CLC number: R9
On-line Access: 2024-08-27
Received: 2023-10-17
Revision Accepted: 2024-05-08
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Suo-fu Ye, Yong Yang, Lin Wu, Wei-wei Ma, Hui-hui Zeng. Ethaselen: a novel organoselenium anticancer agent targeting thioredoxin reductase 1 reverses cisplatin resistance in drug-resistant K562 cells by inducing apoptosis[J]. Journal of Zhejiang University Science B, 2017, 18(5): 373-382.
@article{title="Ethaselen: a novel organoselenium anticancer agent targeting thioredoxin reductase 1 reverses cisplatin resistance in drug-resistant K562 cells by inducing apoptosis",
author="Suo-fu Ye, Yong Yang, Lin Wu, Wei-wei Ma, Hui-hui Zeng",
journal="Journal of Zhejiang University Science B",
volume="18",
number="5",
pages="373-382",
year="2017",
publisher="Zhejiang University Press & Springer",
doi="10.1631/jzus.B1600073"
}
%0 Journal Article
%T Ethaselen: a novel organoselenium anticancer agent targeting thioredoxin reductase 1 reverses cisplatin resistance in drug-resistant K562 cells by inducing apoptosis
%A Suo-fu Ye
%A Yong Yang
%A Lin Wu
%A Wei-wei Ma
%A Hui-hui Zeng
%J Journal of Zhejiang University SCIENCE B
%V 18
%N 5
%P 373-382
%@ 1673-1581
%D 2017
%I Zhejiang University Press & Springer
%DOI 10.1631/jzus.B1600073
TY - JOUR
T1 - Ethaselen: a novel organoselenium anticancer agent targeting thioredoxin reductase 1 reverses cisplatin resistance in drug-resistant K562 cells by inducing apoptosis
A1 - Suo-fu Ye
A1 - Yong Yang
A1 - Lin Wu
A1 - Wei-wei Ma
A1 - Hui-hui Zeng
J0 - Journal of Zhejiang University Science B
VL - 18
IS - 5
SP - 373
EP - 382
%@ 1673-1581
Y1 - 2017
PB - Zhejiang University Press & Springer
ER -
DOI - 10.1631/jzus.B1600073
Abstract: It has been reported that ethaselen shows inhibitory effects on thioredoxin reductase (TrxR) activity and human tumor cell growth. In order to find an efficient way to reverse cisplatin resistance%29&ck%5B%5D=abstract&ck%5B%5D=keyword'>cisplatin resistance, we investigated the reversal effects of ethaselen on cisplatin resistance%29&ck%5B%5D=abstract&ck%5B%5D=keyword'>cisplatin resistance in K562/cisplatin (CDDP) cells that were established by pulse-inducing human erythrocyte leukemic cell line K562, which are fivefold more resistant to cisplatin compared to K562 cells. The morphology and growth showed that the adhesion of K562/CDDP further decreased while the cell volume increased. The proliferation of K562/CDDP is strengthened. The antitumor activities in vitro were assessed by MTT (3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide) assay and combination index (CI), showing the significant synergic effects of cisplatin and ethaselen. Focusing on apoptosis, a series of comparisons was made between K562 and K562/CDDP. cisplatin induced higher reactive oxygen species (ROS) generation in K562 and subsequently induced the formation of mitochondrial permeability transition pores (PTPs). In addition, cisplatin increased the ratio of Bax to bcl-2 in K562, which can influence the mitochondrial membrane permeability. PTP formation and mitochondrial membrane permeabilization eventually resulted in the release of cytochrome c and activation of the Caspase pathway. However, these effects were not clearly seen in K562/CDDP, which may be the reason for the acquired CDDP resistance. However, ethaselen can induce a high level of ROS in K562/CDDP by TrxR activity inhibition and increased ratio of Bax to bcl-2 in K562/CDDP by nuclear factor κB (NF-κB) suppression, which subsequently induces the release of cytochrome c in K562/CDDP. This response is partly responsible for the reversal of the cisplatin resistance%29&ck%5B%5D=abstract&ck%5B%5D=keyword'>cisplatin resistance in K562/CDDP cells.
