARIAN NEOPLASMS; PACLITAXEL; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTORS, ESTROGEN; SIGNAL TRANSDUCTION;

EID: 84870372396     PISSN: 01433334     EISSN: 14602180     Source Type: Journal    
DOI: 10.1093/carcin/bgs302     Document Type: Article

References (84)

1. Parkin, D.M. et al. (2005) Global cancer statistics, 2002. CA. Cancer J. Clin., 55, 74-108.
2. Conte, P.F. et al. (1999) Up date in the management of advanced ovarian carcinoma. Crit. Rev. Oncol. Hematol., 32, 49-58.
3. Omura, G.A. et al. (1991) Long-term follow-up and prognostic factor analysis in advanced ovarian carcinoma: the Gynecologic Oncology Group experience. J. Clin. Oncol., 9, 1138-1150.
4. Agarwal, R. et al. (2003) Ovarian cancer: strategies for overcoming resistance to chemotherapy. Nat. Rev. Cancer, 3, 502-516.
5. Zunino, F. et al. (1997) Role of apoptotic response in cellular resistance to cytotoxic agents. Pharmacol. Ther., 76, 177-185.
6. Arts, H.J. et al. (2000) Options for modulation of drug resistance in ovarian cancer. Int. J. Gynecol. Cancer, 10(S1), 47-52.
7. Eliopoulos, A.G. et al. (1995) The control of apoptosis and drug resistance in ovarian cancer: influence of p53 and Bcl-2. Oncogene, 11, 1217-1228.
8. Herod, J.J. et al. (1996) The prognostic significance of Bcl-2 and p53 expression in ovarian carcinoma. Cancer Res., 56, 2178-2184.
9. Ling, X. et al. (2004) Induction of survivin expression by taxol (paclitaxel) is an early event, which is independent of taxol-mediated G2/M arrest. J. Biol. Chem., 279, 15196-15203.
10. Sasaki, H. et al. (2000) Down-regulation of X-linked inhibitor of apoptosis protein induces apoptosis in chemoresistant human ovarian cancer cells. Cancer Res., 60, 5659-5666.
11. Kirchhoff, S. et al. (2000) TCR-mediated up-regulation of c-FLIPshort correlates with resistance toward CD95-mediated apoptosis by blocking death-inducing signaling complex activity. J. Immunol., 165, 6293-6300.
12. Krueger, A. et al. (2001) Cellular FLICE-inhibitory protein splice variants inhibit different steps of caspase-8 activation at the CD95 death-inducing signaling complex. J. Biol. Chem., 276, 20633-20640.
13. Havsteen, B. (1983) Flavonoids, a class of natural products of high pharmacological potency. Biochem. Pharmacol., 32, 1141-1148.
14. Nishiumi, S. et al. (2011) Dietary flavonoids as cancer-preventive and therapeutic biofactors. Front. Biosci. (Schol. Ed)., 3, 1332-1362.
15. Shen, F. et al. (1997) Synergistic action of quercetin and genistein in human ovarian carcinoma cells. Oncol. Res., 9, 597-602.
16. Chen, M.H. et al. (2007) The proportional odds model for multivariate interval-censored failure time data. Stat. Med., 26, 5147-5161.
17. Tanaka, T. et al. (2002) Inhibitory effects of estrogenic compounds, 4-nonylphenol and genistein, on 7, 12-dimethylbenz[a]anthracene-induced ovarian carcinogenesis in rats. Ecotoxicol. Environ. Saf., 52, 38-45.
18. Klein, A. et al. (2006) Prolonged stabilization of platinum-resistant ovarian cancer in a single patient consuming a fermented soy therapy. Gynecol. Oncol., 100, 205-209.
19. McCann, S.E. et al. (2003) Risk of human ovarian cancer is related to dietary intake of selected nutrients, phytochemicals and food groups. J. Nutr., 133, 1937-1942.
20. Ouyang, G. et al. (2009) Genistein induces G2/M cell cycle arrest and apoptosis of human ovarian cancer cells via activation of DNA damage checkpoint pathways. Cell Biol. Int., 33, 1237-1244.
21. Thasni, K.A. et al. (2008) Genistein induces apoptosis in ovarian cancer cells via different molecular pathways depending on Breast Cancer Susceptibility gene-1 (BRCA1) status. Eur. J. Pharmacol., 588, 158-164.
