Synergistic Induction of Apoptosis by the Combination of an Axl Inhibitor and Auranofin in Human Breast Cancer Cells |
Ryu, Yeon-Sang
(Center for Metareceptome Research, College of Pharmacy, Chung-Ang University)
Shin, Sangyun (Center for Metareceptome Research, College of Pharmacy, Chung-Ang University) An, Hong-Gyu (Center for Metareceptome Research, College of Pharmacy, Chung-Ang University) Kwon, Tae-Uk (Center for Metareceptome Research, College of Pharmacy, Chung-Ang University) Baek, Hyoung-Seok (Center for Metareceptome Research, College of Pharmacy, Chung-Ang University) Kwon, Yeo-Jung (Center for Metareceptome Research, College of Pharmacy, Chung-Ang University) Chun, Young-Jin (Center for Metareceptome Research, College of Pharmacy, Chung-Ang University) |
1 | Holland, S. J., Pan, A., Franci, C., Hu, Y., Chang, B., Li, W., Duan, M., Torneros, A., Yu, J., Heckrodt, T. J., Zhang, J., Ding, P., Apatira, A., Chua, J., Brandt, R., Pine, P., Goff, D., Singh, R., Payan, D. G. and Hitoshi, Y. (2010) R428, a selective small molecule inhibitor of Axl kinase, blocks tumor spread and prolongs survival in models of metastatic breast cancer. Cancer Res. 70, 1544-1554. DOI |
2 | Jin, S. and Ye, K. (2013) Targeted drug delivery for breast cancer treatment. Recent Pat. Anticancer Drug Discov. 8, 143-153. |
3 | Jung, J. (2019) Role of G protein-coupled estrogen receptor in cancer progression. Toxicol. Res. 35, 209-214. DOI |
4 | Kapur, A., Beres, T., Rathi, K., Nayak, A. P., Czarnecki, A., Felder, M., Gillette, A., Ericksen, S. S., Sampene, E., Skala, M. C., Barroilhet, L. and Patankar, M. S. (2018) Oxidative stress via inhibition of the mitochondrial electron transport and Nrf-2-mediated anti-oxidative response regulate the cytotoxic activity of plumbagin. Sci. Rep. 8, 1073. DOI |
5 | Katoh, H., Hiramoto, K. and Negishi, M. (2006) Activation of Rac1 by RhoG regulates cell migration. J. Cell Sci. 119, 56-65. DOI |
6 | Koorstra, J. B., Karikari, C. A., Feldmann, G., Bisht, S., Rojas, P. L., Offerhaus, G. J., Alvarez, H. and Maitra, A. (2009) The Axl receptor tyrosine kinase confers an adverse prognostic influence in pancreatic cancer and represents a new therapeutic target. Cancer Biol. Ther. 8, 618-626. DOI |
7 | Leconet, W., Chentouf, M., du Manoir, S., Chevalier, C., Sirvent, A., Ait-Arsa, I., Busson, M., Jarlier, M., Radosevic-Robin, N., Theillet, C., Chalbos, D., Pasquet, J. M., Pelegrin, A., Larbouret, C. and Robert, B. (2017) Therapeutic activity of anti-Axl antibody against triple-negative breast cancer patient-derived xenografts and metastasis. Clin. Cancer Res. 23, 2806-2816. DOI |
8 | Lu, K., Alcivar, A. L., Ma, J., Foo, T. K., Zywea, S., Mahdi, A., Huo, Y., Kensler, T. W., Gatza, M. L. and Xia, B. (2017) NRF2 induction supporting breast cancer cell survival is enabled by oxidative stress-induced DPP3-Keap1 interaction. Cancer Res. 77, 2881-2892. DOI |
9 | Lee, J. E., Kwon, Y. J., Baek, H. S., Ye, D. J., Cho, E., Choi, H. K., Oh, K. S. and Chun, Y. J. (2017) Synergistic induction of apoptosis by combination treatment with mesupron and auranofin in human breast cancer cells. Arch. Pharm. Res. 40, 746-759. DOI |
10 | Lee, W. P., Wen, Y., Varnum, B. and Hung, M. C. (2002) Akt is required for Axl-Gas6 signaling to protect cells from E1A-mediated apoptosis. Oncogene 21, 329-336. DOI |
