MicroRNA-101 negatively regulates Ezh2 and its expression is modulated by androgen receptor and HIF-1α/HIF-1β

Molecular Cancer

Volumn 9, Issue , 2010, Pages

  Cao, Paul ^a   Deng, Zhiyong ^a   Wan, Meimei ^a   Huang, Weiwei ^a,b   Cramer, Scott D ^a   Xu, Jianfeng ^a   Lei, Ming ^b   Sui, Guangchao ^a  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

^b NORTHWEST A F UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGEN RECEPTOR; DEFEROXAMINE MESYLATE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; HYPOXIA INDUCIBLE FACTOR 1BETA; MICRORNA; MICRORNA 101; MICRORNA 26A; TRANSCRIPTION FACTOR EZH2; UNCLASSIFIED DRUG; ARNT PROTEIN, HUMAN; DNA BINDING PROTEIN; EZH2 PROTEIN, HUMAN; HIF1A PROTEIN, HUMAN; MIRN101 MICRORNA, HUMAN; MIRN26A MICRORNA, HUMAN; TRANSCRIPTION FACTOR;

3' UNTRANSLATED REGION; ARTICLE; CANCER CELL; CARCINOGENESIS; CELL GROWTH; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; CELL STRUCTURE; CELL SURVIVAL; CONTROLLED STUDY; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; PROSTATE CANCER; BIOSYNTHESIS; CANCER INVASION; GENE EXPRESSION; GENETIC TRANSFECTION; GENETICS; MALE; METABOLISM; PROSTATE TUMOR; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR CELL LINE;

ARYL HYDROCARBON RECEPTOR NUCLEAR TRANSLOCATOR; CELL LINE, TUMOR; CELL PROLIFERATION; DNA-BINDING PROTEINS; GENE EXPRESSION; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MALE; MICRORNAS; NEOPLASM INVASIVENESS; PROSTATIC NEOPLASMS; RECEPTORS, ANDROGEN; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TRANSCRIPTION FACTORS; TRANSFECTION;

EID: 77952160818     PISSN: None     EISSN: 14764598     Source Type: Journal    
DOI: 10.1186/1476-4598-9-108     Document Type: Article

References (55)

