Effects of oestrogen on microRNA expression in hormone-responsive breast cancer cells

Hormones and Cancer

Volumn 3, Issue 3, 2012, Pages 65-78

  Ferraro, Lorenzo ^a,b   Ravo, Maria ^a   Nassa, Giovanni ^a   Tarallo, Roberta ^a   de Filippo, Maria Rosaria ^c   Giurato, Giorgio ^a   Cirillo, Francesca ^b   Stellato, Claudia ^a   Silvestro, Silvana ^a   Cantarella, Concita ^a   Rizzo, Francesca ^a   Cimino, Daniela ^d   Friard, Olivier ^d   Biglia, Nicoletta ^d   de Bortoli, Michele ^d   Cicatiello, Luigi ^b   Nola, Ernesto ^b   Weisz, Alessandro ^a,b  

^a UNIVERSITY OF SALERNO   (Italy)

^b SECOND UNIVERSITY OF NAPLES   (Italy)

^c IRCCS SDN   (Italy)

^d UNIVERSITY OF TURIN   (Italy)

Author keywords

Breast cancer; Cell cycle; Gene expression; MicroRNA; Oestrogen receptor

Indexed keywords

ESTRADIOL; ESTROGEN RECEPTOR ALPHA; MESSENGER RNA; MICRORNA;

ADULT; AGED; ARTICLE; BREAST CANCER; CELL STRAIN MCF 7; CELL STRAIN ZR 75.1; CLINICAL ARTICLE; DNA BINDING; ESTROGEN ACTIVITY; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; ONCOGENE; PRIORITY JOURNAL; TRANSCRIPTION REGULATION; TUMOR SUPPRESSOR GENE;

ADULT; AGED; BINDING SITES; BREAST NEOPLASMS; CELL LINE, TUMOR; CLUSTER ANALYSIS; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MICRORNAS; MIDDLE AGED; RESPONSE ELEMENTS;

EID: 84860588204     PISSN: 18688497     EISSN: 18688500     Source Type: Journal    
DOI: 10.1007/s12672-012-0102-1     Document Type: Article

References (71)

