Nrf2- and ATF4-dependent upregulation of xCT modulates the sensitivity of T24 bladder carcinoma cells to proteasome inhibition

Molecular and Cellular Biology

Volumn 34, Issue 18, 2014, Pages 3421-3434

  Ye, Peng ^a   Mimura, Junsei ^a   Okada, Tomomi ^b   Sato, Hideyo ^b   Liu, Tao ^a   Maruyama, Atsushi ^a   Ohyama, Chikara ^c   Itoh, Ken ^a  

^a HIROSAKI UNIVERSITY   (Japan)

^b YAMAGATA UNIVERSITY   (Japan)

^c HIROSAKI UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

4 CARBOXYPHENYLGLYCINE; ACTIVATING TRANSCRIPTION FACTOR 4; ANTIPORTER; PROTEASOME; PROTEASOME INHIBITOR; SALAZOSULFAPYRIDINE; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR NRF2;

ARTICLE; BLADDER CANCER CELL LINE; BLADDER CARCINOMA; CELL SURVIVAL; CONTROLLED STUDY; DRUG CYTOTOXICITY; DRUG SENSITIVITY; ENZYME INHIBITION; GENE EXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; PRIORITY JOURNAL; TUMOR CELL; UPREGULATION;

ACTIVATING TRANSCRIPTION FACTOR 4; AMINO ACID TRANSPORT SYSTEM Y+; ANTINEOPLASTIC AGENTS; BORONIC ACIDS; CELL LINE, TUMOR; CYSTEINE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE KNOCKDOWN TECHNIQUES; GLUTATHIONE; GLYCINE; HEK293 CELLS; HELA CELLS; HUMANS; LEUPEPTINS; NF-E2-RELATED FACTOR 2; OLIGOPEPTIDES; PROTEASOME ENDOPEPTIDASE COMPLEX; PYRAZINES; RNA, SMALL INTERFERING; SULFASALAZINE; URINARY BLADDER NEOPLASMS;

EID: 84906054877     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00221-14     Document Type: Article

References (59)