[1]Bargou, R.C., Bommert, K., Weinmann, P., et al., 1995. Induction of Bax-α precedes apoptosis in a human B lymphoma cell line: potential role of the bcl-2 gene family in surface IgM-mediated apoptosis. Eur. J. Immunol., 25(3):770-775.
[2]Chao, C.C., Huang, S.L., Huang, H.M., et al., 1991. Cross-resistance to UV radiation of a cisplatin-resistant human cell line: overexpression of cellular factors that recognize UV-modified DNA. Mol. Cell. Biol., 11(4):2075-2080.
[3]Chen, J., Li, H.M., Zhang, X.N., et al., 2014. Dioscin-induced apoptosis of human LNCaP prostate carcinoma cells through activation of caspase-3 and modulation of Bcl-2 protein family. J. Huazhong Univ. Sci. Technol. Med. Sci., 34(1):125-130.
[4]Chu, G., 1994. Cellular responses to cisplatin. The roles of DNA-binding proteins and DNA repair. J. Biol. Chem., 269(2):787-790.
[5]Du, J.P., Chen, P., Fei, H.X., et al., 2007. Establishment of adriamycin-resistant and cisplatin-resistant gastric cancer cell lines and assessment on their sustainability of drug resistance. Chin. J. Gastroenterol. Hepatol., 16(4):368-372 (in Chinese).
[6]Dumay, A., Laulier, C., Bertrand, P., et al., 2006. Bax and Bid, two proapoptotic Bcl-2 family members, inhibit homologous recombination, independently of apoptosis regulation. Oncogene, 25(22):3196-3205.
[7]Fu, J.N., Li, J., Tan, Q., et al., 2011. Thioredoxin reductase inhibitor ethaselen increases the drug sensitivity of the colon cancer cell line LoVo towards cisplatin via regulation of G1 phase and reversal of G2/M phase arrest. Invest. New Drugs, 29(4):627-636.
[8]Hahn, P., Lindsten, T., Ying, G.S., et al., 2003. Proapoptotic Bcl-2 family members, Bax and Bak, are essential for developmental photoreceptor apoptosis. Invest. Ophthalmol. Vis. Sci., 44(8):3598-3605.
[9]Harrington, C.F., le Pla, R.C., Jones, G.D., et al., 2010. Determination of cisplatin 1,2-intrastrand guanine-guanine DNA adducts in human leukocytes by high-performance liquid chromatography coupled to inductively coupled plasma mass spectrometry. Chem. Res. Toxicol., 23(8): 1313-1321.
[10]Haslehurst, A.M., Koti, M., Dharsee, M., et al., 2012. EMT transcription factors snail and slug directly contribute to cisplatin resistance in ovarian cancer. BMC Cancer, 12:91.
[11]Heath-Engel, H.M., Chang, N.C., Shore, G.C., 2008. The endoplasmic reticulum in apoptosis and autophagy: role of the BCL-2 protein family. Oncogene, 27(50):6419-6433.
[12]Jia, G., Wang, Q., Wang, R., et al., 2015. Tubeimoside-1 induces glioma apoptosis through regulation of Bax/Bcl-2 and the ROS/Cytochrome C/Caspase-3 pathway. OncoTargets Ther., 8:303-311.
[13]Lan, L., Zhao, F., Wang, Y., et al., 2007. The mechanism of apoptosis induced by a novel thioredoxin reductase inhibitor in A549 cells: possible involvement of nuclear factor-κB-dependent pathway. Eur. J. Pharmacol., 555(2-3): 83-92.
[14]Mantri, Y., Lippard, S.J., Baik, M.H., 2007. Bifunctional binding of cisplatin to DNA: why does cisplatin form 1,2-intrastrand cross-links with AG but not with GA? J. Am. Chem. Soc., 129(16):5023-5030.
[15]Miyata, Y., Nomata, K., Ohba, K., et al., 2012. Use of low-dose combined therapy with gemcitabine and paclitaxel for advanced urothelial cancer patients with resistance to cisplatin-containing therapy: a retrospective analysis. Cancer Chemother. Pharmacol., 70(3):451-459.
