Nrf2 expression and apoptosis in quercetin-treated malignant mesothelioma cells

Molecules and Cells

Volumn 38, Issue 5, 2015, Pages 416-425

  Lee, Yoon Jin ^a,b   Lee, David M ^c   Lee, Sang Han ^b  

^a Soonchunhyang Medical Research Institute   (South Korea)

^b Soonchunhyang University   (South Korea)

^c University of Maryland   (United States)

Author keywords

Apoptosis; Chemoresistance; Cisplatin; Mesothelioma; Nrf2; Quercetin

Indexed keywords

CASPASE 3; CISPLATIN; HEME OXYGENASE 1; LIPOCORTIN 5; MESSENGER RNA; PROTEIN; PROTEIN BAX; PROTEIN BCL 2; QUERCETIN; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR NRF2; ANTIOXIDANT; NFE2L2 PROTEIN, HUMAN;

ANTIOXIDANT ACTIVITY; ANTIOXIDANT RESPONSIVE ELEMENT; APOPTOSIS; ARTICLE; CANCER INHIBITION; CELL GROWTH; CELL PROTECTION; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; FLOW CYTOMETRY; HALF LIFE TIME; HUMAN; HUMAN CELL; MALIGNANT MESOTHELIOMA; MESOTHELIOMA CELL LINE; OXIDATIVE STRESS; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSCRIPTION INITIATION; TUMOR GENE; UBIQUITINATION; UPREGULATION; ANTAGONISTS AND INHIBITORS; CELL PROLIFERATION; DRUG EFFECTS; DRUG POTENTIATION; DRUG RESISTANCE; GENE EXPRESSION REGULATION; GENETICS; MESOTHELIOMA; METABOLISM; TUMOR CELL LINE;

ANTIOXIDANTS; APOPTOSIS; CELL LINE, TUMOR; CELL PROLIFERATION; DRUG RESISTANCE, NEOPLASM; DRUG SYNERGISM; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MESOTHELIOMA; NF-E2-RELATED FACTOR 2; QUERCETIN; RNA, SMALL INTERFERING; UP-REGULATION;

EID: 84946404287     PISSN: 10168478     EISSN: 02191032     Source Type: Journal    
DOI: 10.14348/molcells.2015.2268     Document Type: Article

References (36)

