ERβ decreases breast cancer cell survival by regulating the IRE1/XBP-1 pathway

Oncogene

Volumn 34, Issue 31, 2015, Pages 4130-4141

  Rajapaksa, G ^a   Nikolos, F ^a   Bado, I ^a   Clarke, R ^b   Gustafsson, J A ^a   Thomas, C ^a  

^a University of Houston   (United States)

^b GEORGETOWN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; CISPLATIN; ESTROGEN RECEPTOR BETA; FULVESTRANT; INOSITOL REQUIRING KINASE 1 ALPHA; PHOSPHOTRANSFERASE; PROTEIN BCL 2; STAUROSPORINE; UNCLASSIFIED DRUG; X BOX BINDING PROTEIN 1; DNA BINDING PROTEIN; ERN1 PROTEIN, HUMAN; PROTEIN SERINE THREONINE KINASE; REGULATORY FACTOR X TRANSCRIPTION FACTORS; RIBONUCLEASE; TRANSCRIPTION FACTOR;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; BREAST CANCER; CANCER CELL; CELL FRACTIONATION; CELL SURVIVAL; CONTROLLED STUDY; DOWN REGULATION; HUMAN; HUMAN CELL; MCF 7 CELL LINE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN TARGETING; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; UNFOLDED PROTEIN RESPONSE; UPREGULATION; BREAST TUMOR; ENDOPLASMIC RETICULUM STRESS; FEMALE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PATHOLOGY; PHYSIOLOGICAL STRESS; PHYSIOLOGY; TUMOR CELL CULTURE;

BREAST NEOPLASMS; CELL SURVIVAL; DNA-BINDING PROTEINS; DOWN-REGULATION; ENDOPLASMIC RETICULUM STRESS; ENDORIBONUCLEASES; ESTROGEN RECEPTOR BETA; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MCF-7 CELLS; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL; TRANSCRIPTION FACTORS; TUMOR CELLS, CULTURED;

EID: 84938554444     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2014.343     Document Type: Article

References (50)