1. Hochstrasser M. 1995. Ubiquitin, proteasomes, and the regulation of intracellular protein degradation. Curr. Opin. Cell Biol. 7:215-223. http://dx.doi.org/10.1016/0955-0674(95)80031-X.
2. Jentsch S, Schlenker S. 1995. Selective protein degradation: a journey's end within the proteasome. Cell 82:881-884. http://dx.doi.org/10.1016/0092-8674(95)90021-7.
3. Adams J. 2003. The proteasome: structure, function, and role in the cell. Cancer Treat. Rev. 29(Suppl. 1):3-9. http://dx.doi.org/10.1016/S0305-7372(03)00081-1.
4. Voorhees PM, Dees EC, O'Neil B, Orlowski RZ. 2003. The proteasome as a target for cancer therapy. Clin. Cancer Res. 9:6316-6325.
5. Adams J. 2004. The development of proteasome inhibitors as anticancer drugs. Cancer Cell 5:417-421. http://dx.doi.org/10.1016/S1535-6108(04)00120-5.
6. Orlowski RZ, Kuhn DJ. 2008. Proteasome inhibitors in cancer therapy: lessons from the first decade. Clin. Cancer Res. 14:1649-1657. http://dx.doi.org/10.1158/1078-0432.CCR-07-2218.
7. Hideshima T, Richardson P, Chauhan D, Palombella VJ, Elliott PJ, Adams J, Anderson KC. 2001. The proteasome inhibitor PS-341 inhibits growth, induces apoptosis, and overcomes drug resistance in human multiple myeloma cells. Cancer Res. 61:3071-3076.
8. Kuhn DJ, Chen Q, Voorhees PM, Strader JS, Shenk KD, Sun CM, Demo SD, Bennett MK, van Leeuwen FWB, Chanan-Khan AA, Orlowski RZ. 2007. Potent activity of carfilzomib, a novel, irreversible inhibitor of the ubiquitin-proteasome pathway, against preclinical models of multiple myeloma. Blood 110:3281-3290. http://dx.doi.org/10.1182/blood-2007-01-065888.
9. Lü S, Wang J. 2013. The resistance mechanisms of proteasome inhibitor bortezomib. Biomark Res. 1:13. http://dx.doi.org/10.1186/2050-7771-1-13.
10. Qi W, White MC, Choi W, Guo C, Dinney C, McConkey DJ, Siefker-Radtke A. 2013. Inhibition of inducible heat shock protein-70 (hsp72) enhances bortezomib-induced cell death in human bladder cancer cells. PLoS One 8:e69509. http://dx.doi.org/10.1371/journal.pone.0069509.
11. Papageorgiou A, Kamat A, Benedict WF, Dinney C, McConkey DJ. 2006. Combination therapy with IFN-alpha plus bortezomib induces apoptosis and inhibits angiogenesis in human bladder cancer cells. Mol. Cancer Ther. 5:3032-3041. http://dx.doi.org/10.1158/1535-7163.MCT-05-0474.
12. Lashinger LM, Zhu K, Williams SA, Shrader M, Dinney CPN, McConkey DJ. 2005. Bortezomib abolishes tumor necrosis factor-related apoptosis- inducing ligand resistance via a p21-dependent mechanism in human bladder and prostate cancer cells. Cancer Res. 65:4902-4908. http://dx.doi.org/10.1158/0008-5472.CAN-04-3701.
13. Codony-Servat J, Tapia MA, Bosch M, Oliva C, Domingo-Domenech J, Mellado B, Rolfe M, Ross JS, Gascon P, Rovira A, Albanell J. 2006.Differential cellular and molecular effects of bortezomib, a proteasome inhibitor, in human breast cancer cells. Mol. Cancer Ther. 5:665-675. http://dx.doi.org/10.1158/1535-7163.MCT-05-0147.
14. Ling X, Calinski D, Chanan-Khan AA, Zhou M, Li F. 2010. Cancer cell sensitivity to bortezomib is associated with survivin expression and p53 status but not cancer cell types. J. Exp. Clin. Cancer Res. 29:8. http://dx.doi.org/10.1186/1756-9966-29-8.
15. Curran MP, McKeage K. 2009. Bortezomib: a review of its use in patients with multiple myeloma. Drugs 69:859-888. http://dx.doi.org/10.2165/00003495-200969070-00006.
16. Ploeg M, Aben KKH, Kiemeney LA. 2009. The present and future burden of urinary bladder cancer in the world. World J. Urol. 27:289-293. http://dx.doi.org/10.1007/s00345-009-0383-3.
