The estrogen receptor cofactor SPEN functions as a tumor suppressor and candidate biomarker of drug responsiveness in hormone-dependent breast cancers

Cancer Research

Volumn 75, Issue 20, 2015, Pages 4351-4363

  Légaré, Stéphanie ^a,b   Cavallone, Luca ^b   Mamo, Aline ^b   Chabot, Catherine ^b   Sirois, Isabelle ^a,b   Magliocco, Anthony ^c   Klimowicz, Alexander ^c   Tonin, Patricia N ^d   Buchanan, Marguerite ^b   Keilty, Dana ^a,b   Hassan, Saima ^a,b   Laperrière, David ^e   Mader, Sylvie ^e,f   Aleynikova, Olga ^g   Basik, Mark ^a,b  

^a MCGILL UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c UNIVERSITY OF CALGARY   (Canada)

^d RESEARCH INSTITUTE OF THE MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

^e INSTITUTE FOR RESEARCH IN IMMUNOLOGY AND CANCER   (Canada)

^f UNIVERSITÉ DE MONTRÉAL   (Canada)

^g MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

COREPRESSOR PROTEIN; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; RNA; SPLIT ENDS PROTEIN; TAMOXIFEN; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG; ESTROGEN RECEPTOR; HOMEODOMAIN PROTEIN; NUCLEAR PROTEIN; SPEN PROTEIN, HUMAN; TUMOR MARKER;

ARTICLE; BREAST CANCER; BREAST CANCER CELL LINE; CANCER TISSUE; CELL PROLIFERATION; CELL SURVIVAL; CELL VIABILITY; CHROMATIN IMMUNOPRECIPITATION; COLONY FORMATION; COMPARATIVE GENOMIC HYBRIDIZATION; CONTROLLED STUDY; DNA MICROARRAY; DRUG RESPONSE; FLUORESCENCE ACTIVATED CELL SORTING; FLUORESCENCE MICROSCOPY; GENE EXPRESSION; GENE LOCUS; HETEROZYGOSITY LOSS; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOPRECIPITATION; IN VITRO STUDY; IN VIVO STUDY; MAJOR CLINICAL STUDY; MCF 7 CELL LINE; MICROARRAY ANALYSIS; NONSENSE MUTATION; OUTCOME ASSESSMENT; PLASMID; PRIORITY JOURNAL; RECEPTOR BINDING; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; RNA ISOLATION; SPEN GENE; T47D CELL LINE; TUMOR GROWTH; TUMOR SUPPRESSOR GENE; WESTERN BLOTTING; BREAST NEOPLASMS; CELL DEATH; COHORT ANALYSIS; DRUG RESISTANCE; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE SILENCING; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; MORTALITY; MUTATION; PROGNOSIS; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

BIOMARKERS, TUMOR; BREAST NEOPLASMS; CELL DEATH; CELL LINE, TUMOR; COHORT STUDIES; COMPARATIVE GENOMIC HYBRIDIZATION; DRUG RESISTANCE, NEOPLASM; ESTROGEN RECEPTOR ALPHA; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE KNOCKDOWN TECHNIQUES; HOMEODOMAIN PROTEINS; HUMANS; MUTATION; NUCLEAR PROTEINS; PROGNOSIS; RECEPTORS, ESTROGEN; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC; TUMOR SUPPRESSOR PROTEINS;

EID: 84945583510     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-14-3475     Document Type: Article

References (39)