1. Schuettengruber B, Chourrout D, Vervoort M, Leblanc B, Cavalli G. Genome regulation by polycomb and trithorax proteins. Cell 2007, 128:735-745. 10.1016/j.cell.2007.02.009, 17320510.
2. Cao R, Wang L, Wang H, Xia L, Erdjument-Bromage H, Tempst P, Jones RS, Zhang Y. Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science 2002, 298:1039-1043. 10.1126/science.1076997, 12351676.
3. Smith ER, Lee MG, Winter B, Droz NM, Eissenberg JC, Shiekhattar R, Shilatifard A. Drosophila UTX is a histone H3 Lys27 demethylase that colocalizes with the elongating form of RNA polymerase II. Mol Cell Biol 2008, 28:1041-1046. 10.1128/MCB.01504-07, 2223382, 18039863.
4. Tan J, Yang X, Zhuang L, Jiang X, Chen W, Lee PL, Karuturi RK, Tan PB, Liu ET, Yu Q. Pharmacologic disruption of Polycomb-repressive complex 2-mediated gene repression selectively induces apoptosis in cancer cells. Genes Dev 2007, 21:1050-1063. 10.1101/gad.1524107, 1855231, 17437993.
5. Wilkinson FH, Park K, Atchison ML. Polycomb recruitment to DNA in vivo by the YY1 REPO domain. Proc Natl Acad Sci USA 2006, 103:19296-19301. 10.1073/pnas.0603564103, 1748220, 17158804.
6. Bracken AP, Pasini D, Capra M, Prosperini E, Colli E, Helin K. EZH2 is downstream of the pRB-E2F pathway, essential for proliferation and amplified in cancer. EMBO J 2003, 22:5323-5335. 10.1093/emboj/cdg542, 213796, 14532106.
7. Plath K, Fang J, Mlynarczyk-Evans SK, Cao R, Worringer KA, Wang H, de la Cruz CC, Otte AP, Panning B, Zhang Y. Role of histone H3 lysine 27 methylation in X inactivation. Science 2003, 300:131-135. 10.1126/science.1084274, 12649488.
8. Gil J, Bernard D, Peters G. Role of polycomb group proteins in stem cell self-renewal and cancer. DNA Cell Biol 2005, 24:117-125. 10.1089/dna.2005.24.117, 15699631.
9. Kamminga LM, Bystrykh LV, de Boer A, Houwer S, Douma J, Weersing E, Dontje B, de Haan G. The Polycomb group gene Ezh2 prevents hematopoietic stem cell exhaustion. Blood 2006, 107:2170-2179. 10.1182/blood-2005-09-3585, 1895717, 16293602.
10. Caretti G, Di Padova M, Micales B, Lyons GE, Sartorelli V. The Polycomb Ezh2 methyltransferase regulates muscle gene expression and skeletal muscle differentiation. Genes Dev 2004, 18:2627-2638. 10.1101/gad.1241904, 525543, 15520282.
11. Su IH, Dobenecker MW, Dickinson E, Oser M, Basavaraj A, Marqueron R, Viale A, Reinberg D, Wulfing C, Tarakhovsky A. Polycomb group protein ezh2 controls actin polymerization and cell signaling. Cell 2005, 121:425-436. 10.1016/j.cell.2005.02.029, 15882624.
12. Etchegaray JP, Yang X, DeBruyne JP, Peters AH, Weaver DR, Jenuwein T, Reppert SM. The polycomb group protein EZH2 is required for mammalian circadian clock function. J Biol Chem 2006, 281:21209-21215. 10.1074/jbc.M603722200, 16717091.
13. Varambally S, Dhanasekaran SM, Zhou M, Barrette TR, Kumar-Sinha C, Sanda MG, Ghosh D, Pienta KJ, Sewalt RG, Otte AP, et al. The polycomb group protein EZH2 is involved in progression of prostate cancer. Nature 2002, 419:624-629. 10.1038/nature01075, 12374981.
14. Rhodes DR, Sanda MG, Otte AP, Chinnaiyan AM, Rubin MA. Multiplex biomarker approach for determining risk of prostate-specific antigen-defined recurrence of prostate cancer. J Natl Cancer Inst 2003, 95:661-668.
15. Yu J, Yu J, Rhodes DR, Tomlins SA, Cao X, Chen G, Mehra R, Wang X, Ghosh D, Shah RB, et al. A polycomb repression signature in metastatic prostate cancer predicts cancer outcome. Cancer Res 2007, 67:10657-10663. 10.1158/0008-5472.CAN-07-2498, 18006806.
16. Takeshita F, Minakuchi Y, Nagahara S, Honma K, Sasaki H, Hirai K, Teratani T, Namatame N, Yamamoto Y, Hanai K, et al. Efficient delivery of small interfering RNA to bone-metastatic tumors by using atelocollagen in vivo. Proc Natl Acad Sci USA 2005, 102:12177-12182. 10.1073/pnas.0501753102, 1183487, 16091473.
17. Bryant RJ, Cross NA, Eaton CL, Hamdy FC, Cunliffe VT. EZH2 promotes proliferation and invasiveness of prostate cancer cells. Prostate 2007, 67:547-556. 10.1002/pros.20550, 17252556.