17. Siegel R, Naishadham D, Jemal A. 2012. Cancer statistics, 2012. CA Cancer J. Clin. 62:10-29. http://dx.doi.org/10.3322/caac.20138.
18. Cote RJ, Datar RH. 2003. Therapeutic approaches to bladder cancer: identifying targets and mechanisms. Crit. Rev. Oncol. Hematol. 46(Suppl.):S67-S83. http://dx.doi.org/10.1016/S1040-8428(03)00066-0.
19. Yang X, Flaig TW. 2010. Novel targeted agents for the treatment of bladder cancer: translating laboratory advances into clinical application. Int. Braz. J. Urol. 36:273-282. http://dx.doi.org/10.1590/S1677-55382010000300003.
20. Sato H, Tamba M, Ishii T, Bannai S. 1999. Cloning and expression of a plasma membrane cystine/glutamate exchange transporter composed of two distinct proteins. J. Biol. Chem. 274:11455-11458. http://dx.doi.org/10.1074/jbc.274.17.11455.
21. Lewerenz J, Hewett SJ, Huang Y, Lambros M, Gout PW, Kalivas PW, Massie A, Smolders I, Methner A, Pergande M, Smith SB, Ganapathy V, Maher P. 2013. The cystine/glutamate antiporter system x(c) (-) in health and disease: from molecular mechanisms to novel therapeutic opportunities. Antioxid. Redox Signal. 18:522-555. http://dx.doi.org/10.1089/ars.2011.4391.
22. Lo M, Wang Y-Z, Gout PW. 2008. The x(c)± cystine/glutamate antiporter: a potential target for therapy of cancer and other diseases. J. Cell. Physiol. 215:593-602. http://dx.doi.org/10.1002/jcp.21366.
23. Banjac A, Perisic T, Sato H, Seiler A, Bannai S, Weiss N, Kölle P, Tschoep K, Issels RD, Daniel PT, Conrad M, Bornkamm GW. 2008. The cystine/cysteine cycle: a redox cycle regulating susceptibility versus resistance to cell death. Oncogene 27:1618-1628. http://dx.doi.org/10.1038/sj.onc.1210796.
24. Lu SC. 2013. Glutathione synthesis. Biochim. Biophys. Acta 1830:3143-3153. http://dx.doi.org/10.1016/j.bbagen.2012.09.008.
25. Okuno S, Sato H, Kuriyama-Matsumura K, Tamba M, Wang H, Sohda S, Hamada H, Yoshikawa H, Kondo T, Bannai S. 2003. Role of cystine transport in intracellular glutathione level and cisplatin resistance in human ovarian cancer cell lines. Br. J. Cancer 88:951-956. http://dx.doi.org/10.1038/sj.bjc.6600786.
26. Huang Y, Dai Z, Barbacioru C, Sadée W. 2005. Cystine-glutamate transporter SLC7A11 in cancer chemosensitivity and chemoresistance. Cancer Res. 65:7446-7454. http://dx.doi.org/10.1158/0008-5472.CAN-04-4267.
27. Takeuchi S, Wada K, Toyooka T, Shinomiya N, Shimazaki H, Nakanishi K, Nagatani K, Otani N, Osada H, Uozumi Y, Matsuo H, Nawashiro H. 2013. Increased xCT expression correlates with tumor invasion and outcome in patients with glioblastomas. Neurosurgery 72:33-41. http: //dx.doi.org/10.1227/NEU.0b013e318276b2de.
28. Kinoshita H, Okabe H, Beppu T, Chikamoto A, Hayashi H, Imai K, Mima K, Nakagawa S, Ishimoto T, Miyake K, Yokoyama N, Ishiko T, Baba H. 2013. Cystine/glutamic acid transporter is a novel marker for predicting poor survival in patients with hepatocellular carcinoma. Oncol. Rep. 29:685-689. http://dx.doi.org/10.3892/or.2012.2162.
29. Ishimoto T, Nagano O, Yae T, Tamada M, Motohara T, Oshima H, Oshima M, Ikeda T, Asaba R, Yagi H, Masuko T, Shimizu T, Ishikawa T, Kai K, Takahashi E, Imamura Y, Baba Y, Ohmura M, Suematsu M, Baba H, Saya H. 2011. CD44 variant regulates redox status in cancer cells by stabilizing the xCT subunit of system xc(-) and thereby promotes tumor growth. Cancer Cell 19:387-400. http://dx.doi.org/10.1016/j.ccr.2011.01.038.
30. Sasaki H, Sato H, Kuriyama-Matsumura K, Sato K, Maebara K, Wang H, Tamba M, Itoh K, Yamamoto M, Bannai S. 2002. Electrophile response element-mediated induction of the cystine/glutamate exchange transporter gene expression. J. Biol. Chem. 277:44765-44771. http://dx .doi.org/10.1074/jbc.M208704200.