22. Choi, E.J. et al. (2007) Pro-apoptotic effect and cytotoxicity of genistein and genistin in human ovarian cancer SK-OV-3 cells. Life Sci., 80, 1403-1408.
23. Gossner, G. et al. (2007) Genistein-induced apoptosis and autophagocytosis in ovarian cancer cells. Gynecol. Oncol., 105, 23-30.
24. Solomon, L.A. et al. (2008) Sensitization of ovarian cancer cells to cisplatin by genistein: the role of NF-kappaB. J. Ovarian Res., 1, 9.
25. Papazisis, K.T. et al. (2006) Synergistic effects of protein tyrosine kinase inhibitor genistein with camptothecins against three cell lines in vitro. Cancer Lett., 233, 255-264.
26. Silasi, D.A. et al. (2009) Phenoxodiol: pharmacology and clinical experience in cancer monotherapy and in combination with chemotherapeutic drugs. Expert Opin. Pharmacother., 10, 1059-1067.
27. Shin, J.E. et al. (2006) Estrogenic effect of main components kakkalide and tectoridin of Puerariae Flos and their metabolites. Biol. Pharm. Bull., 29, 1202-1206.
28. Pan, C.H. et al. (2008) Tectorigenin inhibits IFN-gamma/LPS-induced inflammatory responses in murine macrophage RAW 264.7 cells. Arch. Pharm. Res., 31, 1447-1456.
29. Kim, Y.P. et al. (1999) Inhibition by tectorigenin and tectoridin of prostaglandin E2 production and cyclooxygenase-2 induction in rat peritoneal macrophages. Biochim. Biophys. Acta, 1438, 399-407.
30. Morrissey, C. et al. (2004) Phytoestrogens derived from Belamcanda chinensis have an antiproliferative effect on prostate cancer cells in vitro. J. Urol., 172(6 Pt 1), 2426-2433.
31. Thelen, P. et al. (2005) Tectorigenin and other phytochemicals extracted from leopard lily Belamcanda chinensis affect new and established targets for therapies in prostate cancer. Carcinogenesis, 26, 1360-1367.
32. Kang, S.C. et al. (2006) Evaluation of oriental medicinal herbs for estrogenic and antiproliferative activities. Phytother. Res., 20, 1017-1019.
33. Umehara, K. et al. (2009) Flavonoids from the heartwood of the Thai medicinal plant Dalbergia parviflora and their effects on estrogenic-responsive human breast cancer cells. J. Nat. Prod., 72, 2163-2168.
34. Park, H.-J. et al. (1999) Isoflavone glycosides from the flowers of Pueraria thunbergiana. Phytochemistry, 51, 147-151.
35. Pohl, G. et al. (2005) Inactivation of the mitogen-activated protein kinase pathway as a potential target-based therapy in ovarian serous tumors with KRAS or BRAF mutations. Cancer Res., 65, 1994-2000.
36. Choi, J.H. et al. (2009) Functional analysis of 11q13.5 amplicon identifies Rsf-1 (HBXAP) as a gene involved in paclitaxel resistance in ovarian cancer. Cancer Res., 69, 1407-1415.
37. Choi, J.H. et al. (2004) Overexpression of follicle-stimulating hormone receptor activates oncogenic pathways in preneoplastic ovarian surface epithelial cells. J. Clin. Endocrinol. Metab., 89, 5508-5516.
38. Lee, K.T. et al. (2001) Tectorigenin, an isoflavone of Pueraria thunbergiana Benth., induces differentiation and apoptosis in human promyelocytic leukemia HL-60 cells. Biol. Pharm. Bull., 24, 1117-1121.
39. Chou, T.C. et al. (1984) Quantitative analysis of dose-effect relationships: the combined effects of multiple drugs or enzyme inhibitors. Adv. Enzyme Regul., 22, 27-55.
40. Prasad, S. et al. (2010) Targeting inflammatory pathways by flavonoids for prevention and treatment of cancer. Planta Med., 76, 1044-1063.
41. Chen, S.S. et al. (2012) Advances in the treatment of ovarian cancer: a potential role of antiinflammatory phytochemicals. Discov. Med., 13, 7-17.
42. Nakanishi, C. et al. (2005) Nuclear factor-kappaB inhibitors as sensitizers to anticancer drugs. Nat. Rev. Cancer, 5, 297-309.
43. Kim, S.H. et al. (2007) Akt involvement in paclitaxel chemoresistance of human ovarian cancer cells. Ann. N. Y. Acad. Sci., 1095, 82-89.