18. Sellers WR, Loda M. The EZH2 polycomb transcriptional repressor--a marker or mover of metastatic prostate cancer?. Cancer Cell 2002, 2:349-350. 10.1016/S1535-6108(02)00187-3, 12450788.
19. Tang X, Milyavsky M, Shats I, Erez N, Goldfinger N, Rotter V. Activated p53 suppresses the histone methyltransferase EZH2 gene. Oncogene 2004, 23:5759-5769. 10.1038/sj.onc.1207706, 15208672.
20. Cha TL, Zhou BP, Xia W, Wu Y, Yang CC, Chen CT, Ping B, Otte AP, Hung MC. Akt-mediated phosphorylation of EZH2 suppresses methylation of lysine 27 in histone H3. Science 2005, 310:306-310. 10.1126/science.1118947, 16224021.
21. Lai EC. Micro RNAs are complementary to 3' UTR sequence motifs that mediate negative post-transcriptional regulation. Nat Genet 2002, 30:363-364. 10.1038/ng865, 11896390.
22. Fabbri M, Croce CM, Calin GA. MicroRNAs. Cancer J 2008, 14:1-6. 10.1097/PPO.0b013e318164145e, 18303474.
23. Barbarotto E, Schmittgen TD, Calin GA. MicroRNAs and cancer: profile, profile, profile. Int J Cancer 2008, 122:969-977. 10.1002/ijc.23343, 18098138.
24. Varambally S, Cao Q, Mani RS, Shankar S, Wang X, Ateeq B, Laxman B, Cao X, Jing X, Ramnarayanan K, et al. Genomic loss of microRNA-101 leads to overexpression of histone methyltransferase EZH2 in cancer. Science 2008, 322:1695-1699. 10.1126/science.1165395, 2684823, 19008416.
25. Deng Z, Wan M, Sui G. PIASy-mediated sumoylation of Yin Yang 1 depends on their interaction but not the RING finger. Mol Cell Biol 2007, 27:3780-3792. 10.1128/MCB.01761-06, 1899983, 17353273.
26. Rubinson DA, Dillon CP, Kwiatkowski AV, Sievers C, Yang L, Kopinja J, Rooney DL, Ihrig MM, McManus MT, Gertler FB, et al. A lentivirus-based system to functionally silence genes in primary mammalian cells, stem cells and transgenic mice by RNA interference. Nat Genet 2003, 33:401-406. 10.1038/ng1117, 12590264.
27. Deng Z, Wan M, Cao P, Rao A, Cramer SD, Sui G. Yin Yang 1 regulates the transcriptional activity of androgen receptor. Oncogene 2009, 28:3746-3757. 10.1038/onc.2009.231, 19668226.
28. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001, 25:402-408. 10.1006/meth.2001.1262, 11846609.
29. Griffiths-Jones S, Saini HK, van Dongen S, Enright AJ. miRBase: tools for microRNA genomics. Nucleic Acids Res 2008, 36:D154-158. 10.1093/nar/gkm952, 2238936, 17991681.
30. John B, Enright AJ, Aravin A, Tuschl T, Sander C, Marks DS. Human MicroRNA targets. PLoS Biol 2004, 2:e363. 10.1371/journal.pbio.0020363, 521178, 15502875.
31. Lewis BP, Burge CB, Bartel DP. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 2005, 120:15-20. 10.1016/j.cell.2004.12.035, 15652477.
32. Krek A, Grun D, Poy MN, Wolf R, Rosenberg L, Epstein EJ, MacMenamin P, da Piedade I, Gunsalus KC, Stoffel M, Rajewsky N. Combinatorial microRNA target predictions. Nat Genet 2005, 37:495-500. 10.1038/ng1536, 15806104.
33. Wong CF, Tellam RL. MicroRNA-26a targets the histone methyltransferase Enhancer of Zeste homolog 2 during myogenesis. J Biol Chem 2008, 283:9836-9843. 10.1074/jbc.M709614200, 18281287.
34. Sander S, Bullinger L, Klapproth K, Fiedler K, Kestler HA, Barth TF, Moller P, Stilgenbauer S, Pollack JR, Wirth T. MYC stimulates EZH2 expression by repression of its negative regulator miR-26a. Blood 2008, 112:4202-4212. 10.1182/blood-2008-03-147645, 18713946.
35. Lu J, Getz G, Miska EA, Alvarez-Saavedra E, Lamb J, Peck D, Sweet-Cordero A, Ebert BL, Mak RH, Ferrando AA, et al. MicroRNA expression profiles classify human cancers. Nature 2005, 435:834-838. 10.1038/nature03702, 15944708.
36. Volinia S, Calin GA, Liu CG, Ambs S, Cimmino A, Petrocca F, Visone R, Iorio M, Roldo C, Ferracin M, et al. A microRNA expression signature of human solid tumors defines cancer gene targets. Proc Natl Acad Sci USA 2006, 103:2257-2261. 10.1073/pnas.0510565103, 1413718, 16461460.
37. Webber MM, Bello D, Kleinman HK, Wartinger DD, Williams DE, Rhim JS. Prostate specific antigen and androgen receptor induction and characterization of an immortalized adult human prostatic epithelial cell line. Carcinogenesis 1996, 17:1641-1646. 10.1093/carcin/17.8.1641, 8761420.
