Identification of an Enhancer That Increases miR-200b~200a~429 Gene Expression in Breast Cancer Cells

PLoS ONE

Volumn 8, Issue 9, 2013, Pages

  Attema, Joanne L ^a,d   Bert, Andrew G ^a   Lim, Yat Yuen ^a,b,c   Kolesnikoff, Natasha ^a   Lawrence, David M ^a,d   Pillman, Katherine A ^a   Smith, Eric ^d   Drew, Paul A ^e   Khew Goodall, Yeesim ^a,d   Shannon, Frances ^f   Goodall, Gregory J ^a,b,d  

^a CENTRE FOR CANCER BIOLOGY   (Australia)

^b UNIVERSITY OF ADELAIDE   (Australia)

^c UNIVERSITY OF MALAYA   (Malaysia)

^d UNIVERSITY OF ADELAIDE   (Australia)

^e FLINDERS UNIVERSITY   (Australia)

^f UNIVERSITY OF CANBERRA   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

DINUCLEOTIDE; DNA; ENHANCER RNA; MICRORNA; MICRORNA 200A; MICRORNA 200B; MICRORNA 429; RNA; RNA POLYMERASE II; UNCLASSIFIED DRUG;

ARTICLE; BREAST CANCER; CANCER CELL; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; CPG ISLAND; DNA METHYLATION; DNA MODIFICATION; EPIGENETICS; EPITHELIUM CELL; GC RICH SEQUENCE; GENE CLUSTER; GENE EXPRESSION; GENE LOCUS; GENE OVEREXPRESSION; GENE SILENCING; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; MESENCHYME CELL; PROMOTER REGION; TRANSCRIPTION INITIATION SITE; TRANSCRIPTION REGULATION;

BREAST NEOPLASMS; CELL LINE, TUMOR; CHROMATIN; ENHANCER ELEMENTS, GENETIC; EPIGENOMICS; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MICRORNAS; PROMOTER REGIONS, GENETIC; RNA; TRANSCRIPTION INITIATION SITE;

EID: 84884575728     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0075517     Document Type: Article

References (49)