31. Sato H, Nomura S, Maebara K, Sato K, Tamba M, Bannai S. 2004. Transcriptional control of cystine/glutamate transporter gene by amino acid deprivation. Biochem. Biophys. Res. Commun. 325:109-116. http: //dx.doi.org/10.1016/j.bbrc.2004.10.009.
32. Zong Z-H, Du Z-X, Li N, Li C, Zhang Q, Liu B-Q, Guan Y, Wang H-Q. 2012. Implication of Nrf2 and ATF4 in differential induction of CHOP by proteasome inhibition in thyroid cancer cells. Biochim. Biophys. Acta 1823:1395-1404. http://dx.doi.org/10.1016/j.bbamcr.2012.06.001.
33. Taguchi K, Tamba M, Bannai S, Sato H. 2007. Induction of cystine/ glutamate transporter in bacterial lipopolysaccharide induced endotoxemia in mice. J. Inflamm. (London) 4:20. http://dx.doi.org/10.1186/1476-9255-4-20.
34. Dun Y, Mysona B, Van Ells T, Amarnath L, Ola MS, Ganapathy V, Smith SB. 2006. Expression of the cystine-glutamate exchanger (xc-) in retinal ganglion cells and regulation by nitric oxide and oxidative stress. Cell Tissue Res. 324:189-202. http://dx.doi.org/10.1007/s00441-005-0116-x.
35. Itoh K, Mimura J, Yamamoto M. 2010. Discovery of the negative regulator of Nrf2, Keap1: a historical overview. Antioxid. Redox Signal. 13: 1665-1678. http://dx.doi.org/10.1089/ars.2010.3222.
36. Taguchi K, Motohashi H, Yamamoto M. 2011. Molecular mechanisms of the Keap1-Nrf2 pathway in stress response and cancer evolution. Genes Cells 16:123-140. http://dx.doi.org/10.1111/j.1365-2443.2010.01473.x.
37. Lewerenz J, Sato H, Albrecht P, Henke N, Noack R, Methner A, Maher P. 2012. Mutation of ATF4 mediates resistance of neuronal cell lines against oxidative stress by inducing xCT expression. Cell Death Differ. 19:847-858. http://dx.doi.org/10.1038/cdd.2011.165.
38. Ameri K, Harris AL. 2008. Activating transcription factor 4. Int. J. Biochem. Cell Biol. 40:14-21. http://dx.doi.org/10.1016/j.biocel.2007.01.020.
39. Kilberg MS, Shan J, Su N. 2009. ATF4-dependent transcription mediates signaling of amino acid limitation. Trends Endocrinol. Metab. 20:436-443. http://dx.doi.org/10.1016/j.tem.2009.05.008.
40. Maruyama A, Mimura J, Harada N, Itoh K. 2013. Nrf2 activation is associated with Z-DNA formation in the human HO-1 promoter. Nucleic Acids Res. 41:5223-5234. http://dx.doi.org/10.1093/nar/gkt243.
41. Gout PW, Buckley AR, Simms CR, Bruchovsky N. 2001. Sulfasalazine, a potent suppressor of lymphoma growth by inhibition of the x(c)- cystine transporter: a new action for an old drug. Leukemia 15:1633-1640. http://dx.doi.org/10.1038/sj.leu.2402238.
42. Ishii T, Bannai S, Sugita Y. 1981. Mechanism of growth stimulation of L1210 cells by 2-mercaptoethanol in vitro. Role of the mixed disulfide of 2-mercaptoethanol and cysteine. J. Biol. Chem. 256:12387-12392.
43. Wu G, Fang YZ, Yang S, Lupton JR, Turner ND. 2004. Glutathione metabolism and its implications for health. J. Nutr. 134:489-492.
44. Oerlemans R, Franke NE, Assaraf YG, Cloos J, van Zantwijk I, Berkers CR, Scheffer GL, Debipersad K, Vojtekova K, Lemos C, van der Heijden JW, Ylstra B, Peters GJ, Kaspers GL, Dijkmans BAC, Scheper RJ, Jansen G. 2008. Molecular basis of bortezomib resistance: proteasome subunit beta5 (PSMB5) gene mutation and overexpression of PSMB5 protein. Blood 112:2489-2499. http://dx.doi.org/10.1182/blood-2007-08-104950.
45. Kuhn DJ, Berkova Z, Jones RJ, Woessner R, Bjorklund CC, Ma W, Davis RE, Lin P, Wang H, Madden TL, Wei C, Baladandayuthapani V, Wang M, Thomas SK, Shah JJ, Weber DM, Orlowski RZ. 2012. Targeting the insulin-like growth factor-1 receptor to overcome bortezomib resistance in preclinical models of multiple myeloma. Blood 120:3260-3270. http://dx.doi.org/10.1182/blood-2011-10-386789.