38. Engl T, Relja B, Blumenberg C, Muller I, Ringel EM, Beecken WD, Jonas D, Blaheta RA. Prostate tumor CXC-chemokine profile correlates with cell adhesion to endothelium and extracellular matrix. Life Sci 2006, 78:1784-1793. 10.1016/j.lfs.2005.08.019, 16263140.
39. Mishra PJ, Humeniuk R, Mishra PJ, Longo-Sorbello GS, Banerjee D, Bertino JR. A miR-24 microRNA binding-site polymorphism in dihydrofolate reductase gene leads to methotrexate resistance. Proc Natl Acad Sci USA 2007, 104:13513-13518. 10.1073/pnas.0706217104, 1948927, 17686970.
40. Nicoloso MS, Sun H, Spizzo R, Kim H, Wickramasinghe P, Shimizu M, Wojcik SE, Ferdin J, Kunej T, Xiao L, et al. Single-nucleotide polymorphisms inside microRNA target sites influence tumor susceptibility. Cancer Res 70:2789-2798. 10.1158/0008-5472.CAN-09-3541, 20332227.
41. Cao R, Zhang Y. The functions of E(Z)/EZH2-mediated methylation of lysine 27 in histone H3. Curr Opin Genet Dev 2004, 14:155-164. 10.1016/j.gde.2004.02.001, 15196462.
42. Rodriguez A, Griffiths-Jones S, Ashurst JL, Bradley A. Identification of mammalian microRNA host genes and transcription units. Genome Res 2004, 14:1902-1910. 10.1101/gr.2722704, 524413, 15364901.
43. Heinemeyer T, Wingender E, Reuter I, Hermjakob H, Kel AE, Kel OV, Ignatieva EV, Ananko EA, Podkolodnaya OA, Kolpakov FA, et al. Databases on transcriptional regulation: TRANSFAC, TRRD and COMPEL. Nucleic Acids Res 1998, 26:362-367. 10.1093/nar/26.1.362, 147251, 9399875.
44. Kimbro KS, Simons JW. Hypoxia-inducible factor-1 in human breast and prostate cancer. Endocr Relat Cancer 2006, 13:739-749. 10.1677/erc.1.00728, 16954428.
45. Martinez-Romero R, Martinez-Lara E, Aguilar-Quesada R, Peralta A, Oliver FJ, Siles E. PARP-1 modulates deferoxamine-induced HIF-1alpha accumulation through the regulation of nitric oxide and oxidative stress. J Cell Biochem 2008, 104:2248-2260. 10.1002/jcb.21781, 18459142.
46. Heinlein CA, Chang C. Androgen receptor in prostate cancer. Endocr Rev 2004, 25:276-308. 10.1210/er.2002-0032, 15082523.
47. Ripple MO, Henry WF, Rago RP, Wilding G. Prooxidant-antioxidant shift induced by androgen treatment of human prostate carcinoma cells. J Natl Cancer Inst 1997, 89:40-48. 10.1093/jnci/89.1.40, 8978405.
48. Shao C, Wang Y, Yue HH, Zhang YT, Shi CH, Liu F, Bao TY, Yang ZY, Yuan JL, Shao GX. Biphasic effect of androgens on prostate cancer cells and its correlation with androgen receptor coactivator dopa decarboxylase. J Androl 2007, 28:804-812. 10.2164/jandrol.106.002154, 17581945.
49. Tonini T, D'Andrilli G, Fucito A, Gaspa L, Bagella L. Importance of Ezh2 polycomb protein in tumorigenesis process interfering with the pathway of growth suppressive key elements. J Cell Physiol 2008, 214:295-300. 10.1002/jcp.21241, 17786943.
50. Kedde M, Strasser MJ, Boldajipour B, Vrielink JA, Slanchev K, le Sage C, Nagel R, Voorhoeve PM, van Duijse J, Orom UA, et al. RNA-binding protein Dnd1 inhibits microRNA access to target mRNA. Cell 2007, 131:1273-1286. 10.1016/j.cell.2007.11.034, 18155131.
51. Kruger J, Rehmsmeier M. RNAhybrid: microRNA target prediction easy, fast and flexible. Nucleic Acids Res 2006, 34:W451-454. 10.1093/nar/gkl243, 1538877, 16845047.
52. To KK, Zhan Z, Litman T, Bates SE. Regulation of ABCG2 expression at 3'-untranslated region of its mRNA through modulation of transcript stability and protein translation by a putative microRNA in S1 colon cancer cell line. Mol Cell Biol 2008, 28:5147-5161. 10.1128/MCB.00331-08, 2519722, 18573883.
53. Sandberg R, Neilson JR, Sarma A, Sharp PA, Burge CB. Proliferating cells express mRNAs with shortened 3' untranslated regions and fewer microRNA target sites. Science 2008, 320:1643-1647. 10.1126/science.1155390, 2587246, 18566288.
54. Hobert O. miRNAs play a tune. Cell 2007, 131:22-24. 10.1016/j.cell.2007.09.031, 17923083.
55. Karres JS, Hilgers V, Carrera I, Treisman J, Cohen SM. The conserved microRNA miR-8 tunes atrophin levels to prevent neurodegeneration in Drosophila. Cell 2007, 131:136-145. 10.1016/j.cell.2007.09.020, 17923093.