1. Gangaraju VK, Lin H, (2009) MicroRNAs: key regulators of stem cells. Nat Rev Mol Cell Biol 10: 116-125. doi:10.1038/nrm2621. PubMed: 19165214.
2. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, et al. (2008) The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 133: 704-715. doi:10.1016/j.cell.2008.03.027. PubMed: 18485877.
3. Brabletz S, Brabletz T, (2010) The ZEB/miR-200 feedback loop--a motor of cellular plasticity in development and cancer? EMBO Rep 11: 670-677. doi:10.1038/embor.2010.117. PubMed: 20706219.
4. Bracken CP, Gregory PA, Kolesnikoff N, Bert AG, Wang J, et al. (2008) A double-negative feedback loop between ZEB1-SIP1 and the microRNA-200 family regulates epithelial-mesenchymal transition. Cancer Res 68: 7846-7854. doi:10.1158/0008-5472.CAN-08-1942. PubMed: 18829540.
5. Gregory PA, Bert AG, Paterson EL, Barry SC, Tsykin A, et al. (2008) The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat Cell Biol 10: 593-601. doi:10.1038/ncb1722. PubMed: 18376396.
6. Hurteau GJ, Carlson JA, Spivack SD, Brock GJ, (2007) Overexpression of the microRNA hsa-miR-200c leads to reduced expression of transcription factor 8 and increased expression of E-cadherin. Cancer Res 67: 7972-7976. doi:10.1158/0008-5472.CAN-07-1058. PubMed: 17804704.
7. Burk U, Schubert J, Wellner U, Schmalhofer O, Vincan E, et al. (2008) A reciprocal repression between ZEB1 and members of the miR-200 family promotes EMT and invasion in cancer cells. EMBO Rep 9: 582-589. doi:10.1038/embor.2008.74. PubMed: 18483486.
8. Park SM, Gaur AB, Lengyel E, Peter ME, (2008) The miR-200 family determines the epithelial phenotype of cancer cells by targeting the E-cadherin repressors ZEB1 and ZEB2. Genes Dev 22: 894-907. doi:10.1101/gad.1640608. PubMed: 18381893.
9. Korpal M, Lee ES, Hu G, Kang Y, (2008) The miR-200 family inhibits epithelial-mesenchymal transition and cancer cell migration by direct targeting of E-cadherin transcriptional repressors ZEB1 and ZEB2. J Biol Chem 283: 14910-14914. doi:10.1074/jbc.C800074200. PubMed: 18411277.
10. Bulger M, Groudine M, (2011) Functional and mechanistic diversity of distal transcription enhancers. Cell 144: 327-339. doi:10.1016/j.cell.2011.01.024. PubMed: 21295696.
11. Jin F, Li Y, Ren B, Natarajan R, (2011) Enhancers: multi-dimensional signal integrators. Transcription 2: 226-230. doi:10.4161/trns.2.5.17712. PubMed: 22231119.
12. Deaton AM, Bird A, (2011) CpG islands and the regulation of transcription. Genes Dev 25: 1010-1022. doi:10.1101/gad.2037511. PubMed: 21576262.
13. Van Bortle K, Corces VG, (2012) Nuclear organization and genome function. Annu Rev Cell Dev Biol 28: 163-187. doi:10.1146/annurev-cellbio-101011-155824. PubMed: 22905954.
14. Pike JW, (2011) Genome-scale techniques highlight the epigenome and redefine fundamental principles of gene regulation. Journal of bone and mineral research: the official journal of the American Society for Bone and Mineral Research 26: 1155-1162. doi:10.1002/jbmr.317. PubMed: 21611959.
15. Smallwood A, Ren B, (2013) Genome organization and long-range regulation of gene expression by enhancers. Curr Opin Cell Biol, 25: 1-8. doi:10.1016/j.ceb.2013.02.005.
16. Heintzman ND, Stuart RK, Hon G, Fu Y, Ching CW, et al. (2007) Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome. Nat Genet 39: 311-318. doi:10.1038/ng1966. PubMed: 17277777.
17. Heintzman ND, Ren B, (2009) Finding distal regulatory elements in the human genome. Curr Opin Genet Dev 19: 541-549. doi:10.1016/j.gde.2009.09.006. PubMed: 19854636.
18. Heintzman ND, Hon GC, Hawkins RD, Kheradpour P, Stark A, et al. (2009) Histone modifications at human enhancers reflect global cell-type-specific gene expression. Nature 459: 108-112. doi:10.1038/nature07829. PubMed: 19295514.
19. Visel A, Blow MJ, Li Z, Zhang T, Akiyama JA, et al. (2009) ChIP-seq accurately predicts tissue-specific activity of enhancers. Nature 457: 854-858. doi:10.1038/nature07730. PubMed: 19212405.
20. Creyghton MP, Cheng AW, Welstead GG, Kooistra T, Carey BW, et al. (2010) Histone H3K27ac separates active from poised enhancers and predicts developmental state. Proc Natl Acad Sci U S A 107: 21931-21936. doi:10.1073/pnas.1016071107. PubMed: 21106759.
21. De Santa F, Barozzi I, Mietton F, Ghisletti S, Polletti S, et al. (2010) A large fraction of extragenic RNA pol II transcription sites overlap enhancers. PLOS Biol 8: e1000384. doi:10.1371/journal.pbio.1000384.
22. Blow MJ, McCulley DJ, Li Z, Zhang T, Akiyama JA, et al. (2010) ChIP-Seq identification of weakly conserved heart enhancers. Nat Genet 42: 806-810. doi:10.1038/ng.650. PubMed: 20729851.
23. Rada-Iglesias A, Bajpai R, Swigut T, Brugmann SA, Flynn RA, et al. (2011) A unique chromatin signature uncovers early developmental enhancers in humans. Nature 470: 279-283. doi:10.1038/nature09692. PubMed: 21160473.
24. Pekowska A, Benoukraf T, Zacarias-Cabeza J, Belhocine M, Koch F, et al. (2011) H3K4 tri-methylation provides an epigenetic signature of active enhancers. EMBO J 30: 4198-4210. doi:10.1038/emboj.2011.295. PubMed: 21847099.
