Oncogenic ETS fusions deregulate E2F3 target genes in Ewing sarcoma and prostate cancer

Genome Research

Volumn 23, Issue 11, 2013, Pages 1797-1809

  Bilke, Sven ^a   Schwentner, Raphaela ^b   Yang, Fan ^a   Kauer, Maximilian ^b   Jug, Gunhild ^b   Walker, Robert L ^a   Davis, Sean ^a   Zhu, Yuelin J ^a   Pineda, Marbin ^a   Meltzer, Paul S ^a   Kovar, Heinrich ^b,c  

^a NATIONAL CANCER INSTITUTE   (United States)

^b CHILDREN'S CANCER RESEARCH INSTITUTE   (Austria)

^c MEDICAL UNIVERSITY OF VIENNA   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CYCLE PROTEIN; EWSR1 FLI1 FUSION PROTEIN; HYBRID PROTEIN; ONCOPROTEIN; TMPRSS2 ERG FUSION PROTEIN; TRANSCRIPTION FACTOR E2F3; TRANSCRIPTION FACTOR ETS; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; EWING SARCOMA; GENE REPRESSION; GENETIC ASSOCIATION; GENETIC REGULATION; MUTATIONAL ANALYSIS; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; PROSTATE CANCER; PROTEIN BINDING;

APOPTOSIS; CELL CYCLE; CELL DIFFERENTIATION; CELL LINE, TUMOR; CELL PROLIFERATION; DNA-BINDING PROTEINS; E2F3 TRANSCRIPTION FACTOR; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MALE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; ONCOGENE PROTEINS, FUSION; PROMOTER REGIONS, GENETIC; PROSTATIC NEOPLASMS; PROTEIN BINDING; PROTO-ONCOGENE PROTEIN C-FLI-1; RNA-BINDING PROTEIN EWS; SARCOMA, EWING; SERINE ENDOPEPTIDASES; TRANS-ACTIVATORS;

EID: 84887455419     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.151340.112     Document Type: Article

References (42)