11 | Maes, M. E., Schlamp, C. L. and Nickells, R. W. (2017) Live-cell imaging to measure Bax recruitment kinetics to mitochondria during apoptosis. PLoS ONE 12, e0184434. DOI |
12 | Oommen, D., Yiannakis, D. and Jha, A. N. (2016) BRCA1 deficiency increases the sensitivity of ovarian cancer cells to auranofin. Mutat. Res. 784-785, 8-15. DOI |
13 | Miller, M. A., Oudin, M. J., Sullivan, R. J., Wang, S. J., Meyer, A. S., Im, H., Frederick, D. T., Tadros, J., Griffith, L. G., Lee, H., Weissleder, R., Flaherty, K. T., Gertler, F. B. and Lauffenburger, D. A. (2016) Reduced proteolytic shedding of receptor tyrosine kinases is a post-translational mechanism of kinase inhibitor resistance. Cancer Discov. 6, 382-399. DOI |
14 | Mine, N., Yamamoto, S., Kufe, D. W., Von Hoff, D. D. and Kawabe, T. (2014) Activation of Nrf2 pathways correlates with resistance of NSCLC cell lines to CBP501 in vitro. Mol. Cancer Ther. 13, 2215-2225. DOI |
15 | Nagini, S. (2017) Breast cancer: current molecular therapeutic targets and new players. Anticancer Agents Med. Chem. 17, 152-163. DOI |
16 | Pawlowski, J. and Kraft, A. S. (2000) Bax-induced apoptotic cell death. Proc. Natl. Acad. Sci. U.S.A. 97, 529-531. DOI |
17 | Shaw, I. C. (1999) Gold-based therapeutic agents. Chem. Rev. 99, 2589-2600. DOI |
18 | Probst, B. L., McCauley, L., Trevino, I., Wigley, W. C. and Ferguson, D. A. (2015) Cancer cell growth is differentially affected by constitutive activation of NRF2 by Keap1 deletion and pharmacological activation of NRF2 by the synthetic triterpenoid, RTA 405. PLoS ONE 10, e0135257. DOI |
19 | Richa, S., Dey, P., Park, C., Yang, J., Son, J. Y., Park, J. H., Lee, S. H., Ahn, M. Y., Kim, I. S., Moon, H. R. and Kim, H. S. (2020) A new histone deacetylase inhibitor, MHY4381, induces apoptosis via generation of reactive oxygen species in human prostate cancer cells. Biomol. Ther. (Seoul) 28, 184-194. DOI |
20 | Shamas-Din, A., Kale, J., Leber, B. and Andrews, D. W. (2013) Mechanisms of action of Bcl-2 family proteins. Cold Spring Harb. Perspect. Biol. 5, a008714. |
21 | Sun, S. Y. (2010) N-acetylcysteine, reactive oxygen species and beyond. Cancer Biol. Ther. 9, 109-110. DOI |
22 | Tallarida, R. J. (2001) Drug synergism: its detection and applications. J. Pharmacol. Exp. Ther. 298, 865-872. |
23 | Tang, B., Tang, F., Wang, Z., Qi, G., Liang, X., Li, B., Yuan, S., Liu, J., Yu, S. and He, S. (2016) Upregulation of -regulated inflammation and Akt/Bad-related apoptosis signaling pathway involved in hepatic carcinoma process: suppression by carnosic acid nanoparticle. Int. J. Nanomedicine 11, 6401-6420. DOI |
24 | Yao, H., He, G., Yan, S., Chen, C., Song, L., Rosol, T. J. and Deng, X. (2017) Triple-negative breast cancer: is there a treatment on the horizon. Oncotarget 8, 1913-1924. DOI |
25 | Varghese, E. and Busselberg, D. (2014) Auranofin, an anti-rheumatic gold compound, modulates apoptosis by elevating the intracellular calcium concentration in MCF-7 breast cancer cells. Cancers (Basal) 6, 2243-2258. DOI |
26 | Vidula, N. and Bardia, A. (2017) Targeted therapy for metastatic triple negative breast cancer: the next frontier in precision oncology. Oncotarget 8, 106167-106168. DOI |
27 | Bayat Mokhtari, R., Homayouni, T. S., Baluch, N., Morgatskaya, E., Kumar, S., Das, B. and Yeger, H. (2017) Combination therapy in combating cancer. Oncotarget 8, 38022-38043. DOI |