1. Bao, L.J., Jaramillo, M.C., Zhang, Z.B., Zheng, Y.X., Yao, M., Zhang, D.D., and Yi, X.F. (2014). Nrf2 induces cisplatin resistance through activation of autophagy in ovarian carcinoma. Int. J. Clin. Exp. Pathol. 7, 1502-1513.
2. Borska, S., Chmielewska, M., Wysocka, T., Drag-Zalesinska, M., Zabel, M., and Dziegiel, P. (2012). In vitro effect of quercetin on human gastric carcinoma: targeting cancer cells death and MDR. Food Chem. Toxicol. 50, 3375-3383.
3. Ceccarelli, J., Delfino, L., Zappia, E., Castellani, P., Borghi, M., and Ferrini, S. (2008). The redox state of the lung cancer microenvironment depends on the levels of thioredoxin expressed by tumor cells and affects tumor progression and response to prooxidants. Int. J. Cancer 123, 1770-1778.
4. Chung, T.W., Choi, H.J., Kim, S.J., Kwak, C.H., Song, K.H., Jin, U.H., Chang, Y.C., Chang, H.W., Lee, Y.C., Ha, K.T., et al. (2014). The ganglioside GM3 is associated with cisplatininduced apoptosis in human colon cancer cells. PLoS One 9, e92786.
5. Ferraresi, R., Troiano, L., Roat, E., Lugli, E., Nemes, E., Nasi, M., Pinti, M., Fernandez, M.I., Cooper, E.L., and Cossarizza, A. (2005). Essential requirement of reduced glutathione (GSH) for the anti-oxidant effect of the flavonoid quercetin. Free Radic. Res. 39, 1249-1258.
6. Granado-Serrano, A., Martin, M., Bravo, L., Goya, L., and Ramos, S. (2006). Quercetin induces apoptosis via caspase activation, regulation of Bcl-2, and inhibition of PI-3-Kinase/Akt and ERK pathways in a human hepatoma cell line (HepG2). J. Nutr. 136, 2715-2721.
7. Jiang, T., Chen, N., Zhao, F., Wang, X.J., Kong, B., Zheng, W., and Zhang, D.D. (2010). High levels of Nrf2 determine chemoresistance in type II endometrial cancer. Cancer Res. 70, 5486-5496.
8. Jiang, B., Xiao, S., Khan, MA., and Xue, M. (2013). Defective antioxidant systems in cervical cancer. Tumour Biol. 34, 2003-2009.
9. Ji, X.J., Chen, S.H., Zhu, L., Pan, H., Zhou, Y., Li, W., You, W.C., Gao, C.C., Zhu, J.H., Jiang, K., et al. (2013). Knockdown of NFE2-related factor 2 inhibits the proliferation and growth of U251MG human glioma cells in a mouse xenograft model. Oncol. Rep. 30, 157-164.
10. Khanduja, K.L., Gandhi, R.K., Pathania, V., and Syal, N. (1999). Prevention of N-nitrosodiethylamine-induced lung tumorigenesis by ellagic acid and quercetin in mice. Food Chem. Toxicol. 37, 313-318.
11. Kim, S.J., Miyoshi, Y., Taguchi, T., Tamaki, Y., Nakamura, H., Yodoi, J., Kato, K., and Noguchi, S. (2005). High thioredoxin expression is associated with resistance to docetaxel in primary breast cancer. Clin. Cancer Res. 11, 8425-8430.
12. Kim, Y.R., Oh, J.E., Kim, M.S., Kang, M.R., Park, S.W., Han, J.Y., Eom, H.S., Yoo, N.J., and Lee, S.H. (2011). Oncogenic NRF2 mutations in squamous cell carcinomas of oesophagus and skin. J. Pathol. 220, 446-451.
13. Lau, A., Villeneuve, N.F., Sun, Z., Wong, P.K., and Zhang, D.D. (2008). Dual roles of Nrf2 in cancer. Pharmacol. Res. 58, 262-270.
14. Lee, Y.J., Jeong, H.Y., Kim, Y.B., Lee, Y.J., Won, S.Y., Shim, J.H., Cho, M.K., Nam, H.S., and Lee S.H. (2012). Reactive oxygen species and PI3K/Akt signaling play key roles in the induction of Nrf2-driven heme oxygenase-1 expression in sulforaphanetreated human mesothelioma MSTO-211H cells. Food Chem. Toxicol. 50, 116-123.
15. Lee, H.S., Lee, G.S., Kim, S.H., Kim, H.K., Suk, D.H., and Lee, D.S. (2014). Anti-oxidizing effect of the dichloromethane and hexane fractions from Orostachys japonicus in LPS-stimulated RAW 264.7 cells via upregulation of Nrf2 expression and activation of MAPK signaling pathway. BMB Rep. 47, 98-103.
16. Li, N., Sun, C., Zhou, B., Xing, H., Ma, D., Chen, G., and Weng, D. (2014). Low concentration of quercetin antagonizes the cytotoxic effects of anti-neoplastic drugs in ovarian cancer. PLoS One 9, e100314.
17. Merikallio, H., Pääkkö, P., Kinnula, V.L., and Harju, T. (2012). Nuclear factor erythroid-derived 2-like 2 (Nrf2) and DJ1 are prognostic factors in lung cancer. Hum. Pathol. 43, 577-584.