1. Osborne CK, Hobbs K, Clark GM. Effect of estrogens and antiestrogens on growth of human breast cancer cells in athymic nude mice. Cancer Res 1985;45:584-90.
2. Shang Y, Hu X, DiRenzo J, Lazar MA, Brown M. Cofactor dynamics and sufficiency in estrogen receptor-regulated transcription. Cell 2000;103: 843-52.
3. Metivier R, Penot G, Hubner MR, Reid G, Brand H, Kos M, et al. Estrogen receptor-alpha directs ordered, cyclical, and combinatorial recruitment of cofactors on a natural target promoter. Cell 2003;115:751-63.
4. Robinson DR,WuYM, Vats P, Su F, Lonigro RJ, Cao X, et al. Activating ESR1 mutations in hormone-resistant metastatic breast cancer. Nat Genet 2013;45:1446-51.
5. Toy W, Shen Y,Won H, Green B, Sakr RA, Will M, et al. ESR1 ligand-binding domain mutations in hormone-resistant breast cancer. NatGenet 2013;45: 1439-45.
6. Fleming FJ, Hill AD, McDermott EW, O'Higgins NJ, Young LS. Differential recruitment of coregulator proteins steroid receptor coactivator-1 and silencing mediator for retinoid and thyroid receptors to the estrogen receptor-estrogen response element by beta-estradiol and 4-hydroxytamoxifen in human breast cancer. J Clin Endocrinol Metab 2004;89: 375-83.
7. Ring A, Dowsett M. Mechanisms of tamoxifen resistance. Endocr Relat Cancer 2004;11:643-58.
8. Doroquez DB, Orr-Weaver TL, Rebay I. Split ends antagonizes the Notch and potentiates the EGFR signaling pathways during Drosophila eye development. Mech Dev 2007;124:792-806.
9. Oswald F, Winkler M, Cao Y, Astrahantseff K, Bourteele S, KnöchelW, et al. RBP-Jkappa/SHARP recruits CtIP/CtBP corepressors to silence Notch target genes. Mol Cell Biol 2005;25:10379-90.
10. Shi Y, Downes M, Xie W, Kao HY, Ordentlich P, Tsai CC, et al. Sharp, an inducible cofactor that integrates nuclear receptor repression and activation. Genes Dev 2001;15:1140-51.
11. Ariyoshi M, Schwabe JW. A conserved structural motif reveals the essential transcriptional repression function of Spen proteins and their role in developmental signaling. Genes Dev 2003;17:1909-20.
12. Sanchez-Pulido L, Rojas AM, van Wely KH, Martinez AC, Valencia A. SPOC: a widely distributed domain associated with cancer, apoptosis and transcription. BMC Bioinformatics 2004;5:91.
13. Feng Y, Bommer GT, Zhai Y, Akyol A, Hinoi T, Winer I, et al. Drosophila split ends homologue SHARP functions as a positive regulator of Wnt/betacatenin/T-cell factor signaling in neoplastic transformation. Cancer Res 2007;67:482-91.
14. Mamo A, Cavallone L, Tuzmen S, Chabot C, Ferrario C, Hassan S, et al. An integrated genomic approach identifies ARID1A as a candidate tumorsuppressor gene in breast cancer. Oncogene 2012;31:2090-100.
15. Hosein AN, Wu M, Arcand SL, Lavallée S, Hébert J, Tonin PN, et al. Breast carcinoma-associated fibroblasts rarely contain p53 mutations or chromosomal aberrations. Cancer Res 2010;70:5770-7.
16. Tolhurst RS, Thomas RS, Kyle FJ, Patel H, Periyasamy M, Photiou A, et al. Transient over-expression of estrogen receptor-alpha in breast cancer cells promotes cell survival and estrogen-independent growth. Breast Cancer Res Treat 2011;128:357-68.
17. Mercola D, Welsh J. From mRNA to tumor suppressor. Nat Genet 2004; 36:937-8.
18. Cornen S, Adelaide J, Bertucci F, Finetti P, Guille A, Birnbaum DJ, et al. Mutations and deletions of ARID1A in breast tumors. Oncogene 2012; 31:4255-6.
19. Rhodes DR, Yu J, Shanker K, Deshpande N, Varambally R, Ghosh D, et al. ONCOMINE: a cancer microarray database and integrated data-mining platform. Neoplasia 2004;6:1-6.
20. Gao J, Aksoy BA, Dogrusoz U, Dresdner G, Gross B, Sumer SO, et al. Integrative analysis of complex cancer genomics and clinical profiles using the cBioPortal. Sci Signal 2013;6:pl1.
21. Lee KY, Lee JW,NamHJ, Shim JH, Song Y, Kang KW. PI3-kinase/p38 kinasedependent E2F1 activation is critical for Pin1 induction in tamoxifenresistant breast cancer cells. Mol Cells 2011;32:107-11.