44. Bava, S.V. et al. (2005) Sensitization of taxol-induced apoptosis by curcumin involves down-regulation of nuclear factor-kappaB and the serine/ threonine kinase Akt and is independent of tubulin polymerization. J. Biol. Chem., 280, 6301-6308.
45. Goel, A. et al. (2010) Curcumin, the golden spice from Indian saffron, is a chemosensitizer and radiosensitizer for tumors and chemoprotector and radioprotector for normal organs. Nutr. Cancer, 62, 919-930.
46. Sreekanth, C.N. et al. (2011) Molecular evidences for the chemosensitizing efficacy of liposomal curcumin in paclitaxel chemotherapy in mouse models of cervical cancer. Oncogene, 30, 3139-3152.
47. Matsui, Y. et al. (2008) Cancer-specific enhancement of cisplatin-induced cytotoxicity with triptolide through an interaction of inactivated glycogen synthase kinase-3beta with p53. Oncogene, 27, 4603-4614.
48. Westfall, S.D. et al. (2008) Role of triptolide as an adjunct chemotherapy for ovarian cancer. Chemotherapy, 54, 67-76.
49. Fidler, J.M. et al. (2003) PG490-88, a derivative of triptolide, causes tumor regression and sensitizes tumors to chemotherapy. Mol. Cancer Ther., 2, 855-862.
50. Chang, W.T. et al. (2001) Triptolide and chemotherapy cooperate in tumor cell apoptosis. A role for the p53 pathway. J. Biol. Chem., 276, 2221-2227.
51. Park, B. et al. (2011) Triptolide, histone acetyltransferase inhibitor, suppresses growth and chemosensitizes leukemic cells through inhibition of gene expression regulated by TNF-TNFR1-TRADD-TRAF2-NIK-TAK1-IKK pathway. Biochem. Pharmacol., 82, 1134-1144.
52. Arafa, S.A. et al. (2009) Tangeretin sensitizes cisplatin-resistant human ovarian cancer cells through downregulation of phosphoinositide 3-kinase/Akt signaling pathway. Cancer Res., 69, 8910-8917.
53. Kelly, M.G. et al. (2011) Phase II evaluation of phenoxodiol in combination with cisplatin or paclitaxel in women with platinum/taxane-refractory/resistant epithelial ovarian, fallopian tube, or primary peritoneal cancers. Int. J. Gynecol. Cancer, 21, 633-639.
54. Fang, R. et al. (2008) Cytotoxic effects of compounds from Iris tectorum on human cancer cell lines. J. Ethnopharmacol., 118, 257-263.
55. Thelen, P. et al. (2007) Phytoestrogens from Belamcanda chinensis regulate the expression of steroid receptors and related cofactors in LNCaP prostate cancer cells. BJU Int., 100, 199-203.
56. Zhao, E. et al. (2011) Phytoestrogen biological actions on Mammalian reproductive system and cancer growth. Sci. Pharm., 79, 1-20.
57. Risch, H.A. (1998) Hormonal etiology of epithelial ovarian cancer, with a hypothesis concerning the role of androgens and progesterone. J. Natl. Cancer Inst., 90, 1774-1786.
58. Vierikko, P. et al. (1983) Cytosol and nuclear estrogen and progestin receptors and 17 beta-hydroxysteroid dehydrogenase activity in non-diseased tissue and in benign and malignant tumors of the human ovary. Int. J. Cancer, 32, 413-422.
59. Willcocks, D. et al. (1983) Estrogen and progesterone receptors in human ovarian tumors. Gynecol. Oncol., 16, 246-253.
60. Rao, B.R. et al. (1991) Endocrine factors in common epithelial ovarian cancer. Endocr. Rev., 12, 14-26.
61. Klaunig, J.E. et al. (2004) The role of oxidative stress in carcinogenesis. Annu. Rev. Pharmacol. Toxicol., 44, 239-267.
62. Brandenberger, A.W. et al. (1998) Estrogen receptor alpha (ER-alpha) and beta (ER-beta) mRNAs in normal ovary, ovarian serous cystadenocarcinoma and ovarian cancer cell lines: down-regulation of ER-beta in neoplastic tissues. J. Clin. Endocrinol. Metab., 83, 1025-1028.
63. Pujol, P. et al. (1998) Differential expression of estrogen receptor-alpha and -beta messenger RNAs as a potential marker of ovarian carcinogenesis. Cancer Res., 58, 5367-5373.