1. Heldring N, Pike A, Andersson S, Matthews J, Cheng G, Hartman J, Tujague M et al (2007) Estrogen receptors: how do they signal and what are their targets. Physiol Rev 87: 905-931.
2. Hall JM, Couse JF, Korach KS (2001) The multifaceted mechanisms of estradiol and estrogen receptor signaling. J Biol Chem 276: 36869-36872.
3. Bai Z, Gust R (2009) Breast cancer, estrogen receptor and ligands. Arch Pharm (Weinheim) 342: 133-149.
4. Kushner PJ, Agard DA, Greene GL, Scanlan TS, Shiau AK, Uht RM, Webb P (2000) Estrogen receptor pathways to AP-1. J Steroid Biochem Mol Biol 74: 311-317.
5. Saville B, Wormke M, Wang F, Nguyen T, Enmark E, Kuiper G, Gustafsson JA et al (2000) Ligand-, cell-, estrogen receptor subtype (alpha/beta)-dependent activation at GC-rich (Sp1) promoter elements. J Biol Chem 275: 5379-5387.
6. McDonnell DP, Norris JD (2002) Connections and regulation of the human estrogen receptor. Science 296: 1642-1644.
7. Klinge CM, Jernigan SC, Mattingly KA, Risinger KE, Zhang J (2004) Estrogen response element-dependent regulation of transcriptional activation of estrogen receptors alpha and beta by coactivators and corepressors. J Mol Endocrinol 33: 387-410.
8. Chen GG, Zeng Q, Tse GM (2008) Estrogen and its receptors in cancer. Med Res Rev 28: 954-974.
9. Manavathi B, Kumar R (2006) Steering estrogen signals from the plasma membrane to the nucleus: two sides of the coin. J Cell Physiol 207: 594-604.
10. Safe S, Kim KJ (2008) Non-classical genomic estrogen receptor (ER)/specificity protein and ER/activating protein-1 signaling pathways. J Mol Endocrinol 41: 263-275.
11. Gronemeyer H, Gustafsson JA, Laudet V (2004) Principles for modulation of the nuclear receptor superfamily. Nat Rev Drug Discov 3: 950-964.
12. Kim VN (2005) MicroRNA biogenesis: coordinated cropping and dicing. Nat Rev Mol Cell Biol 6: 376-385.
13. Xiong H, Qian J, He T, Li F (2009) Indipendent transcription of miR-281 in the intron of ODA in Drosophila melanogaster. Biochem Biophys Res Commun 378: 883-889.
14. Rodriguez A, Griffiths-Jones S, Ashurst JL, Bradley A (2004) Identification of mammalian microRNA host genes and transcription units. Genome Res 14: 1902-1910.
15. Saini HK, Griffiths-Jones S, Enright AJ (2007) Genomic analysis of human microRNA transcripts. Proc Natl Acad Sci USA 104: 17719-17724.
16. Lee Y, Kim M, Han JJ, Yeom KH, Lee S, Baek SH, Kim VN (2004) MicroRNA genes are transcribed by RNA polymerase II. EMBO J 23: 4051-4060.
17. Denli AM, Tops BB, Plasterk RH, Ketting RF, Hannon GJ (2004) Processing of primary microRNAs by the Microprocessor complex. Nature 432: 231-235.
18. Lee Y, Jeon K, Lee JT, Kim S, Kim VN (2002) microRNA maturation: stepwise processing and subcellular localization. EMBO J 21: 4663-4670.
19. Gregory RI, Chendrimada TP, Cooch N, Shiekhattar R (2005) Human RISC couples microRNA biogenesis and posttranscriptional gene silencing. Cell 123: 631-640.
20. Engels BM, Hutvagner G (2006) Principles and effects of microRNA-mediated post-transcriptional gene regulation. Oncogene 25: 6163-6169.
21. He L, Hannon GJ (2004) MicroRNAs: small RNAs with a big role in gene regulation. Nat Rev Genet 5: 522-531.
22. Linsen S, Tops B, Cuppen E (2008) miRNAs small changes, widespread effects. Cell Res 18: 1157-1159.
23. Lewis BP, Burge CB, Bartel DP (2005) Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120: 15-20.
24. Zhao Y, Srivastava D (2007) A developmental view of microRNA function. Trends Biochem Sci 32: 189-197.
25. Ventura A, Jacks T (2009) MicroRNAs and cancer: short RNAs go a long way. Cell 136: 586-591.
26. Tessel MA, Krett NL, Rosen ST (2010) Steroid receptor and microRNA regulation in cancer. Curr Opin Oncol 22: 592-597.
27. Klinge CM (2009) Estrogen regulation of miRNA expression. Curr Genomics 10: 169-183.
28. Bhat-Nakshatri P, Wang G, Collins NR, Thomson MJ, Geistlinger TR, Carroll JS, Brown M et al (2009) Estradiol-regulated microRNAs control estradiol response in breast cancer cells. Nucleic Acids Res 37: 4850-4861.
29. Yang Z, Wang L (2011) Regulation of microRNA expression and function by nuclear receptor signaling. Cell Biosci 1: 31.
