Chimeric EWSR1-FLI1 regulates the Ewing sarcoma susceptibility gene EGR2 via a GGAA microsatellite

Nature Genetics

Volumn 47, Issue 9, 2015, Pages 1073-1078

  Grünewald, Thomas G P ^a,n   Bernard, Virginie ^b   Gilardi Hebenstreit, Pascale ^c   Raynal, Virginie ^a,b   Surdez, Didier ^a   Aynaud, Marie Ming ^a   Mirabeau, Olivier ^a   Cidre Aranaz, Florencia ^d   Tirode, Franck ^a   Zaidi, Sakina ^a   Perot, Gaëlle ^e   Jonker, Anneliene H ^a   Lucchesi, Carlo ^a   Le Deley, Marie Cécile ^f   Oberlin, Odile ^f   Marec Bérard, Perrine ^g   Véron, Amélie S ^h   Reynaud, Stephanie ^b   Lapouble, Eve ^b   Boeva, Valentina ^i,j   Frio, Thomas Rio ^b   Alonso, Javier ^d   Bhatia, Smita ^k   Pierron, Gaëlle ^b   Cancel Tassin, Geraldine ^l   Cussenot, Olivier ^l   Cox, David G ^h   Morton, Lindsay M ^m   MacHiela, Mitchell J ^m   Chanock, Stephen J ^m   Charnay, Patrick ^c   Delattre, Olivier ^a,b   more..

^a INSTITUT CURIE   (France)

^b INSTITUT CURIE   (France)

^c ECOLE NORMALE SUPÉRIEURE   (France)

^d Ministry of Science and Innovation   (Spain)

^e INSTITUT BERGONIÉ   (France)

^f INSTITUT GUSTAVE ROUSSY   (France)

^g UNIVERSITÉ DE LYON   (France)

^h CENTRE DE RECHERCHE EN CANCÉROLOGIE DE LYON   (France)

ⁱ INSERM U900   (France)

^j PSL RESEARCH UNIVERSITY   (France)

^k UNIVERSITY OF ALABAMA SCHOOL OF MEDICINE   (United States)

^l HÔPITAL TENON   (France)

^m NATIONAL CANCER INSTITUTE   (United States)

ⁿ UNIVERSITY OF MUNICH   (Germany)

more..

Author keywords

[No Author keywords available]

Indexed keywords

EARLY GROWTH RESPONSE FACTOR 2; BETA-APOCAROTENOID-14',13'-DIOXYGENASE; CAROTENOID; EGR2 PROTEIN, HUMAN; EWS-FLI FUSION PROTEIN; MICROSATELLITE DNA; ONCOPROTEIN; OXYGENASE; RNA BINDING PROTEIN EWS; TRANSCRIPTION FACTOR FLI 1;

ALLELE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL VIABILITY; CHROMATIN IMMUNOPRECIPITATION; CLONOGENESIS; CONTROLLED STUDY; ENHANCER REGION; EWING SARCOMA; EWING SARCOMA CELL LINE; EWSR1 FLI1 GENE; GENE; GENE FREQUENCY; GENETIC ASSOCIATION; GENETIC SUSCEPTIBILITY; GGAA MOTIF; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN MOTIF; QUANTITATIVE TRAIT LOCUS; REAL TIME POLYMERASE CHAIN REACTION; SCHWANN CELL; SINGLE NUCLEOTIDE POLYMORPHISM; TUMOR XENOGRAFT; ANIMAL; BONE TUMOR; CANCER TRANSPLANTATION; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETIC ASSOCIATION STUDY; GENETIC PREDISPOSITION; GENETICS; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PATHOLOGY; SCID MOUSE; TUMOR CELL LINE; TUMOR VOLUME;

ANIMALS; BASE SEQUENCE; BONE NEOPLASMS; CAROTENOIDS; CELL LINE, TUMOR; CELL PROLIFERATION; EARLY GROWTH RESPONSE PROTEIN 2; GENE EXPRESSION; GENE EXPRESSION REGULATION, NEOPLASTIC; GENETIC ASSOCIATION STUDIES; GENETIC PREDISPOSITION TO DISEASE; HUMANS; MICE, SCID; MICROSATELLITE REPEATS; MOLECULAR SEQUENCE DATA; NEOPLASM TRANSPLANTATION; ONCOGENE PROTEINS, FUSION; OXYGENASES; POLYMORPHISM, SINGLE NUCLEOTIDE; PROTO-ONCOGENE PROTEIN C-FLI-1; QUANTITATIVE TRAIT LOCI; RNA-BINDING PROTEIN EWS; SARCOMA, EWING; TUMOR BURDEN;

EID: 84940568773     PISSN: 10614036     EISSN: 15461718     Source Type: Journal    
DOI: 10.1038/ng.3363     Document Type: Article

References (60)