46. Chung WJ, Lyons SA, Nelson GM, Hamza H, Gladson CL, Gillespie GY, Sontheimer H. 2005. Inhibition of cystine uptake disrupts the growth of primary brain tumors. J. Neurosci. 25:7101-7110. http://dx.doi.org/10.1523/JNEUROSCI.5258-04.2005.
47. Doxsee DW, Gout PW, Kurita T, Lo M, Buckley AR, Wang Y, Xue H, Karp CM, Cutz J-C, Cunha GR, Wang Y-Z. 2007. Sulfasalazine-induced cystine starvation: potential use for prostate cancer therapy. Prostate 67: 162-171. http://dx.doi.org/10.1002/pros.20508.
48. Guo W, Zhao Y, Zhang Z, Tan N, Zhao F, Ge C, Liang L, Jia D, Chen T, Yao M, Li J, He X. 2011. Disruption of xCT inhibits cell growth via the ROS/autophagy pathway in hepatocellular carcinoma. Cancer Lett. 312: 55-61. http://dx.doi.org/10.1016/j.canlet.2011.07.024.
49. Chen R-S, Song Y-M, Zhou Z-Y, Tong T, Li Y, Fu M, Guo X-L, Dong L-J, He X, Qiao H-X, Zhan Q-M, Li W. 2009. Disruption of xCT inhibits cancer cell metastasis via the caveolin-1/beta-catenin pathway. Oncogene 28:599-609. http://dx.doi.org/10.1038/onc.2008.414.
50. Ehren JL, Maher P. 2013. Concurrent regulation of the transcriptionfactors Nrf2 and ATF4 mediates the enhancement of glutathione levels by the flavonoid fisetin. Biochem. Pharmacol. 85:1816-1826. http://dx.doi.org/10.1016/j.bcp.2013.04.010.
51. Venè R, Castellani P, Delfino L, Lucibello M, Ciriolo MR, Rubartelli A. 2011. The cystine/cysteine cycle and GSH are independent and crucial antioxidant systems in malignant melanoma cells and represent druggable targets. Antioxid. Redox Signal. 15:2439-2453. http://dx.doi.org/10.1089/ars.2010.3830.
52. Gasol E, Jiménez-Vidal M, Chillarón J, Zorzano A, Palacín M. 2004. Membrane topology of system xc-light subunit reveals a re-entrant loop with substrate-restricted accessibility. J. Biol. Chem. 279:31228-31236. http://dx.doi.org/10.1074/jbc.M402428200.
53. Siegel DS. 2013. From clinical trials to clinical practice: single-agent carfilzomib adverse events and their management in patients with relapsed and/or refractory multiple myeloma. Ther. Adv. Hematol. 4:354-365. http://dx.doi.org/10.1177/2040620713511176.
54. He CH, Gong P, Hu B, Stewart D, Choi ME, Choi AM, Alam J. 2001. Identification of activating transcription factor 4 (ATF4) as an Nrf2- interacting protein. Implication forhemeoxygenase-1 gene regulation. J. Biol. Chem. 276:20858-20865. http://dx.doi.org/10.1074/jbc.M101198200.
55. Nioi P, Nguyen T, Sherratt PJ, Pickett CB. 2005. The carboxy-terminal Neh3 domain of Nrf2 is required for transcriptional activation. Mol. Cell. Biol. 25:10895-10906. http://dx.doi.org/10.1128/MCB.25.24.10895-10906.2005.
56. Singleton DC, Harris AL. 2012. Targeting the ATF4 pathway in cancer therapy. Expert Opin. Ther. Targets 16:1189-1202. http://dx.doi.org/10.1517/14728222.2012.728207.
57. Mitsuishi Y, Motohashi H, Yamamoto M. 2012. The Keap1-Nrf2 system in cancers: stress response and anabolic metabolism. Front. Oncol. 2:200. http://dx.doi.org/10.3389/fonc.2012.00200.
58. Mitsuishi Y, Taguchi K, Kawatani Y, Shibata T, Nukiwa T, Aburatani H, Yamamoto M, Motohashi H. 2012. Nrf2 redirects glucose and glutamine into anabolic pathways in metabolic reprogramming. Cancer Cell 22:66-79. http://dx.doi.org/10.1016/j.ccr.2012.05.016.
59. Zhang Z, Yin J, Zhang C, Liang N, Bai N, Chang A, Liu Y, Li Z, Tan X, Li N, Lv D, Xiang R, Tian Y, Liu C. 2012. Activating transcription factor 4 increases chemotherapeutics resistance of human hepatocellular carcinoma. Cancer Biol. Ther. 13:435- 442. http://dx.doi.org/10.4161/cbt.19295.