28 | Cazanave, S. C., Wang, X., Zhou, H., Rahmani, M., Grant, S., Durrant, D. E., Klaassen, C. D., Yamamoto, M. and Sanyal, A. J. (2014) Degradation of Keap1 activates BH3-only proteins Bim and PUMA during hepatocyte lipoapoptosis. Cell Death Differ. 21, 1303-1312. DOI |
29 | Chu, C., Gao, X., Li, X., Zhang, X., Ma, R., Jia, Y., Li, D., Wang, D. and Xu, F. (2020) Involvement of estrogen in the activation of Nrf2-antioxidative signaling pathways by silibinin in pancreatic -cells. Biomol. Ther. (Seoul) 28, 163-171. DOI |
30 | Wang, C., Jin, H., Wang, N., Fan, S., Wang, Y., Zhang, Y., Wei, L., Tao, X., Gu, D., Zhao, F., Fang, J., Yao, M. and Qin, W. (2016) Gas6/Axl axis contributes to chemoresistance and metastasis in breast cancer through kat/GSK--catenin signaling. Theranostics 6, 1205-1219. DOI |
31 | Zhang, P., Singh, A., Yegnasubramanian, S., Esopi, D., Kombairaju, P., Bodas, M., Wu, H., Bova, S. G. and Biswal, S. (2010) Loss of Kelch-like ECH-associated protein 1 function in prostate cancer cells causes chemoresistance and radioresistance and promotes tumor growth. Mol. Cancer Ther. 9, 336-346. DOI |
32 | Zhang, Y. X., Knyazev, P. G., Cheburkin, Y. V., Sharma, K., Knyazev, Y. P., Orfi, L., Szabadkai, I., Daub, H., Keri, G. and Ullrich, A. (2008) Axl is a potential target for therapeutic intervention in breast cancer progression. Cancer Res. 68, 1905-1915. DOI |
33 | Katz, H. and Alsharedi, M. (2017) Immunotherapy in triple-negative breast cancer. Med. Oncol. 35, 13. |
34 | Fiskus, W., Saba, N., Shen, M., Ghias, M., Liu, J., Gupta, S. D., Chauhan, L., Rao, R., Gunewardena, S., Schorno, K., Austin, C. P., Maddocks, K., Byrd, J., Melnick, A., Huang, P., Wiestner, A. and Bhalla, K. N. (2014) Auranofin induces lethal oxidative and endoplasmic reticulum stress and exerts potent preclinical activity against chronic lymphocytic leukemia. Cancer Res. 74, 2520-2532. DOI |
35 | Cuadrado, A., Manda, G., Hassan, A., Alcaraz, M. J., Barbas, C., Daiber, A., Ghezzi, P., Leon, R., Lopez, M. G., Oliva, B., Pajares, M., Rojo, A. I., Robledinos-Anton, N., Valverde, A. M., Guney, E. and Schmidt, H. (2018) Transcription factor NRF2 as a therapeutic target for chronic diseases: a systems medicine approach. Pharmacol. Rev. 70, 348-383. DOI |
36 | Cuadrado, A., Martin-Moldes, Z., Ye, J. and Lastres-Becker, I. (2014) Transcription factors NRF2 and are coordinated effectors of the Rho family, GTP-binding protein RAC1 during inflammation. J. Biol. Chem. 289, 15244-15258. DOI |
37 | Faix, J. and Weber, I. (2013) A dual role model for active Rac1 in cell migration. Small GTPases 4, 110-115. DOI |
38 | Gay, C. M., Balaji, K. and Byers, L. A. (2017) Giving AXL the axe: targeting AXL in human malignancy. Br. J. Cancer 116, 415-423. DOI |
39 | Gelmon, K., Dent, R., Mackey, J. R., Laing, K., McLeod, D. and Verma, S. (2012) Targeting triple-negative breast cancer: optimising therapeutic outcomes. Ann. Oncol. 23, 2223-2234. DOI |
40 | Goyette, M. A., Duhamel, S., Aubert, L., Pelletier, A., Savage, P., Thibault, M. P., Johnson, R. M., Carmeliet, P., Basik, M., Gaboury, L., Muller, W. J., Park, M., Roux, P. P., Gratton, J. P. and Cote, J. F. (2018) The receptor tyrosine kinase Axl is required at multiple steps of the metastatic cascade during HER2-positive breast cancer progression. Cell Rep. 23, 1476-1490. DOI |