1. Chen H-Z, Tsai S-Y, Leone G. 2009. Emerging roles of E2Fs in cancer: An exit from cell cycle control. Nat Rev Cancer 9: 785-797.
2. Clark JP, Cooper CS. 2009. ETS gene fusions in prostate cancer. Nat Rev Urol 6: 429-439.
3. De Bleser P, Hooghe B, Vlieghe D, van Roy F. 2007. A distance difference matrix approach to identifying transcription factors that regulate differential gene expression. Genome Biol 8: R83.
4. Delattre O, Zucman J, Plougastel B, Desmaze C, Melot T, Peter M, Kovar H, Joubert I, De Jong P, Rouleau G. 1992. Gene fusion with an ETS DNAbinding domain caused by chromosome translocation in human tumours. Nature 359: 162-165.
5. DennisG Jr, Sherman BT, Hosack DA, Yang J, GaoW, Lane HC, Lempicki RA. 2003. DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome Biol 4: 3.
6. Forster A, Pannell R, Drynan L, Cano F, Chan N, Codrington R, Daser A, Lobato N, Metzler M, Nam CH, et al. 2005. Chromosomal translocation engineering to recapitulate primary events of human cancer. Cold Spring Harb Symp Quant Biol 70: 275-282.
7. Freedman JA, Chang JT, Jakoi L, Nevins JR. 2009. A combinatorial mechanism for determining the specificity of E2F activation and repression. Oncogene 28: 2873-2881.
8. Gangwal K, Lessnick SL. 2008. Microsatellites are EWS/FLI response elements: Genomic "junk" is EWS/FLI's treasure. Cell Cycle 7: 3127-3132.
9. Ginsberg JP, De Alava E, Ladanyi M, Wexler LH, Kovar H, Paulussen M, Zoubek A, Dockhorn-Dworniczak B, Juergens H,Wunder JS, et al. 1999. EWS-FLI1 and EWS-ERG gene fusions are associated with similar clinical phenotypes in Ewing's sarcoma. J Clin Oncol 17: 1809.
10. Guillon N, Tirode F, Boeva V, Zynovyev A, Barillot E, Delattre O. 2009. The oncogenic EWS-FLI1 protein binds in vivo GGAA microsatellite sequences with potential transcriptional activation function. PLoS ONE 4: e4932.
11. Gupta S, Iljin K, Sara H, Mpindi JP, Mirtti T, Vainio P, Rantala J, Alanen K, Nees M, Kallioniemi O. 2010. FZD4 as a mediator of ERG oncogeneinduced WNT signaling and epithelial-to-mesenchymal transition in human prostate cancer cells. Cancer Res 70: 6735-6745.
12. Hancock JD, Lessnick SL. 2008. A transcriptional profiling meta-analysis reveals a core EWS-FLI gene expression signature. Cell Cycle 7: 250-256.
13. Holmes E, Antti H. 2002. Chemometric contributions to the evolution of metabonomics: Mathematical solutions to characterising and interpreting complex biological NMR spectra. Analyst (Lond) 127: 1549-1557.
14. Hu-Lieskovan S, Zhang J, Wu L, Shimada H, Schofield DE, Triche TJ. 2005. EWS-FLI1 fusion protein up-regulates critical genes in neural crest development and is responsible for the observed phenotype of Ewing's family of tumors. Cancer Res 65: 4633-4644.
15. Izumi M, Yokoi M, Nishikawa NS, Miyazawa H, Sugino A, Yamagishi M, Yamaguchi M, Matsukage A, Yatagai F, Hanaoka F. 2000. Transcription of the catalytic 180-kDa subunit gene of mouse DNA polymerase a is controlled by E2F, an Ets-related transcription factor, and Sp1. Biochim Biophys Acta 1492: 341-352.
16. Joung JG, Shin D, Seong RH, Zhang BT. 2006. Identification of regulatory modules by co-clustering latent variable models: Stem cell differentiation. Bioinformatics 22: 2005-2011.
17. Kauer M, Ban J, Kofler R, Walker B, Davis S, Meltzer P, Kovar H. 2009. A molecular function map of Ewing's sarcoma. PLoS ONE 4: e5415.
18. Kovar H. 2010. Downstream EWS/FLI1-upstream Ewing's sarcoma. Genome Med 2: 8.
19. Kovar H, Aryee DN, Jug G, Henockl C, Schemper M, Delattre O, Thomas G, Gadner H. 1996. EWS/FLI-1 antagonists induce growth inhibition of Ewing tumor cells in vitro. Cell Growth Differ 7: 429-437.
20. Landt SG, Marinov GK, Kundaje A, Kheradpour P, Pauli F, Batzoglou S, Bernstein BE, Bickel P, Brown JB, Cayting P, et al. 2012. ChIP-seq guidelines and practices of the ENCODE and modENCODE consortia. Genome Res 22: 1813-1831.
21. Li R, Pei H,Watson DK. 2000. Regulation of Ets function by protein-protein interactions. Oncogene 19: 6514-6523.
22. Mahony S, Auron PE, Benos PV. 2007. DNA familial binding profiles made easy: Comparison of various motif alignment and clustering strategies. PLoS Comput Biol 3: e61.