18. Niture, S.K., and Jaiswal, A.K. (2013). Nrf2-induced antiapoptotic Bcl-xL protein enhances cell survival and drug resistance. Free Radic. Biol. Med. 57, 119-131.
19. Oberley, T.D., and Oberley, L.W. (1997). Antioxidant enzyme levels in cancer. Histol. Histopathol. 12, 525-535.
20. Ogretmen, B., Bahadori, H.R., McCauley, M.D., Boylan, A., Green, M.R., and Safam A.R. (1998). Co-ordinated over-expression of the MRP and gamma-glutamylcysteine synthetase genes, but not MDR1, correlates with doxorubicin resistance in human malignant mesothelioma cell lines. Int. J. Cancer 75, 757-761.
21. Ohta, T., Iijima, K., Miyamoto, M., Nakahara, I., Tanaka, H., Ohtsuji, M., Suzuki, T., Kobayashi, A., Yokota, J., Sakiyama, T., et al. (2008). Loss of Keap1 function activates Nrf2 and provides advantages for lung cancer cell growth. Cancer Res. 68, 1303-1309.
22. Qu, L.Y., Gao, P., Wang, H.Y., Wang, X.J., and Tang, X.W. (2010). Nrf2 down-regulated cell line H460-N5 with Keap1 overexpression increased sensitivity to anti-cancer drugs. Zhejiang Da Xue Xue Bao Yi Xue Ban 39, 6-10.
23. Robaszkiewicz, A., Balcerczyk, A., and Bartosz, G. (2007). Antioxidative and prooxidative effects of quercetin on A549 cells. Cell Biol. Int. 31, 1245-1250.
24. Samuel, T., Fadlalla, K., Mosley, L., Katkoori, V., Turner, T., and Manne, U. (2012). Dual-mode interaction between quercetin and DNA-damaging drugs in cancer cells. Anticancer Res. 32, 61-71.
25. Saw, C.L., Guo, Y., Yang, A.Y., Paredes-Gonzalez, X., Ramirez, C., Pung, D., and Kong, A.N. (2014). The berry constituents quercetin, kaempferol, and pterostilbene synergistically attenuate reactive oxygen species: Involvement of the Nrf2-ARE signaling pathway. Food Chem. Toxicol. 72, 303-311.
26. Sharma, M., Rajappa, M., Kumar, G., and Sharma, A. (2009). Oxidant-antioxidant status in Indian patients with carcinoma of posterior one-third of tongue. Cancer Biomark. 5, 253-260.
27. Shibata, T., Kokubu, A., Gotoh, M., Ojima, H., Ohta, T., Yamamoto, M., and Hirohashi, S. (2008). Genetic alteration of Keap1 confers constitutive Nrf2 activation and resistance to chemotherapy in gallbladder cancer. Gastroenterology 135, 1358-1368.
28. Shim, G.S., Manandhar, S., Shin, D.H., Kim, T.H., and Kwak, M.K. (2009). Acquisition of doxorubicin resistance in ovarian carcinoma cells accompanies activation of the NRF2 pathway. Free Radic. Biol. Med. 47, 1619-1631.
29. Slocum, S.L., and Kensler, T.W. (2011). Nrf2: control of sensitivity to carcinogens. Arch. Toxicol. 85, 273-284.
30. Stacy, D.R., Ely, K., Massion, P.P., Yarbrough, W.G., Hallahan, D.E., and Sekhar, K.R. (2006). Increased expression of nuclear factor E2 p45-related factor 2 (NRF2) in head and neck squamous cell carcinomas. Head Neck 28, 813-818.
31. Thrower, J.S., Hoffman, L., Rechsteiner, M., and Pickart, C.M. (2000). Recognition of the polyubiquitin proteolytic signal. EMBO J. 19, 94-102.
32. Wakabayashi, N., Dinkova-Kostova, A.T., Holtzclaw, W.D., Kang, M.I., Kobayashi, A., Yamamoto, M., Kensler, T.W., and Talalay P. (2004). Protection against electrophile and oxidant stress by induction of the phase 2 response: fate of cysteines of the Keap1 sensor modified by inducers. Proc. Natl. Acad. Sci. USA. 101, 2040-2045.
33. Wang, X.J., Sun, Z., Villeneuve, N.F., Zhang, S., Zhao, F., Li, Y., Chen, W., Yi, X., Zheng, W., Wondrak, G.T., Wong, P.K., et al. (2008). Nrf2 enhances resistance of cancer cells to chemotherapeutic drugs, the dark side of Nrf2. Carcinogenesis 29, 1235-1243.
34. Yang, H., Wang, W., Zhang, Y., Zhao, J., Lin, E., Gao, J., and He, J. (2011). The role of NF-E2-related factor 2 in predicting chemoresistance and prognosis in advanced non-small-cell lung cancer. Clin. Lung Cancer 12, 166-171.
35. 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.
36. Zhong, Y., Zhang, F., Sun, Z., Zhou, W., Li, Z.Y., You, Q.D., Guo Q.L., and Hu, R. (2012). Drug resistance associates with activation of Nrf2 in MCF-7/DOX cells, and wogonin reverses it by down-regulating Nrf2-mediated cellular defense response. Mol. Carcinog. 52, 824-834.