miR-22 inhibits estrogen signaling by directly targeting the estrogen receptor α mRNA

Molecular and Cellular Biology

Volumn 29, Issue 13, 2009, Pages 3783-3790

  Pandey, Deo Prakash ^a   Picard, Didier ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ESTROGEN; ESTROGEN RECEPTOR ALPHA; MESSENGER RNA; MICRORNA; UNTRANSLATED RNA;

3' UNTRANSLATED REGION; ARTICLE; BREAST CANCER; CELL PROLIFERATION; GENE OVEREXPRESSION; GENETIC CONSERVATION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN TARGETING; REGULATORY MECHANISM; RNA DEGRADATION; RNA STABILITY; RNA TRANSLATION; SIGNAL TRANSDUCTION;

3' UNTRANSLATED REGIONS; ANIMALS; BASE SEQUENCE; BREAST NEOPLASMS; CELL LINE; ESTROGEN RECEPTOR ALPHA; ESTROGENS; FEMALE; HUMANS; MICRORNAS; MOLECULAR SEQUENCE DATA; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION;

EID: 67650135755     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.01875-08     Document Type: Article

References (59)

1. Adams, B. D., H. Furneaux, and B. A. White. 2007. The micro-ribonucleic acid (miRNA) miR-206 targets the human estrogen receptor-α (ERα) and represses ERα messenger RNA and protein expression in breast cancer cell lines. Mol. Endocrinol. 21:1132-1147.
2. Ali, S., and R. C. Coombes. 2002. Endocrine-responsive breast cancer and strategies for combating resistance. Nat. Rev. Cancer 2:101-112.
3. Ambs, S., R. L. Prueitt, M. Yi, R. S. Hudson, T. M. Howe, F. Petrocca, T. A. Wallace, C. G. Liu, S. Volinia, G. A. Calin, H. G. Yfantis, R. M. Stephens, and C. M. Croce. 2008. Genomic profiling of microRNA and messenger RNA reveals deregulated microRNA expression in prostate cancer. Cancer Res. 68:6162-6170.
4. Baek, D., J. Villen, C. Shin, F. D. Camargo, S. P. Gygi, and D. P. Bartel. 2008. The impact of microRNAs on protein output. Nature 455:64-71.
5. Bartel, D. P. 2004. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116:281-297.
6. Bartel, D. P. 2009. MicroRNAs: target recognition and regulatory functions. Cell 136:215-233.
7. Bentwich, I., A. Avniel, Y. Karov, R. Aharonov, S. Gilad, O. Barad, A. Barzilai, P. Einat, U. Einav, E. Meiri, E. Sharon, Y. Spector, and Z. Bentwich. 2005. Identification of hundreds of conserved and nonconserved human microRNAs. Nat. Genet. 37:766-770.
8. Berezikov, E., V. Guryev, J. van de Belt, E. Wienholds, R. H. Plasterk, and E. Cuppen. 2005. Phylogenetic shadowing and computational identification of human microRNA genes. Cell 120:21-24.
9. Bookout, A. L., Y. Jeong, M. Downes, R. T. Yu, R. M. Evans, and D. J. Mangelsdorf. 2006. Anatomical profiling of nuclear receptor expression reveals a hierarchical transcriptional network. Cell 126:789-799.
10. Brummelkamp, T. R., R. Bernards, and R. Agami. 2002. A system for stable expression of short interfering RNAs in mammalian cells. Science 296:550-553.
11. Bunone, G., P.-A. Briand, R. J. Miksicek, and D. Picard. 1996. Activation of the unliganded estrogen receptor by EGF involves the MAP kinase pathway and direct phosphorylation. EMBO J. 15:2174-2183.
12. Calin, G. A., and C. M. Croce. 2006. MicroRNA signatures in human cancers. Nat. Rev. Cancer 6:857-866.