23. Maier H, Colbert J, Fitzsimmons D, Clark DR, Hagman J. 2003. Activation of the early B-cell-specific mb-1 (Ig-a) gene by Pax-5 is dependent on an unmethylated Ets binding site. Mol Cell Biol 23: 1946-1960.
24. Mao X, Miesfeldt S, Yang H, Leiden JM, Thompson CB. 1994. The FLI-1 and chimeric EWS-FLI-1 oncoproteins display similar DNA binding specificities. J Biol Chem 269: 18216-18222.
25. Mirny LA. 2010. Nucleosome-mediated cooperativity between transcription factors. Proc Natl Acad Sci 107: 22534-22539.
26. Patel M, Simon JM, Iglesia MD, Wu SB, McFadden AW, Lieb JD, Davis IJ. 2012. Tumor-specific retargeting of an oncogenic transcription factor chimera results in dysregulation of chromatin and transcription. Genome Res 22: 259-270.
27. Prieur A, Tirode F, Cohen P, Delattre O. 2004. EWS/FLI-1 silencing and gene profiling of Ewing cells reveal downstream oncogenic pathways and a crucial role for repression of insulin-like growth factor binding protein 3. Mol Cell Biol 24: 7275-7283.
28. Quandt K, Frech K, Karas H, Wingender E, Werner T. 1995. MatInd and MatInspector: New fast and versatile tools for detection of consensus matches in nucleotide sequence data. Nucleic Acids Res 23: 4878-4884.
29. Rahim S, Beauchamp EM, Kong Y, Brown ML, Toretsky JA, Uren A. 2011. YK- 4-279 inhibits ERG and ETV1 mediated prostate cancer cell invasion. PLoS ONE 6: e19343.
30. Riggi N, Cironi L, Provero P, Suva ML, Kaloulis K, Garcia-Echeverria C, Hoffmann F, Trumpp A, Stamenkovic I. 2005. Development of Ewing's sarcoma from primary bone marrow-derived mesenchymal progenitor cells. Cancer Res 65: 11459-11468.
31. Riggi N, Suva ML, De Vito C, Provero P, Stehle JC, Baumer K, Cironi L, Janiszewska M, Petricevic T, Suva D, et al. 2010. EWS-FLI-1 modulates miRNA145 and SOX2 expression to initiate mesenchymal stem cell reprogramming toward Ewing sarcoma cancer stem cells. Genes Dev 24: 916-932.
32. Sankar S, Bell R, Stephens B, Zhuo R, Sharma S, Bearss DJ, Lessnick SL. 2012. Mechanism and relevance of EWS/FLI-mediated transcriptional repression in Ewing sarcoma. Oncogene doi: 10.1038/onc.2012.525.
33. Schlisio S, Halperin T, Vidal M, Nevins JR. 2002. Interaction of YY1 with E2Fs, mediated by RYBP, provides a mechanism for specificity of E2F function. EMBO J 21: 5775-5786.
34. Shirasaki F, Makhluf HA, LeRoy C, Watson DK, Trojanowska M. 1999. ETS transcription factors cooperate with Sp1 to activate the human tenascin- C promoter. Oncogene 18: 7755-7764.
35. Staege MS, Hutter C, Neumann I, Foja S, Hattenhorst UE, Hansen G, Afar D, Burdach SE. 2004. DNA microarrays reveal relationship of Ewing family tumors to both endothelial and fetal neural crest-derived cells and define novel targets. Cancer Res 64: 8213-8221.
36. Tirado OM, Mateo-Lozano S, Villar J, Dettin LE, Llort A, Gallego S, Ban J, Kovar H, Notario V. 2006. Caveolin-1 (CAV1) is a target of EWS/FLI-1 and a key determinant of the oncogenic phenotype and tumorigenicity of Ewing's sarcoma cells. Cancer Res 66: 9937-9947.
37. Tirode F, Laud-Duval K, Prieur A, Delorme B, Charbord P, Delattre O. 2007. Mesenchymal stem cell features of Ewing tumors. Cancer Cell 11: 421-429.
38. Tsai SY, Opavsky R, Sharma N, Wu L, Naidu S, Nolan E, Feria-Arias E, Timmers C, Opavska J, de Bruin A, et al. 2008. Mouse development with a single E2F activator. Nature 454: 1137-1141.
39. Watson DK, Robinson L, Hodge DR, Kola I, Papas TS, Seth A. 1997. FLI1 and EWS-FLI1 function as ternary complex factors and ELK1 and SAP1a function as ternary and quaternary complex factors on the Egr1 promoter serum response elements. Oncogene 14: 213-221.
40. Wu Z, Irizarry RA, Gentleman R, Martinez-Murillo F, Spencer F. 2004. A model-based background adjustment for oligonucleotide expression arrays. J Am Stat Assoc 99: 909-917.
41. Yang ZF, Mott S, Rosmarin AG. 2007. The ETS transcription factor GABP is required for cell-cycle progression. Nat Cell Biol 9: 339-346.
42. Yu J, Mani RS, Cao Q, Brenner CJ, Cao X,Wang X,Wu L, Li J, Hu M, Gong Y, et al. 2010. An integrated network of androgen receptor, Polycomb, and TMPRSS2-ERG gene fusions in prostate cancer progression. Cancer Cell 17: 443-454.