1. Delattre, O. et al. Gene fusion with an ETS DNA-binding domain caused by chromosome translocation in human tumours. Nature 359, 162-165 (1992).
2. Gangwal, K. et al. Microsatellites as EWS/FLI response elements in Ewing's sarcoma. Proc. Natl. Acad. Sci. USA 105, 10149-10154 (2008).
3. Guillon, N. et al. The oncogenic EWS-FLI1 protein binds in vivo GGAA microsatellite sequences with potential transcriptional activation function. PLoS One 4, e4932 (2009).
4. Postel-Vinay, S. et al. Common variants near TARDBP and EGR2 are associated with susceptibility to Ewing sarcoma. Nat. Genet. 44, 323-327 (2012).
5. von Levetzow, C. et al. Modeling initiation of Ewing sarcoma in human neural crest cells. PLoS One 6, e19305 (2011).
6. Tirode, F. et al. Mesenchymal stem cell features of Ewing tumors. Cancer Cell 11, 421-429 (2007).
7. Delattre, O. et al. The Ewing family of tumors-A subgroup of small-round-cell tumors defned by specifc chimeric transcripts. N. Engl. J. Med. 331, 294-299 (1994).
8. Patel, M. et al. Tumor-specifc retargeting of an oncogenic transcription factor chimera results in dysregulation of chromatin and transcription. Genome Res. 22, 259-270 (2012).
9. Brohl, A.S. et al. The genomic landscape of the Ewing sarcoma family of tumors reveals recurrent STAG2 mutation. PLoS Genet. 10, e1004475 (2014).
10. Crompton, B.D. et al. The genomic landscape of pediatric Ewing sarcoma. Cancer Discov. 4, 1326-1341 (2014).
11. Tirode, F. et al. Genomic landscape of Ewing sarcoma defnes an aggressive subtype with co-association of STAG2 and TP53 mutations. Cancer Discov. 4, 1342-1353 (2014).
12. Worch, J. et al. Racial differences in the incidence of mesenchymal tumors associated with EWSR1 translocation. Cancer Epidemiol. Biomarkers Prev. 20, 449-453 (2011).
13. Chung, C.C. & Chanock, S.J. Current status of genome-wide association studies in cancer. Hum. Genet. 130, 59-78 (2011).
14. Dominy, J.E. Jr. et al. Discovery and characterization of a second mammalian thiol dioxygenase, cysteamine dioxygenase. J. Biol. Chem. 282, 25189-25198 (2007).
15. Chandra, A., Lan, S., Zhu, J., Siclari, V.A. & Qin, L. Epidermal growth factor receptor (EGFR) signaling promotes proliferation and survival in osteoprogenitors by increasing early growth response 2 (EGR2) expression. J. Biol. Chem. 288, 20488-20498 (2013).
16. Topilko, P. et al. Krox-20 controls myelination in the peripheral nervous system. Nature 371, 796-799 (1994).
17. Mackintosh, C., Madoz-Gúrpide, J., Ordóñez, J.L., Osuna, D. & Herrero-Martín, D. The molecular pathogenesis of Ewing's sarcoma. Cancer Biol. Ther. 9, 655-667 (2010).
18. Gao, C. et al. HEFT: eQTL analysis of many thousands of expressed genes while simultaneously controlling for hidden factors. Bioinformatics 30, 369-376 (2014).
19. Radtke, I. et al. Genomic analysis reveals few genetic alterations in pediatric acute myeloid leukemia. Proc. Natl. Acad. Sci. USA 106, 12944-12949 (2009).
20. Moffatt, M.F. et al. Genetic variants regulating ORMDL3 expression contribute to the risk of childhood asthma. Nature 448, 470-473 (2007).
21. Northcott, P.A. et al. Subgroup-specifc structural variation across 1,000 medulloblastoma genomes. Nature 488, 49-56 (2012).
22. Wang, K. et al. Integrative genomics identifes LMO1 as a neuroblastoma oncogene. Nature 469, 216-220 (2011).
23. GTEx Consortium. The Genotype-Tissue Expression (GTEx) project. Nat. Genet. 45, 580-585 (2013).
24. Labalette, C. et al. Hindbrain patterning requires fne-tuning of early krox20 transcription by Sprouty 4. Development 138, 317-326 (2011).
25. Weisinger, K., Kayam, G., Missulawin-Drillman, T. & Sela-Donenfeld, D. Analysis of expression and function of FGF-MAPK signaling components in the hindbrain reveals a central role for FGF3 in the regulation of Krox20, mediated by Pea3. Dev. Biol. 344, 881-895 (2010).
26. ENCODE Project Consortium. et al. An integrated encyclopedia of DNA elements in the human genome. Nature 489, 57-74 (2012).
27. Riggi, N. et al. EWS-FLI1 utilizes divergent chromatin remodeling mechanisms to directly activate or repress enhancer elements in Ewing sarcoma. Cancer Cell 26, 668-681 (2014).
28. Ernst, J. et al. Mapping and analysis of chromatin state dynamics in nine human cell types. Nature 473, 43-49 (2011).
29. Maurano, M.T. et al. Systematic localization of common disease-associated variation in regulatory DNA. Science 337, 1190-1195 (2012).
