Expression of oestrogen receptor β isoforms is regulated by transcriptional and post-transcriptional mechanisms

Biochemical Journal

Volumn 429, Issue 2, 2010, Pages 283-290

  Smith, Laura ^a   Coleman, Louise J ^a   Cummings, Michele ^a   Satheesha, Sampoorna ^a   Shaw, Spencer O ^a   Speirs, Valerie ^a   Hughes, Thomas A ^a  

^a UNIVERSITY OF LEEDS   (United Kingdom)

Author keywords

Breast tissue; Differential polyadenylation; Esr2; Oestrogen receptor (ER); Translational regulation; Untranslated region (UTR)

Indexed keywords

BREAST TISSUES; OESTROGEN RECEPTORS; POLYADENYLATION; TRANSLATIONAL REGULATION; UNTRANSLATED REGIONS;

TISSUE;

ESTROGEN RECEPTOR BETA; ESTRADIOL; ISOPROTEIN; MESSENGER RNA; RNA;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; ARTICLE; CELL STRAIN MCF 7; CONTROLLED STUDY; HUMAN; HUMAN CELL; MOLECULAR INTERACTION; PRIORITY JOURNAL; REGULATORY RNA SEQUENCE; TRANSLATION REGULATION; ALTERNATIVE RNA SPLICING; BREAST TUMOR; DRUG EFFECT; FEMALE; GENETIC TRANSCRIPTION; GENETIC TRANSFECTION; GENETICS; METABOLISM; NEOPLASM; PROMOTER REGION; PROTEIN SYNTHESIS; REPORTER GENE; RNA PROCESSING; TUMOR CELL LINE;

3' UNTRANSLATED REGIONS; 5' UNTRANSLATED REGIONS; ALTERNATIVE SPLICING; BREAST NEOPLASMS; CELL LINE, TUMOR; ESTRADIOL; ESTROGEN RECEPTOR BETA; FEMALE; GENES, REPORTER; HUMANS; NEOPLASMS, HORMONE-DEPENDENT; PROMOTER REGIONS, GENETIC; PROTEIN BIOSYNTHESIS; PROTEIN ISOFORMS; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, MESSENGER; RNA, NEOPLASM; TRANSCRIPTION, GENETIC; TRANSFECTION;

EID: 77954712607     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20100373     Document Type: Article

References (40)