13. Carroll, J. S., C. A. Meyer, J. Song, W. Li, T. R. Geistlinger, J. Eeckhoute, A. S. Brodsky, E. K. Keeton, K. C. Fertuck, G. F. Hall, Q. Wang, S. Bekiranov, V. Sementchenko, E. A. Fox, P. A. Silver, T. R. Gingeras, X. S. Liu, and M. Brown. 2006. Genome-wide analysis of estrogen receptor binding sites. Nat. Genet. 38:1289-1297.
14. Chang, T. C., D. Yu, Y. S. Lee, E. A. Wentzel, D. E. Arking, K. M. West, C. V. Dang, A. Thomas-Tikhonenko, and J. T. Mendell. 2008. Widespread microRNA repression by Myc contributes to tumorigenesis. Nat. Genet. 40:43-50.
15. Donzé, O., and D. Picard. 2002. RNA interference in mammalian cells using siRNAs synthesized with T7 RNA polymerase. Nucleic Acids Res. 30:e46.
16. Farh, K. K., A. Grimson, C. Jan, B. P. Lewis, W. K. Johnston, L. P. Lim, C. B. Burge, and D. P. Bartel. 2005. The widespread impact of mammalian MicroRNAs on mRNA repression and evolution. Science 310:1817-1821.
17. Filipowicz, W., S. N. Bhattacharyya, and N. Sonenberg. 2008. Mechanisms of post-transcriptional regulation by microRNAs: are the answers in sight? Nat. Rev. Genet. 9:102-114.
18. Gaur, A., D. A. Jewell, Y. Liang, D. Ridzon, J. H. Moore, C. Chen, V. R. Ambros, and M. A. Israel. 2007. Characterization of microRNA expression levels and their biological correlates in human cancer cell lines. Cancer Res. 67:2456-2468.
19. Giacinti, L., P. P. Claudio, M. Lopez, and A. Giordano. 2006. Epigenetic information and estrogen receptor alpha expression in breast cancer. Oncologist 11:1-8.
20. Griffiths-Jones, S., H. K. Saini, S. van Dongen, and A. J. Enright. 2008. miRBase: tools for microRNA genomics. Nucleic Acids Res. 36:D154-D158.
21. Grimson, A., K. K. Farh, W. K. Johnston, P. Garrett-Engele, L. P. Lim, and D. P. Bartel. 2007. MicroRNA targeting specificity in mammals: determinants beyond seed pairing. Mol. Cell 27:91-105.
22. Hammes, S. R., and E. R. Levin. 2007. Extranuclear steroid receptors: nature and actions. Endocr. Rev. 28:726-741.
23. Heldring, N., A. Pike, S. Andersson, J. Matthews, G. Cheng, J. Hartman, M. Tujague, A. Strom, E. Treuter, M. Warner, and J.-Å. Gustafsson. 2007. Estrogen receptors: how do they signal and what are their targets. Physiol. Rev. 87:905-931.
24. Herynk, M. H., and S. A. Fuqua. 2007. Estrogen receptors in resistance to hormone therapy. Adv. Exp. Med. Biol. 608:130-143.
25. Ibarra, I., Y. Erlich, S. K. Muthuswamy, R. Sachidanandam, and G. J. Hannon. 2007. A role for microRNAs in maintenance of mouse mammary epithelial progenitor cells. Genes Dev. 21:3238-3243.
26. Ing, N. H. 2005. Steroid hormones regulate gene expression posttranscriptionally by altering the stabilities of messenger RNAs. Biol. Reprod. 72: 1290-1296.
27. Ing, N. H., D. A. Massuto, and L. A. Jaeger. 2008. Estradiol up-regulates AUF1p45 binding to stabilizing regions within the 3′-untranslated region of estrogen receptor α mRNA. J. Biol. Chem. 283:1764-1772.
28. Iorio, M. V., M. Ferracin, C. G. Liu, A. Veronese, R. Spizzo, S. Sabbioni, E. Magri, M. Pedriali, M. Fabbri, M. Campiglio, S. Menard, J. P. Palazzo, A. Rosenberg, P. Musiani, S. Volinia, I. Nenci, G. A. Calin, P. Querzoli, M. Negrini, and C. M. Croce. 2005. MicroRNA gene expression deregulation in human breast cancer. Cancer Res. 65:7065-7070.