[16]Oiso, S., Takayama, Y., Nakazaki, R., et al., 2014. Factors involved in the cisplatin resistance of KCP-4 human epidermoid carcinoma cells. Oncol. Rep., 31(2):719-726.
[17]Rossé, T., Olivier, R., Monney, L., et al., 1998. Bcl-2 prolongs cell survival after Bax-induced release of cytochrome c. Nature, 391(6666):496-499.
[18]Sainz, R.M., Mayo, J.C., Tan, D.X., et al., 2003. Antioxidant activity of melatonin in Chinese hamster ovarian cells: changes in cellular proliferation and differentiation. Biochem. Biophys. Res. Commun., 302(3):625-634.
[19]Shi, C., Yu, L., Yang, F., et al., 2003. A novel organoselenium compound induces cell cycle arrest and apoptosis in prostate cancer cell lines. Biochem. Biophys. Res. Commun., 309(3):578-583.
[20]Tan, Q., Li, J., Yin, H.W., et al., 2010. Augmented antitumor effects of combination therapy of cisplatin with ethaselen as a novel thioredoxin reductase inhibitor on human A549 cell in vivo. Invest. New Drugs, 28(3):205-215.
[21]Tanaka, S., Wakeyama, H., Akiyama, T., et al., 2010. Regulation of osteoclast apoptosis by Bcl-2 family protein Bim and Caspase-3. Adv. Exp. Med. Biol., 658:111-116.
[22]Tao, X.J., Tilly, K.I., Maravei, D.V., et al., 1997. Differential expression of members of the bcl-2 gene family in proliferative and secretory human endometrium: glandular epithelial cell apoptosis is associated with increased expression of bax. J. Clin. Endocrinol. Metab., 82(8):2738-2746.
[23]Tilly, J.L., Tilly, K.I., Kenton, M.L., et al., 1995. Expression of members of the bcl-2 gene family in the immature rat ovary: equine chorionic gonadotropin-mediated inhibition of granulosa cell apoptosis is associated with decreased bax and constitutive bcl-2 and bcl-xlong messenger ribonucleic acid levels. Endocrinology, 136(1): 232-241.
[24]Torigoe, T., Izumi, H., Ishiguchi, H., et al., 2005. Cisplatin resistance and transcription factors. Curr. Med. Chem. Anticancer Agents, 5(1):15-27.
[25]Wang, L., Fu, J.N., Wang, J.Y., et al., 2011. Selenium-containing thioredoxin reductase inhibitor ethaselen sensitizes non-small cell lung cancer to radiotherapy. Anticancer Drugs, 22(8):732-740.
[26]Wang, L., Yang, Z., Fu, J., et al., 2012. Ethaselen: a potent mammalian thioredoxin reductase 1 inhibitor and novel organoselenium anticancer agent. Free Radic. Biol. Med., 52(5):898-908.
[27]Xing, F., Li, S., Ge, X., et al., 2008. The inhibitory effect of a novel organoselenium compound BBSKE on the tongue cancer Tca8113 in vitro and in vivo. Oral Oncol., 44(10):963-969.
[28]Yaneva, J.N., Paneva, E.G., Zacharieva, S.I., et al., 2007. Histone H1 interacts preferentially with DNA fragments containing a cisplatin-induced 1,2-intrastrand cross-link. Z. Naturforsch. C, 62(11-12):905-908.
[29]Yeh, K.H., Cheng, A.L., 1997. High-dose tamoxifen reverses drug resistance to cisplatin and etoposide in a patient with advanced large cell carcinoma of lung. Anticancer Res., 17(2B):1341-1343.
[30]Zhao, F., Yan, J., Deng, S., et al., 2006. A thioredoxin reductase inhibitor induces growth inhibition and apoptosis in five cultured human carcinoma cell lines. Cancer Lett., 236(1):46-53.
[31]Zheng, S., Zhao, M., Ren, Y., et al., 2015. Sesamin suppresses STZ induced INS-1 cell apoptosis through inhibition of NF-κB activation and regulation of Bcl-2 family protein expression. Eur. J. Pharmacol., 750:52-58.
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