1. Chen, G. G., Zeng, Q. and Tse, G. M. (2008) Estrogen and its receptors in cancer. Med. Res. Rev. 28, 954-974
2. O'Neill, P. A., Davies, M. P., Shaaban, A. M., Innes, H., Torevell, A., Sibson, D. R. and Foster, C. S. (2004) Wild-type oestrogen receptor β (ERβ1) mRNA and protein expression in Tamoxifen-treated post-menopausal breast cancers. Br. J. Cancer. 91, 1694-1702
3. Green, C. A., Peter, M. B., Speirs, V. and Shaaban, A. M. (2008) The potential role of ERβ isoforms in the clinical management of breast cancer. Histopathology 53, 374-380
4. Moore, J. T., McKee, D. D., Slentz-Kesler, K., Moore, L. B., Jones, S. A., Horne, E. L., Su, J. L., Kliewer, S. A., Lehmann, J. M. and Willson, T. M. (1998) Cloning and characterization of human estrogen receptor β isoforms. Biochem. Biophys. Res. Commun. 247, 75-78
5. Shaaban, A. M., Green, A. R., Karthik, S., Alizadeh, Y., Hughes, T. A., Harkins, L., Ellis, I. O., Robertson, J. F., Paish, E. C., Saunders, P. T. et al. (2008) Nuclear and cytoplasmic expression of ERβ1, ERβ2, and ERβ5 identifies distinct prognostic outcome for breast cancer patients. Clin. Cancer Res. 14, 5228-5235
6. Honma, N., Horii, R., Iwase, T., Saji, S., Younes, M., Takubo, K., Matsuura, M., Ito, Y., Akiyama, F. and Sakamoto, G. (2008) Clinical importance of estrogen receptor-β evaluation in breast cancer patients treated with adjuvant tamoxifen therapy. J. Clin. Oncol. 26, 3727-3734
7. Novelli, F., Milella, M., Melucci, E., Di Benedetto, A., Sperduti, I., Perrone-Donnorso, R., Perracchio, L., Venturo, I., Nistico, C., Fabi, A. et al. (2008) A divergent role for estrogen receptor-β in node-positive and node-negative breast cancer classified according to molecular subtypes: an observational prospective study. Breast Cancer Res. 10, R74
8. Vinayagam, R., Sibson, D. R., Holcombe, C., Aachi, V. and Davies, M. P. (2007) Association of oestrogen receptor β2 (ERβ2/ERβcx) with outcome of adjuvant endocrine treatment for primary breast cancer: a retrospective study. BMC Cancer 7, 131
9. Skliris, G. P., Munot, K., Bell, S. M., Carder, P. J., Lane, S., Horgan, K., Lansdown, M. R., Parkes, A. T., Hanby, A. M., Markham, A. F. and Speirs, V. (2003) Reduced expression of oestrogen receptor β in invasive breast cancer and its re-expression using DNA methyl transferase inhibitors in a cell line model. J. Pathol. 201, 213-220
10. Shaaban, A. M., O'Neill, P. A., Davies, M. P., Sibson, R., West, C. R., Smith, P. H. and Foster, C. S. (2003) Declining estrogen receptor-β expression defines malignant progression of human breast neoplasia. Am. J. Surg. Pathol. 27, 1502-1512
11. Bardin, A., Boulle, N., Lazennec, G., Vignon, F. and Pujol, P. (2004) Loss of ER?β expression as a common step in estrogen-dependent tumor progression. Endocr. Relat. Cancer 11, 537-551
12. Lazennec, G. (2006) Estrogen receptor β, a possible tumor suppressor involved in ovarian carcinogenesis. Cancer Lett. 231, 151-157
13. Galluzzo, P., Caiazza, F., Moreno, S. and Marino, M. (2007) Role of ERβ palmitoylation in the inhibition of human colon cancer cell proliferation. Endocr. Relat. Cancer 14, 153-167
14. Esslimani-Sahla, M., Kramar, A., Simony-Lafontaine, J., Warner, M., Gustafsson, J.-Å. and Rochefort, H. (2005) Increased estrogen receptor βcx expression during mammary carcinogenesis. Clin. Cancer Res. 11, 3170-3174
15. Park, B. W., Kim, K. S., Heo, M. K., Yang, W. I., Kim, S. I., Kim, J. H., Kim, G. E. and Lee, K. S. (2006) The changes of estrogen receptor-β variants expression in breast carcinogenesis: decrease of estrogen receptor-β2 expression is the key event in breast cancer development. J. Surg. Oncol. 93, 504-510
16. Smith, L., Brannan, R. A., Hanby, A. M., Shaaban, A. M., Verghese, E. T., Peter, M., Pollock, S., Satheesha, S., Szynkiewicz, M., Speirs, V. and Hughes, T. A. (2009) Differential regulation of estrogen receptor β isoforms by 5′ untranslated regions in cancer. J. Cell. Mol. Med., doi:10.1111/j.1582-4934.2009.00867.x
17. Hughes, T. A. and Brady, H. J. M. (2005) Cross-talk between pRb/E2F and Wnt/β-catenin pathways: E2F1 induces axin2 leading to repression of Wnt signalling and to increased cell death. Exp. Cell Res. 303, 32-46
18. Akamine, R., Yamamoto, T., Watanabe, M., Yamazaki, N., Kataoka, M., Ishikawa, M., Ooie, T., Baba, Y. and Shinohara, Y. (2007) Usefulness of the 5′ region of the cDNA encoding acidic ribosomal phosphoprotein P0 conserved among rats, mice, and humans as a standard probe for gene expression analysis in different tissues and animal species. J. Biochem. Biophys. Methods 70, 481-486
19. Zuker, M. (2003) Mfold web server for nucleic acid folding and hydrization prediction. Nucleic Acids Res. 31, 3406-3415
20. Hirata, S., Shoda, T., Kato, J. and Hoshi, K. (2001) The multiple untranslated first exons system of the human estrogen receptor β (ERβ) gene. J. Steroid Biochem. Mol. Biol. 78, 33-40