1. Cancer Genome Atlas Network. Comprehensive molecular portraits of human breast tumours. Nature 2012; 490: 61-70.
2. Curtis C, Shah SP, Chin SF, Turashvili G, Rueda OM, Dunning MJ et al. The genomic and transcriptomic architecture of 2000 breast tumours reveals novel subgroups. Nature 2012; 486: 346-352.
3. Siegel R, Ma J, Zou Z, Jemal A. Cancer statistics, 2014. CA Cancer J Clin 2014; 64: 9-29.
4. Thomas C, Gustafsson JA. The different roles of ER subtypes in cancer biology and therapy. Nat Rev Cancer 2011; 11: 597-608.
5. Clarke R, Shajahan AN, Wang Y, Tyson JJ, Riggins RB, Weiner LM et al. Endoplasmic reticulum stress, the unfolded protein response, and gene network modeling in antiestrogen resistant breast cancer. Horm Mol Biol Clin Invest 2011; 5: 35-44.
6. Koong AC, Chauhan V, Romero-Ramirez L. Targeting XBP-1 as a novel anti-cancer strategy. Cancer Biol Ther 2006; 5: 756-759.
7. Ma Y, Hendershot LM. The role of the unfolded protein response in tumour development: friend or foe? Nat Rev Cancer 2004; 4: 966-977.
8. Koumenis C, Naczki C, Koritzinsky M, Rastani S, Diehl A, Sonenberg N et al. Regulation of protein synthesis by hypoxia via activation of the endoplasmic reticulum kinase PERK and phosphorylation of the translation initiation factor eIF2alpha. Mol Cell Biol 2002; 22: 7405-7416.
9. Zhang K, Kaufman RJ. The unfolded protein response: a stress signaling pathway critical for health and disease. Neurology 2006; 66: S102-S109.
10. Calfon M, Zeng H, Urano F, Till JH, Hubbard SR, Harding HP et al. IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature 2002; 415: 92-96.
11. Lee K, Tirasophon W, Shen X, Michalak M, Prywes R, Okada T et al. IRE1-mediated unconventional mRNA splicing and S2P-mediated ATF6 cleavage merge to regulate XBP1 in signaling the unfolded protein response. Genes Dev 2002; 16: 452-466.
12. Lee AH, Iwakoshi NN, Glimcher LH. XBP-1 regulates a subset of endoplasmic reticulum resident chaperone genes in the unfolded protein response. Mol Cell Biol 2003; 23: 7448-7459.
13. Yoshida H, Matsui T, Hosokawa N, Kaufman RJ, Nagata K, Mori K. A timedependent phase shift in the mammalian unfolded protein response. Dev Cell 2003; 4: 265-271.
14. Xu C, Bailly-Maitre B, Reed JC. Endoplasmic reticulum stress: cell life and death decisions. J Clin Invest 2005; 115: 2656-2664.
15. Fu Y, Li J, Lee AS. GRP78/BiP inhibits endoplasmic reticulum BIK and protects human breast cancer cells against estrogen starvation-induced apoptosis. Cancer Res 2007; 67: 3734-3740.
16. Cook KL, Shajahan AN, Warri A, Jin L, Hilakivi-Clarke LA, Clarke R. Glucoseregulated protein 78 controls cross-talk between apoptosis and autophagy to determine antiestrogen responsiveness. Cancer Res 2012; 72: 3337-3349.
17. Lee E, Nichols P, Groshen S, Spicer D, Lee AS. GRP78 as potential predictor for breast cancer response to adjuvant taxane therapy. Int J Cancer 2011; 128: 726-731.
18. Gu Z, Lee RY, Skaar TC, Bouker KB, Welch JN, Lu J et al. Association of interferon regulatory factor-1, nucleophosmin, nuclear factor-kappaB, and cyclic AMP response element binding with acquired resistance to Faslodex (ICI 182 780). Cancer Research 2002; 62: 3428-3437.
19. Gomez BP, Riggins RB, Shajahan AN, Klimach U, Wang A, Crawford AC et al. Human X-box binding protein-1 confers both estrogen independence and antiestrogen resistance in breast cancer cell lines. FASEB J Biology 2007; 21: 4013-4027.
20. Davies MP, Barraclough DL, Stewart C, Joyce KA, Eccles RM, Barraclough R et al. Expression and splicing of the unfolded protein response gene XBP-1 are significantly associated with clinical outcome of endocrine-treated breast cancer. International J Cancer 2008; 123: 85-88.
21. Sengupta S, Sharma CG, Jordan VC. Estrogen regulation of X-box binding protein-1 and its role in estrogen induced growth of breast and endometrial cancer cells. Horm Mol Biol Clin Invest 2010; 2: 235-243.
22. Ding L, Yan J, Zhu J, Zhong H, Lu Q, Wang Z et al. Ligand-independent activation of estrogen receptor alpha by XBP-1. Nucleic Acids Res 2003; 31: 5266-5274.
23. Chen X, Iliopoulos D, Zhang Q, Tang Q, Greenblatt MB, Hatziapostolou M et al. XBP1 promotes triple-negative breast cancer by controlling the HIF1alpha pathway. Nature 2014; 508: 103-107.
24. Thomas C, Rajapaksa G, Nikolos F, Hao R, Katchy A, McCollum CW et al. ERbeta1 represses basal-like breast cancer epithelial to mesenchymal transition by destabilizing EGFR. Breast Cancer Res 2012; 14: R148.
25. Honma N, Horii R, Iwase T, Saji S, Younes M, Takubo K et al. Clinical importance of estrogen receptor-beta evaluation in breast cancer patients treated with adjuvant tamoxifen therapy. J Clin Oncol 2008; 26: 3727-3734.
26. Clarke R, Cook KL, Hu R, Facey CO, Tavassoly I, Schwartz JL et al. Endoplasmic reticulum stress, the unfolded protein response, autophagy, and the integrated regulation of breast cancer cell fate. Cancer Res 2012; 72: 1321-1331.