25. Guttman M, Donaghey J, Carey BW, Garber M, Grenier JK, et al. (2011) lincRNAs act in the circuitry controlling pluripotency and differentiation. Nature 477: 295-300. doi:10.1038/nature10398. PubMed: 21874018.
26. Ørom UA, Shiekhattar R, (2011) Long non-coding RNAs and enhancers. Curr Opin Genet Dev 21: 194-198. doi:10.1016/j.gde.2011.01.020. PubMed: 21330130.
27. Kim TK, Hemberg M, Gray JM, Costa AM, Bear DM, et al. (2010) Widespread transcription at neuronal activity-regulated enhancers. Nature 465: 182-187. doi:10.1038/nature09033. PubMed: 20393465.
28. Melo CA, Drost J, Wijchers PJ, Van de Werken H, De Wit E, et al. (2013) eRNAs Are Required for p53-Dependent Enhancer Activity and Gene Transcription. Mol Cell 49: 524-535. doi:10.1016/j.molcel.2012.11.021. PubMed: 23273978.
29. Flynn RA, Chang HY, (2012) Active chromatin and noncoding RNAs: an intimate relationship. Curr Opin Genet Dev 22: 172-178. doi:10.1016/j.gde.2011.11.002. PubMed: 22154525.
30. Kowalczyk MS, Hughes JR, Garrick D, Lynch MD, Sharpe JA, et al. (2012) Intragenic enhancers act as alternative promoters. Mol Cell 45: 447-458. doi:10.1016/j.molcel.2011.12.021. PubMed: 22264824.
31. Zentner GE, Scacheri PC, (2012) The chromatin fingerprint of gene enhancer elements. J Biol Chem 287: 30888-30896. doi:10.1074/jbc.R111.296491. PubMed: 22952241.
32. Ebisuya M, Yamamoto T, Nakajima M, Nishida E, (2008) Ripples from neighbouring transcription. Nat Cell Biol 10: 1106-1113. doi:10.1038/ncb1771. PubMed: 19160492.
33. Iliopoulos D, Lindahl-Allen M, Polytarchou C, Hirsch HA, Tsichlis PN, et al. (2010) Loss of miR-200 inhibition of Suz12 leads to polycomb-mediated repression required for the formation and maintenance of cancer stem cells. Mol Cell 39: 761-772. doi:10.1016/j.molcel.2010.08.013. PubMed: 20832727.
34. Vrba L, Garbe JC, Stampfer MR, Futscher BW, (2011) Epigenetic regulation of normal human mammary cell type-specific miRNAs. Genome Res 21: 2026-2037. doi:10.1101/gr.123935.111. PubMed: 21873453.
35. Cao Q, Mani RS, Ateeq B, Dhanasekaran SM, Asangani IA, et al. (2011) Coordinated regulation of polycomb group complexes through microRNAs in cancer. Cancer cell 20: 187-199. doi:10.1016/j.ccr.2011.06.016.
36. Lim YY, Wright JA, Attema JA, Gregory PA, Bert AG, et al. (n.d.) Epigenetic modulation of the miR-200 family is associated with transition to a breast cancer stem cell-like state. Journal of cell science 126: 2256-66.
37. Elenbaas B, (2001) Human breast cancer cells generated by oncogenic transformation of primary mammary epithelial cells. Genes Dev 15: 50-65. doi:10.1101/gad.828901. PubMed: 11156605.
38. Gregory PA, Bracken CP, Bert AG, Goodall GJ, (2008) MicroRNAs as regulators of epithelial-mesenchymal transition. Cell Cycle 7: 3112-3118. doi:10.4161/cc.7.20.6851. PubMed: 18927505.
39. Himes SR, Tagoh H, Goonetilleke N, Sasmono T, Oceandy D, et al. (2001) A highly conserved c-fms gene intronic element controls macrophage-specific and regulated expression. J Leukoc Biol 70: 812-820. PubMed: 11698502.
40. Lefevre P, Witham J, Lacroix CE, Cockerill PN, Bonifer C, (2008) The LPS-induced transcriptional upregulation of the chicken lysozyme locus involves CTCF eviction and noncoding RNA transcription. Mol Cell 32: 129-139. doi:10.1016/j.molcel.2008.07.023. PubMed: 18851839.
41. Ørom UA, Derrien T, Beringer M, Gumireddy K, Gardini A, et al. (2010) Long noncoding RNAs with enhancer-like function in human cells. Cell 143: 46-58. doi:10.1016/j.cell.2010.09.001. PubMed: 20887892.
42. Kanhere A, Viiri K, Araújo CC, Rasaiyaah J, Bouwman RD, et al. (2010) Short RNAs are transcribed from repressed polycomb target genes and interact with polycomb repressive complex-2. Mol Cell 38: 675-688. doi:10.1016/j.molcel.2010.03.019. PubMed: 20542000.
43. Sandelin A, Carninci P, Lenhard B, Ponjavic J, Hayashizaki Y, et al. (2007) Mammalian RNA polymerase II core promoters: insights from genome-wide studies. Nat Rev Genet 8: 424-436. doi:10.1038/nrg2026. PubMed: 17486122.
44. Frith MC, Valen E, Krogh A, Hayashizaki Y, Carninci P, et al. (2008) A code for transcription initiation in mammalian genomes. Genome Res 18: 1-12. doi:10.1101/gr.6831208. PubMed: 18032727.
45. Boussouar F, Rousseaux S, Khochbin S, (2008) A new insight into male genome reprogramming by histone variants and histone code. Cell Cycle 7: 3499-3502. doi:10.4161/cc.7.22.6975. PubMed: 19001855.
46. Weake VM, Workman JL, (2010) Inducible gene expression: diverse regulatory mechanisms. Nat Rev Genet 11: 426-437. doi:10.1038/nrg2781. PubMed: 20421872.
47. Calo E, Wysocka J, (2013) Modification of Enhancer Chromatin: What, How, and Why? Mol Cell 49: 825-837. doi:10.1016/j.molcel.2013.01.038. PubMed: 23473601.
48. Wang KC, Yang YW, Liu B, Sanyal A, Corces-Zimmerman R, et al. (2011) A long noncoding RNA maintains active chromatin to coordinate homeotic gene expression. Nature 472: 120-124. doi:10.1038/nature09819. PubMed: 21423168.
49. Bertani S, Sauer S, Bolotin E, Sauer F, (2011) The noncoding RNA Mistral activates Hoxa6 and Hoxa7 expression and stem cell differentiation by recruiting MLL1 to chromatin. Mol Cell 43: 1040-1046. doi:10.1016/j.molcel.2011.08.019. PubMed: 21925392.