22. Cerami E, Gao J, Dogrusoz U, Gross BE, Sumer SO, Aksoy BA, et al. The cBio cancer genomics portal: an open platform for exploring multidimensional cancer genomics data. Cancer Discov 2012;2:401-4.
23. Forbes SA, Bindal N, Bamford S, Cole C, Kok CY, Beare D, et al. COSMIC:mining complete cancer genomes in the Catalogue of Somatic Mutations in Cancer. Nucleic Acids Res 2011;39(Database issue): D945-50.
24. Gyorffy B, Lanczky A, Eklund AC, Denkert C, Budczies J, Li Q, et al. An online survival analysis tool to rapidly assess the effect of 22,277 genes on breast cancer prognosis using microarray data of 1,809 patients. Breast Cancer Res Treat 2010;123:725-31.
25. Diez J, Walter D, Munoz-Pinedo C, Gabaldon T. DeathBase: a database on structure, evolution and function of proteins involved in apoptosis and other forms of cell death. Cell Death Differ 2010; 17:735-6.
26. Joseph R, Orlov YL, Huss M, Sun W, Kong SL, Ukil L, et al. Integrativemodel of genomic factors for determining binding site selection by estrogen receptor-alpha. Mol Systems Biol 2010;6:456.
27. Grober OM, Mutarelli M, Giurato G, Ravo M, Cicatiello L, De Filippo MR, et al. Global analysis of estrogen receptor beta binding to breast cancer cell genome reveals an extensive interplay with estrogen receptor alpha for target gene regulation. BMC Genomics 2011;12:36.
28. Fury W, Batliwalla F, Gregersen PK, Li W. Overlapping probabilities of top ranking gene lists, hypergeometric distribution, and stringency of gene selection criterion. Conf Proc IEEE Eng Med Biol Soc 2006; 1:5531-4.
29. Bourdeau V, Deschenes J, Laperriere D, Aid M, White JH, Mader S. Mechanisms of primary and secondary estrogen target gene regulation in breast cancer cells. Nucleic Acids Res 2008;36:76-93.
30. Mihaly Z, Kormos M, Lanczky A, Dank M, Budczies J, Szász MA, et al. A meta-analysis of gene expression-based biomarkers predicting outcome after tamoxifen treatment in breast cancer. Breast Cancer Res Treat 2013; 140:219-32.
31. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011;144:646-74.
32. Arpino G, Green SJ, Allred DC, Lew D, Martino S, Osborne CK, et al. HER-2 amplification, HER-1 expression, and tamoxifen response in estrogen receptor-positive metastatic breast cancer: a southwest oncology group study. Clin Cancer Res 2004;10:5670-6.
33. Campbell RA, Bhat-Nakshatri P, Patel NM, Constantinidou D, Ali S, Nakshatri H. Phosphatidylinositol 3-kinase/AKT-mediated activation of estrogen receptor alpha: a new model for anti-estrogen resistance. J Biol Chem 2001;276:9817-24.
34. Larsen MS, Bjerre K, Lykkesfeldt AE, Giobbie-Hurder A, Laenkholm AV, Henriksen KL, et al. Activated HER-receptors in predicting outcome of ERpositive breast cancer patients treated with adjuvant endocrine therapy. Breast 2012;21:662-8.
35. Yamashita H, Nishio M, Kobayashi S, Ando Y, Sugiura H, Zhang Z, et al. Phosphorylation of estrogen receptor alpha serine 167 is predictive of response to endocrine therapy and increases postrelapse survival in metastatic breast cancer. Breast Cancer Res 2005;7:R753-64.
36. O'Connor PM, Jackman J, Bae I, Myers TG, Fan S, Mutoh M, et al. Characterization of the p53 tumor suppressor pathway in cell lines of the National Cancer Institute anticancer drug screen and correlations with the growth-inhibitory potency of 123 anticancer agents. Cancer Res 1997;57:4285-300.
37. Janicke RU. MCF-7 breast carcinoma cells do not express caspase-3. Breast Cancer Res Treat 2009;117:219-21.
38. Hur J, Chesnes J, Coser KR, Lee RS, Geck P, Isselbacher KJ, et al. The Bik BH3-only protein is induced in estrogen-starved and antiestrogen-exposed breast cancer cells and provokes apoptosis. Proc Natl Acad Sci U S A 2004;101:2351-6.
39. Perillo B, Sasso A, Abbondanza C, Palumbo G. 17beta-estradiol inhibits apoptosis in MCF-7 cells, inducing bcl-2 expression via two estrogenresponsive elements present in the coding sequence. Mol Cell Biol 2000;20:2890-901.