64. Rutherford, T. et al. (2000) Absence of estrogen receptor-beta expression in metastatic ovarian cancer. Obstet. Gynecol., 96, 417-421.
65. Chien, C.H. et al. (1994) Transcriptional activation of c-myc proto-oncogene by estrogen in human ovarian cancer cells. Mol. Cell. Endocrinol., 99, 11-19.
66. Galtier, M. et al. (1992) Beta blockade prophylaxis of accessory pathway catecholamine sensitive circus movement tachycardia. Eur. J. Med., 1, 125-126.
67. Ercoli, A. et al. (2000) Activity of cisplatin and ICI 182, 780 on estrogen receptor negative ovarian cancer cells: cell cycle and cell replication rate perturbation, chromatin texture alteration and apoptosis induction. Int. J. Cancer, 85, 98-103.
68. Lau, K.M. et al. (1999) Expression of human estrogen receptor-alpha and -beta, progesterone receptor, and androgen receptor mRNA in normal and malignant ovarian epithelial cells. Proc. Natl. Acad. Sci. U.S.A., 96, 5722-5727.
69. Brandenberger, A.W. et al. (1998) Estrogen receptor alpha (ER-alpha) and beta (ER-beta) mRNAs in normal ovary, ovarian serous cystadenocarcinoma and ovarian cancer cell lines: down-regulation of ER-beta in neoplastic tissues. J. Clin. Endocrinol. Metab., 83, 1025-1028.
70. Choi, J.H. et al. (2005) Expression of leptin receptors and potential effects of leptin on the cell growth and activation of mitogen-activated protein kinases in ovarian cancer cells. J. Clin. Endocrinol. Metab., 90, 207-210.
71. Mabuchi, S. et al. (2004) Inhibition of inhibitor of nuclear factor-kappaB phosphorylation increases the efficacy of paclitaxel in in vitro and in vivo ovarian cancer models. Clin. Cancer Res., 10, 7645-7654.
72. Fraser, M. et al. (2003) Chemoresistance in human ovarian cancer: the role of apoptotic regulators. Reprod. Biol. Endocrinol., 1, 66.
73. Huang, Y. et al. (2002) IkappaB kinase activation is involved in regulation of paclitaxel-induced apoptosis in human tumor cell lines. Mol. Pharmacol., 61, 105-113.
74. Hu, L. et al. (2002) Inhibition of phosphatidylinositol 3'-kinase increases efficacy of paclitaxel in in vitro and in vivo ovarian cancer models. Cancer Res., 62, 1087-1092.
75. Liu, G.H. et al. (2006) Inhibition of nuclear factor-kappaB by an antioxidant enhances paclitaxel sensitivity in ovarian carcinoma cell line. Int. J. Gynecol. Cancer, 16, 1777-1782.
76. DiDonato, J.A. et al. (1997) A cytokine-responsive IkappaB kinase that activates the transcription factor NF-kappaB. Nature, 388, 548-554.
77. Huxford, T. et al. (1999) Structure and mechanism in NF-kappa B/I kappa B signaling. Cold Spring Harbor Symposia on Quantitative Biology, 64, 533-540.
78. Baldwin, A.S. Jr. (1996) The NF-kappa B and I kappa B proteins: new discoveries and insights. Annu. Rev. Immunol., 14, 649-683.
79. Hernandez, L. et al. (2010) Activation of NF-kappaB signaling by inhibitor of NF-kappaB kinase beta increases aggressiveness of ovarian cancer. Cancer Res., 70, 4005-4014.
80. Darb-Esfahani, S. et al. (2010) Expression of classical NF-kappaB pathway effectors in human ovarian carcinoma. Histopathology, 56, 727-739.
81. Annunziata, C.M. et al. (2010) Nuclear factor kappaB transcription factors are coexpressed and convey a poor outcome in ovarian cancer. Cancer, 116, 3276-3284.
82. Do, P.M. et al. (2012) Mutant p53 cooperates with ETS2 to promote etoposide resistance. Genes Dev., 26, 830-845.
83. Brader, S. et al. (2004) Phosphoinositide 3-kinase signalling pathways in tumor progression, invasion and angiogenesis. Tumori, 90, 2-8.
84. Merritt, W.M. et al. (2009) Anti-angiogenic properties of metronomic topotecan in ovarian carcinoma. Cancer Biol. Ther., 8, 1596-1603.