30. Paris O, Ferraro L, Grober OMV, Ravo M, De Filippo MR, Giurato G, Nassa G, Tarallo et al. (2012) Direct regulation of microRNA biogenesis and expression by estrogen receptor beta in hormone-responsive breast cancer. Oncogene. doi: 10. 1038/onc. 2011. 583.
31. Esquela-Kerscher A, Slack FJ (2006) Oncomirs-microRNAs with a role in cancer. Nat Rev Cancer 6: 259-269.
32. Iorio MV, Ferracin M, Liu CG, Veronese A, Spizzo R, Sabbioni S, Magri E et al (2005) MicroRNA gene expression deregulation in human breast cancer. Cancer Res 65: 7065-7070.
33. Lu J, Getz G, Miska EA, Alvarez-Saavedra E, Lamb J, Peck D, Sweet-Cordero A et al (2005) MicroRNA expression profiles classify human cancers. Nature 435: 834-838.
34. Blenkiron C, Goldstein LD, Thorne NP, Spiteri I, Chin SF, Dunning MJ, Barbosa-Morais NL et al (2007) MicroRNA expression profiling of human breast cancer identifies new markers of tumor subtype. Genome Biol 8: R214.
35. Gaur A, Jewell DA, Liang Y, Ridzon D, Moore JH, Chen C, Ambros VR et al (2007) Characterization of microRNA expression levels and their biological correlates in human cancer cell lines. Cancer Res 67: 2456-2468.
36. O'Day E, Lal A (2010) MicroRNAs and their target gene networks in breast cancer. Breast Cancer Res 12: 201.
37. Adams BD, Furneaux H, White BA (2007) The micro-ribonucleic acid (miRNA) miR-206 targets the human estrogen receptor alpha (ERalpha) and represses ERalpha messenger RNA and protein expression in breast cancer cell lines. Mol Endocrinol 21: 1132-1147.
38. Hossain A, Kuo MT, Saunders GF (2006) Mir-17-5p regulates breast cancer cell proliferation by inhibiting translation of AIB1 mRNA. Mol Cell Biol 26: 8191-8201.
39. Yu Z, Wang C, Wang M, Li Z, Casimiro MC, Liu M, Wu K et al (2008) A cyclin D1/microRNA 17/20 regulatory feedback loop in control of breast cancer cell proliferation. J Cell Biol 182: 509-517.
40. Gaur A, Jewell DA, Liang Y, Ridzon D, Moore JH, Chen C, Ambros VR et al (2007) Characterization of microRNA expression levels and their biological correlates in human cancer cell lines. Cancer Res 67: 2456-2468.
41. Volinia S, Calin GA, Liu CG, Ambs S, Cimmino A, Petrocca F, Visone R et al (2006) A microRNA expression signature of human solid tumors defines cancer gene targets. Proc Natl Acad Sci USA 103: 2257-2261.
42. Gusev Y, Schmittgen TD, Lerner M, Postier R, Brackett D (2007) Computational analysis of biological functions and pathways collectively targeted by co-expressed microRNAs in cancer. BMC Bioinforma 8(Suppl 7): S16.
43. Cochrane DR, Cittelly DM, Howe EN, Spoelstra NS, McKinsey EL, LaPara K, Elias A et al (2010) MicroRNAs link estrogen receptor alpha status and dicer levels in breast cancer. Horm Cancer 1: 306-319.
44. Ambrosino C, Tarallo R, Bamundo A, Cuomo D, Franci G, Nassa G, Paris O et al (2010) Identification of a hormone-regulated dynamic nuclear actin network associated with estrogen receptor alpha in human breast cancer cell nuclei. Mol Cell Proteomics 9: 1352-1367.
45. Cimino D, Fuso L, Sfiligoi C, Biglia N, Ponzone R, Maggiorotto F, Russo G et al (2008) Identification of new genes associated with breast cancer progression by gene expression analysis of predefined set of neoplastic tissues. Int J Cancer 123: 1327-1338.
46. Scafoglio C, Ambrosino C, Cicatiello L, Altucci L, Ardovino M, Bontempo P, Medici N et al (2006) Comparative gene expression profiling reveals partially overlapping but distinct genomic actions of different antiestrogens in human breast cancer cells. J Cell Biochem 98: 1163-1184.
47. Cicatiello L, Scafoglio C, Altucci L, Cancemi M, Natoli G, Facchiano A, Iazzetti G et al (2004) A genomic view of estrogen actions in human breast cancer cells by expression profiling of the hormone-responsive transcriptome. J Mol Endocrinol 32: 719-775.
48. Cicatiello L, Mutarelli M, Grober OMV, Paris O, Ferraro L, Ravo M, Tarallo R et al (2010) A gene network controlled by estrogen receptor α in luminal-like breast cancer cells comprising multiple transcription factors and microRNAs. Am J Pathol 176: 2113-2130.
49. Ravo M, Mutarelli M, Ferraro L, Grober OMV, Paris O, Tarallo R, Vigilante A et al (2008) Quantitative expression profilino of highly degraded RNA from formalin-fixed, paraffin-embedded breast tumor biopsies by oligonucleotide microarrays. Lab Inv 88: 430-440.