27. Zhang B, Li H, Riggins RB, Zhan M, Xuan J, Zhang Z et al. Differential dependency network analysis to identify condition-specific topological changes in biological networks. Bioinformatics 2009; 25: 526-532.
28. Cheng L, Li J, Han Y, Lin J, Niu C, Zhou Z et al. PES1 promotes breast cancer by differentially regulating ERalpha and ERbeta. J Clin Invest 2012; 122: 2857-2870.
29. Kane RC, Dagher R, Farrell A, Ko CW, Sridhara R, Justice R et al. Bortezomib for the treatment of mantle cell lymphoma. Clin Cancer Res 2007; 13: 5291-5294.
30. Gadbois DM, Hamaguchi JR, Swank RA, Bradbury EM. Staurosporine is a potent inhibitor of p34cdc2 and p34cdc2-like kinases. Biochem Biophys Res Commun 1992; 184: 80-85.
31. Thomas CG, Strom A, Lindberg K, Gustafsson JA. Estrogen receptor beta decreases survival of p53-defective cancer cells after DNA damage by impairing G(2)/M checkpoint signaling. Breast Cancer Res Treat 2011; 127: 417-427.
32. Janicke RU, Sprengart ML, Wati MR, Porter AG. Caspase-3 is required for DNA fragmentation and morphological changes associated with apoptosis. J Biol Chem 1998; 273: 9357-9360.
33. Crawford AC, Riggins RB, Shajahan AN, Zwart A, Clarke R. Co-inhibition of BCL-W and BCL2 restores antiestrogen sensitivity through BECN1 and promotes an autophagy-associated necrosis. PLoS ONE 2010; 5: e8604.
34. Shajahan AN, Dobbin ZC, Hickman FE, Dakshanamurthy S, Clarke R. Tyrosine-phosphorylated caveolin-1 (Tyr-14) increases sensitivity to paclitaxel by inhibiting BCL2 and BCLxL proteins via c-Jun N-terminal kinase (JNK). J Biol Chem 2012; 287: 17682-17692.
35. Rodriguez DA, Zamorano S, Lisbona F, Rojas-Rivera D, Urra H, Cubillos-Ruiz JR et al. BH3-only proteins are part of a regulatory network that control the sustained signalling of the unfolded protein response sensor IRE1alpha. EMBO J 2012; 31: 2322-2335.
36. Gao B, Lee SM, Chen A, Zhang J, Zhang DD, Kannan K et al. Synoviolin promotes IRE1 ubiquitination and degradation in synovial fibroblasts from mice with collagen-induced arthritis. EMBO Rep 2008; 9: 480-485.
37. Marcu MG, Doyle M, Bertolotti A, Ron D, Hendershot L, Neckers L. Heat shock protein 90 modulates the unfolded protein response by stabilizing IRE1alpha. Mol Cell Biol 2002; 22: 8506-8513.
38. Davis AM, Mao J, Naz B, Kohl JA, Rosenfeld CS. Comparative effects of estradiol, methyl-piperidino-pyrazole, raloxifene, and ICI 182 780 on gene expression in the murine uterus. J Mol Endocrinol 2008; 41: 205-217.
39. Butler WB, Fontana JA. Responses to retinoic acid of tamoxifen-sensitive and -resistant sublines of human breast cancer cell line MCF-7. Cancer Res 1992; 52: 6164-6167.
40. Hodges-Gallagher L, Valentine CD, El Bader S, Kushner PJ. Estrogen receptor beta increases the efficacy of antiestrogens by effects on apoptosis and cell cycling in breast cancer cells. Breast Cancer Res Treat 2008; 109: 241-250.
41. Shaaban AM, Green AR, Karthik S, Alizadeh Y, Hughes TA, Harkins L et al. Nuclear and cytoplasmic expression of ERbeta1, ERbeta2, and ERbeta5 identifies distinct prognostic outcome for breast cancer patients. Clin Cancer Res 2008; 14: 5228-5235.
42. Hartman J, Edvardsson K, Lindberg K, Zhao C, Williams C, Strom A et al. Tumor repressive functions of estrogen receptor beta in SW480 colon cancer cells. Cancer Res 2009; 69: 6100-6106.
43. Nikolos F, Thomas C, Rajapaksa G, Bado I, Gustafsson JA. ERbeta regulates NSCLC phenotypes by controlling oncogenic RAS signaling. Mol Cancer Res 2014; 12: 843-854.
44. Mak P, Leav I, Pursell B, Bae D, Yang X, Taglienti CA et al. ERbeta impedes prostate cancer EMT by destabilizing HIF-1alpha and inhibiting VEGF-mediated snail nuclear localization: implications for Gleason grading. Cancer Cell 2010; 17: 319-332.
45. Yang CH, Gonzalez-Angulo AM, Reuben JM, Booser DJ, Pusztai L, Krishnamurthy S et al. Bortezomib (VELCADE) in metastatic breast cancer: pharmacodynamics, biological effects, and prediction of clinical benefits. Ann Oncol 2006; 17: 813-817.
46. Jones MD, Liu JC, Barthel TK, Hussain S, Lovria E, Cheng D et al. A proteasome inhibitor, bortezomib, inhibits breast cancer growth and reduces osteolysis by downregulating metastatic genes. Clin Cancer Res 2010; 16: 4978-4989.
47. Leung YK, Gao Y, Lau KM, Zhang X, Ho SM. ICI 182 780-regulated gene expression in DU145 prostate cancer cells is mediated by estrogen receptor-beta/NFkappaB crosstalk. Neoplasia 2006; 8: 242-249.
48. Nakajima Y, Akaogi K, Suzuki T, Osakabe A, Yamaguchi C, Sunahara N et al. Estrogen regulates tumor growth through a nonclassical pathway that includes the transcription factors ERbeta and KLF5. Sci Signal 2011; 4: ra22.
49. Butler WB, Berlinski PJ, Hillman RM, Kelsey WH, Toenniges MM. Relation of in vitro properties to tumorigenicity for a series of sublines of the human breast cancer cell line MCF-7. Cancer Res 1986; 46: 6339-6348.
50. Thomas CG, Spyrou G. ERdj5 sensitizes neuroblastoma cells to endoplasmic reticulum stress-induced apoptosis. J Biol Chem 2009; 284: 6282-6290.