29. Iorio, M. V., R. Visone, G. Di Leva, V. Donati, F. Petrocca, P. Casalini, C. Taccioli, S. Volinia, C. G. Liu, H. Alder, G. A. Calin, S. Menard, and C. M. Croce. 2007. MicroRNA signatures in human ovarian cancer. Cancer Res. 67:8699-8707.
30. John, B., A. J. Enright, A. Aravin, T. Tuschl, C. Sander, and D. S. Marks. 2004. Human MicroRNA targets. PLoS Biol. 2:e363.
31. Kalkhoven, E., E. Beraldi, M. L. Panno, J. P. De Winter, J. H. Thijssen, and B. Van Der Burg. 1996. Growth inhibition by anti-estrogens and progestins in TGF-β-resistant and -sensitive breast-tumor cells. Int. J. Cancer 65:682-687.
32. Kenealy, M. R., G. Flouriot, V. Sonntag-Buck, T. Dandekar, H. Brand, and F. Gannon. 2000. The 3′-untranslated region of the human estrogen receptor α gene mediates rapid messenger ribonucleic acid turnover. Endocrinology 141:2805-2813.
33. Kondo, N., T. Toyama, H. Sugiura, Y. Fujii, and H. Yamashita. 2008. miR-206 expression is down-regulated in estrogen receptor α-positive human breast cancer. Cancer Res. 68:5004-5008.
34. Krek, A., D. Grun, M. N. Poy, R. Wolf, L. Rosenberg, E. J. Epstein, P. MacMenamin, I. da Piedade, K. C. Gunsalus, M. Stoffel, and N. Rajewsky. 2005. Combinatorial microRNA target predictions. Nat. Genet. 37:495-500.
35. Lakkaraju, A. K., P. P. Luyet, P. Parone, T. Falguieres, and K. Strub. 2007. Inefficient targeting to the endoplasmic reticulum by the signal recognition particle elicits selective defects in post-ER membrane trafficking. Exp. Cell Res. 313:834-847.
36. Landgraf, P., et al. 2007. A mammalian microRNA expression atlas based on small RNA library sequencing. Cell 129:1401-1414.
37. Lewis, B. P., C. B. Burge, and D. P. Bartel. 2005. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120:15-20.
38. Lewis, B. P., I. H. Shih, M. W. Jones-Rhoades, D. P. Bartel, and C. B. Burge. 2003. Prediction of mammalian microRNA targets. Cell 115:787-798.
39. Liang, Y., D. Ridzon, L. Wong, and C. Chen. 2007. Characterization of microRNA expression profiles in normal human tissues. BMC Genomics 8:166.
40. Liu, W.-H., S.-H. Yeh, C.-C. Lu, S.-L. Yu, H.-Y. Chen, C.-Y. Lin, D.-S. Chen, and P.-J. Chen. 2009. microRNA-18a prevents estrogen receptor-α expression, promoting proliferation of hepatocellular carcinoma cells. Gastroenterology 136:683-693.
41. Matthews, J., B. Wihlen, J. Thomsen, and J.-Å. Gustafsson. 2005. Aryl hydrocarbon receptor-mediated transcription: ligand-dependent recruitment of estrogen receptor α to 2,3,7,8-tetrachlorodibenzo-p- dioxin-responsive promoters. Mol. Cell. Biol. 25:5317-5328.
42. Mattie, M. D., C. C. Benz, J. Bowers, K. Sensinger, L. Wong, G. K. Scott, V. Fedele, D. Ginzinger, R. Getts, and C. Haqq. 2006. Optimized high-throughput microRNA expression profiling provides novel biomarker assessment of clinical prostate and breast cancer biopsies. Mol. Cancer 5:24.
43. Miller, T. E., K. Ghoshal, B. Ramaswamy, S. Roy, J. Datta, C. L. Shapiro, S. Jacob, and S. Majumder. 2008. MicroRNA-221/222 confers tamoxifen resistance in breast cancer by targeting p27Kip1. J. Biol. Chem. 283:29897-29903.