50. Tusher VG, Tibshirani R, Chu G (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci 98: 5116-5121.
51. Grober OMV, Mutarelli M, Giurato G, Ravo M, Cicatiello L, De Filippo MR, Ferraro L et al (2011) 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 12: 36.
52. Fejes AP, Robertson G, Bilenky M, Varhol R, Bainbridge M, Jones SJ (2008) FindPeaks 3. 1: a tool for identifying areas of enrichment from massively parallel short-read sequencing technology. Bioinformatics 24: 1729-1730.
53. Qiunian AR, Hall IN (2010) BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26: 841-842.
54. Dennis G Jr, Sherman BT, Hosack DA, Yang J, Gao W, Lane HC, Lempicki RA (2003) DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome Biol 4: P3.
55. da Huang W, Sherman BT, Lempicki RA (2009) Systematic and integrative analysis of large gene lists using DAVID Bioinformatics Resources. Nature Protoc 4: 44-57.
56. Weigelt K, Moehle C, Stempfl T, Weber B, Langmann T (2008) An integrated workflow for analysis of ChIP-chip data. Biotechniques 45: 131-132.
57. Cicatiello L, Scafoglio C, Altucci L, Cancemi M, Natoli G, Facchiano A, Iazzetti G et al (2004) A genomic view of estrogen actions in human breast cancer cells by expression profiling of the hormone-responsive transcriptome. J Mol Endocrinol 32: 719-775.
58. Cicatiello L, Addeo R, Altucci L, Belsito Petrizzi V, Boccia V, Cancemi M, Germano D et al (2000) The antiestrogen ICI 182, 780 inhibits proliferation of human breast cancer cells by interfering with multiple, sequential estrogen-regulated processes required for cell cycle completion. Mol Cell Endocrinol 165: 199-209.
59. Castellano L, Giamas G, Jacob J, Coombes RC, Lucchesi W, Thiruchelvam P, Barton G et al (2009) The estrogen receptor-alpha-induced microRNA signature regulates itself and its transcriptional response. Proc Natl Acad Sci U S A 106: 15732-15737.
60. Maillot G, Lacroix-Triki M, Pierredon S, Gratadou L, Schmidt S, Bénès V, Roché H et al (2009) Widespread estrogen-dependent repression of micrornas involved in breast tumor cell growth. Cancer Res 69: 8332-8340.
61. Fullwood MJ, Liu MH, Pan YF, Liu J, Xu H, Mohamed YB, Orlov YL et al (2009) An oestrogen-receptor-alpha bound human chromatin interactome. Nature 462: 58-64.
62. Kim VN, Han J, Siomi MC (2009) Biogenesis of small RNAs in animals. Nat Rev Mol Cell Biol 10: 126-139.
63. Li X, Mertens-Talcott SU, Shu Z, KyoungHyun K, Judith B, Stephen S (2010) MicroRNA-27a indirectly regulates estrogen receptor alpha expression and hormone responsiveness in MCF-7 breast cancer cells. Endocrinology 151: 2462-2473.
64. Nagel R, le Sage C, Diosdado B, van der Waal M, Oude Vrielink JA, Bolijn A, Meijer GA et al (2008) Regulation of the adenomatous polyposis coli gene by the miR-135 family in colorectal cancer. Cancer Res 68: 5795-5802.
65. Navarro A, Diaz T, Martinez A, Gaya A, Pons A, Gel B, Codony C et al (2009) Regulation of JAK2 by miR-135a: prognostic impact in classic Hodgkin lymphoma. Blood 114: 2945-2951.
66. Suzuki HI, Yamagata K, Sugimoto K, Iwamoto T, Kato S, Miyazono K (2009) Modulation of microRNA processing by p53. Nature 460: 529-533.
67. Davis BN, Hilyard AC, Lagna G, Hata A (2008) SMAD proteins control DROSHA-mediated microRNA maturation. Nature 454: 56-61.
68. Yamagata K, Fujiyama S, Ito S, Ueda T, Murata T, Naitou M, Takeyama K et al (2009) Maturation of microRNA is hormonally regulated by a nuclear receptor. Mol Cell 36: 340-347.
69. Buffa FM, Camps C, Winchester L, Snell CE, Gee HE, Sheldon H, Taylor M et al (2011) microRNA-associated progression pathways and potential therapeutic targets identified by integrated mRNA and microRNA expression profiling in breast cancer. Cancer Res 71: 5635-5645.
70. Qian B, Katsaros D, Lu L, Preti M, Durando A, Arisio R, Mu L et al (2009) High miR-21 expression in breast cancer associated with poor disease-free survival in early stage disease and highTGF-beta1. Breast Cancer Rea Treat 117: 131-140.
71. Weisz A, Basile W, Scafoglio C, Altucci L, Bresciani F, Facchiano A, Sismondi P (2004) Molecular identification of ERalpha-positive breast cancer cells by the expression profile of an intrinsic set of estrogen regulated genes. J Cell Physiol 200: 440-450.