21. Hughes, T. A. and Brady, H. J. M. (2005) Expression of axin2 is regulated by the alternative 5′ untranslated regions of its mRNA. J. Biol. Chem. 280, 8581-8588
22. Catanuto, P., Doublier, S., Lupia, E., Fornoni, A., Berho, M., Karl, M., Striker, G. E., Xia, X. and Elliot, S. (2009) 17β-Estradiol and tamoxifen upregulate estrogen receptor β expression and control podocyte signaling pathways in a model of type 2 diabetes. Kidney Int. 75, 1194-1201
23. Montanaro, D., Maggiolini, M., Recchia, A. G., Sirianni, R., Aquila, S., Barzon, L., Fallo, F., Ando, S. and Pezzi, V. (2005) Antiestrogens upregulate estrogen receptor β expression and inhibit adrenocortical H295R cell proliferation. J. Mol. Endocrinol. 35, 245-256
24. Caiazza, F., Galluzzo, P., Lorenzetti, S. and Marino, M. (2007) 17β-Estradiol induces ERβ up-regulation via p38/MAPK activation in colon cancer cells. Biochem. Biophys. Res. Commun. 359, 102-107
25. Ogawa, S., Inoue, S., Watanabe, T., Hiroi, H., Orimo, A., Hosoi, T., Ouchi, Y. and Muramatsu, M. (1998) The complete primary structure of human estrogen receptor β (hERβ) and its heterodimerization with ERα in vivoand in vitro. Biochem. Biophys. Res. Commun. 243, 122-126
26. Zhao, C., Dahlman-Wright, K. and Gustafsson, J.-Å. (2008) Estrogen receptor β: an overview and update. Nucl. Recept. Signaling 6, e003
27. Xue, Q., Lin, Z., Cheng, Y. H., Huang, C. C., Marsh, E., Yin, P., Milad, M. P., Confino, E., Reierstad, S., Innes, J. and Bulun, S. E. (2007) Promoter methylation regulates estrogen receptor 2 in human endometrium and endometriosis. Biol. Reprod. 77, 681-687
28. Zhang, X., Leung, Y. K. and Ho, S. M. (2007) AP-2 regulates the transcription of estrogen receptor (ER)-β by acting through a methylation hotspot of the 0N promoter in prostate cancer cells. Oncogene 26, 7346-7354
29. Zhao, C., Lam, E. W., Sunters, A., Enmark, E., De Bella, M. T., Coombes, R. C., Gustafsson, J.-Å. and Dahlman-Wright, K. (2003) Expression of estrogen receptor β isoforms in normal breast epithelial cells and breast cancer: regulation by methylation. Oncogene 22, 7600-7606
30. Suzuki, F., Akahira, J. I., Miura, I., Suzuki, T., Ito, K., Hayashi, S. I., Sasano, H. and Yaegashi, N. (2008) Loss of estrogen receptor β isoform expression and its correlation with aberrant DNA methylation of the 5′-untranslated region in human epithelial ovarian carcinoma. Cancer Sci. 99, 2365-2372
31. Roger, P., Sahla, M. E., Makela, S., Gustafsson, J.-Å., Baldet, P. and Rochefort, H. (2001) Decreased expression of estrogen receptor β protein in proliferative preinvasive mammary tumors. Cancer Res. 61, 2537-2541
32. Al-Nakhle, H. H., Smith, L., Hughes, T. A., Cummings, M., Hanby, A. M., Shaaban, A. M., Burns, P. A. and Speirs, V. (2009) Methylation status of promoters 0K, 0N and a newly identified promoter regulate ERβ1 expression in breast cancer. Cancer Res. 69, 585S-586S
33. Cheng, S. and Gallie, D. R. (2007) eIF4G, eIFiso4G, and eIF4B bind the poly(A)-binding protein through overlapping sites within the RNA recognition motif domains. J. Biol. Chem. 282, 25247-25258
34. Komarova, A. V., Brocard, M. and Kean, K. M. (2006) The case for mRNA 5′ and 3′ end cross talk during translation in a eukaryotic cell. Prog. Nucleic Acid. Res. Mol. Biol. 81, 331-367
35. Sandberg, R., Neilson, J. R., Sarma, A., Sharp, P. A. and Burge, C. B. (2008) Proliferating cells express mRNAs with shortened 3′ untranslated regions and fewer microRNA target sites. Science 320, 1643-1647
36. Mayr, C. and Bartel, D. P. (2009) Widespread shortening of 3′UTRs by alternative cleavage and polyadenylation activates oncogenes in cancer cells. Cell 138, 673-684
37. Rody, A., Holtrich, U., Solbach, C., Kourtis, K., von Minckwitz, G., Engels, K., Kissler, S., Gatje, R., Karn, T. and Kaufmann, M. (2005) Methylation of estrogen receptor ′ promoter correlates with loss of ER-′ expression in mammary carcinoma and is an early indication marker in premalignant lesions. Endocr. Relat. Cancer 12, 903-916
38. Bhat-Nakshatri, P., Wang, G., Collins, N. R., Thomson, M. J., Geistlinger, T. R., Carroll, J. S., Brown, M., Hammond, S., Srour, E. F., Liu, Y. and Nakshatri, H. (2009) Estradiol-regulated microRNAs control estradiol response in breast cancer cells. Nucleic Acids Res. 37, 4850-4861
39. Maillot, G., Lacroix-Triki, M., Pierredon, S., Gratadou, L., Schmidt, S., Benes, V., Roche, H., Dalenc, F., Auboeuf, D., Millevoi, S. and Vagner, S. (2009) Widespread estrogen-dependent repression of micrornas involved in breast tumor cell growth. Cancer Res. 69, 8332-8340
40. Al-Nakhle, H., Burns, P. A., Cummings, M., Hanby, A. M., Hughes, T. A., Satheesha, S., Shaaban, A. M., Smith, L. and Speirs, V. (2010) Estrogen receptor ′1 expression is regulated by miR-92 in breast cancer. Cancer Res. 70, 4778-4784