44. Nawaz, Z., D. M. Lonard, A. P. Dennis, C. L. Smith, and B. W. O'Malley. 1999. Proteasome-dependent degradation of the human estrogen receptor. Proc. Natl. Acad. Sci. USA 96:1858-1862.
45. Parone, P. A., D. I. James, S. Da Cruz, Y. Mattenberger, O. Donze, F. Barja, and J. C. Martinou. 2006. Inhibiting the mitochondrial fission machinery does not prevent Bax/Bak-dependent apoptosis. Mol. Cell. Biol. 26:7397-7408.
46. Pillai, R. S., S. N. Bhattacharyya, and W. Filipowicz. 2007. Repression of protein synthesis by miRNAs: how many mechanisms? Trends Cell Biol. 17:118-126.
47. Place, R. F., L. C. Li, D. Pookot, E. J. Noonan, and R. Dahiya. 2008. MicroRNA-373 induces expression of genes with complementary promoter sequences. Proc. Natl. Acad. Sci. USA 105:1608-1613.
48. Reid, G., S. Denger, M. Kos, and F. Gannon. 2002. Human estrogen receptor-α: regulation by synthesis, modification and degradation. Cell. Mol. Life Sci. 59:821-831.
49. Saceda, M., M. E. Lippman, P. Chambon, R. L. Lindsey, M. Ponglikitmongkol, M. Puente, and M. B. Martin. 1988. Regulation of the estrogen receptor in MCF-7 cells by estradiol. Mol. Endocrinol. 2:1157-1162.
50. Selbach, M., B. Schwanhausser, N. Thierfelder, Z. Fang, R. Khanin, and N. Rajewsky. 2008. Widespread changes in protein synthesis induced by microRNAs. Nature 455:58-63.
51. Sempere, L. F., M. Christensen, A. Silahtaroglu, M. Bak, C. V. Heath, G. Schwartz, W. Wells, S. Kauppinen, and C. N. Cole. 2007. Altered MicroRNA expression confined to specific epithelial cell subpopulations in breast cancer. Cancer Res. 67:11612-11620.
52. Sleeman, K. E., H. Kendrick, D. Robertson, C. M. Isacke, A. Ashworth, and M. J. Smalley. 2007. Dissociation of estrogen receptor expression and in vivo stem cell activity in the mammary gland. J. Cell Biol. 176:19-26.
53. Stark, A., J. Brennecke, N. Bushati, R. B. Russell, and S. M. Cohen. 2005. Animal MicroRNAs confer robustness to gene expression and have a significant impact on 3′UTR evolution. Cell 123:1133-1146.
54. Sun, M., Z. Estrov, Y. Ji, K. R. Coombes, D. H. Harris, and R. Kurzrock. 2008. Curcumin (diferuloylmethane) alters the expression profiles of microRNAs in human pancreatic cancer cells. Mol. Cancer Ther. 7:464-473.
55. Vasudevan, S., and J. A. Steitz. 2007. AU-rich-element-mediated upregulation of translation by FXR1 and Argonaute 2. Cell 128:1105-1118.
56. Vasudevan, S., Y. Tong, and J. A. Steitz. 2007. Switching from repression to activation: microRNAs can up-regulate translation. Science 318:1931-1934.
57. Verghese, E. T., A. M. Hanby, V. Speirs, and T. A. Hughes. 2008. Small is beautiful: microRNAs and breast cancer-where are we now? J. Pathol. 215:214-221.
58. Yanaihara, N., N. Caplen, E. Bowman, M. Seike, K. Kumamoto, M. Yi, R. M. Stephens, A. Okamoto, J. Yokota, T. Tanaka, G. A. Calin, C. G. Liu, C. M. Croce, and C. C. Harris. 2006. Unique microRNA molecular profiles in lung cancer diagnosis and prognosis. Cancer Cell 9:189-198.
59. Zhao, J. J., J. Lin, H. Yang, W. Kong, L. He, X. Ma, D. Coppola, and J. Q. Cheng. 2008. MicroRNA-221/222 negatively regulates estrogen receptor α and is associated with tamoxifen resistance in breast cancer. J. Biol. Chem. 283:31079-31086.