30. Ghislain, J. et al. Characterisation of cis-acting sequences reveals a biphasic, axon-dependent regulation of Krox20 during Schwann cell development. Development 129, 155-166 (2002).
31. 1000 Genomes Project Consortium. et al. An integrated map of genetic variation from 1,092 human genomes. Nature 491, 56-65 (2012).
32. Robison, L.L. et al. The Childhood Cancer Survivor Study: a National Cancer Institute-supported resource for outcome and intervention research. J. Clin. Oncol. 27, 2308-2318 (2009).
33. Edwards, S.L., Beesley, J., French, J.D. & Dunning, A.M. Beyond GWASs: illuminating the dark road from association to function. Am. J. Hum. Genet. 93, 779-797 (2013).
34. Faye, L.L., Machiela, M.J., Kraft, P. , Bull, S.B. & Sun, L. Re-ranking sequencing variants in the post-GWAS era for accurate causal variant identifcation. PLoS Genet. 9, e1003609 (2013).
35. Surdez, D. et al. Targeting the EWSR1-FLI1 oncogene-induced protein kinase PKC-β abolishes Ewing sarcoma growth. Cancer Res. 72, 4494-4503 (2012).
36. International HapMap 3 Consortium. et al. Integrating common and rare genetic variation in diverse human populations. Nature 467, 52-58 (2010).
37. Robinson, J.T. et al. Integrative genomics viewer. Nat. Biotechnol. 29, 24-26 (2011).
38. Carrillo, J. et al. Cholecystokinin down-regulation by RNA interference impairs Ewing tumor growth. Clin. Cancer Res. 13, 2429-2440 (2007).
39. Conrad, C., Gottgens, B., Kinston, S., Ellwart, J. & Huss, R. GATA transcription in a small rhodamine 123(low)CD34(+) subpopulation of a peripheral blood-derived CD34(-)CD105(+) mesenchymal cell line. Exp. Hematol. 30, 887-895 (2002).
40. Thalmeier, K. et al. Establishment of two permanent human bone marrow stromal cell lines with long-term post irradiation feeder capacity. Blood 83, 1799-1807 (1994).
41. Wiederschain, D. et al. Single-vector inducible lentiviral RNAi system for oncology target validation. Cell Cycle 8, 498-504 (2009).
42. Dai, M. et al. Evolving gene/transcript defnitions signifcantly alter the interpretation of GeneChip data. Nucleic Acids Res. 33, e175 (2005).
43. Culhane, A.C., Thioulouse, J., Perrière, G. & Higgins, D.G. MADE4: an R package for multivariate analysis of gene expression data. Bioinformatics 21, 2789-2790 (2005).
44. Melot, T. et al. Production and characterization of mouse monoclonal antibodies to wild-type and oncogenic FLI-1 proteins. Hybridoma 16, 457-464 (1997).
45. Sievers, F. et al. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol. Syst. Biol. 7, 539 (2011).
46. Franken, N.A.P., Rodermond, H.M., Stap, J., Haveman, J. & van Bree, C. Clonogenic assay of cells in vitro. Nat. Protoc. 1, 2315-2319 (2006).
47. Boeva, V. et al. De novo motif identifcation improves the accuracy of predicting transcription factor binding sites in ChIP-Seq data analysis. Nucleic Acids Res. 38, e126 (2010).
48. Yeager, M. et al. Genome-wide association study of prostate cancer identifes a second risk locus at 8q24. Nat. Genet. 39, 645-649 (2007).
49. Li, H. et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25, 2078-2079 (2009).
50. McKenna, A. et al. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20, 1297-1303 (2010).
51. Pruim, R.J. et al. LocusZoom: regional visualization of genome-wide association scan results. Bioinformatics 26, 2336-2337 (2010).
52. Barrett, J.C., Fry, B., Maller, J. & Daly, M.J. Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 21, 263-265 (2005).
53. Purcell, S. et al. PLINK: a tool set for whole-genome association and population-based linkage analyses. Am. J. Hum. Genet. 81, 559-575 (2007).
54. Gabriel, S.B. et al. The structure of haplotype blocks in the human genome. Science 296, 2225-2229 (2002).
55. Clavel-Chapelon, F. et al. E3N, a French cohort study on cancer risk factors. E3N Group. Etude Epidémiologique auprès de femmes de l'Education Nationale. Eur. J. Cancer Prev. 6, 473-478 (1997).
56. Wang, Z. et al. Improved imputation of common and uncommon SNPs with a new reference set. Nat. Genet. 44, 6-7 (2012).
57. Howie, B.N., Donnelly, P. & Marchini, J. A fexible and accurate genotype imputation method for the next generation of genome-wide association studies. PLoS Genet. 5, e1000529 (2009).
58. Boeva, V., Lermine, A., Barette, C., Guillouf, C. & Barillot, E. Nebula-A web-server for advanced ChIP-seq data analysis. Bioinformatics 28, 2517-2519 (2012).
59. Zhang, Y. et al. Model-based analysis of ChIP-Seq (MACS). Genome Biol. 9, R137 (2008).
60. Meyer, L.R. et al. The UCSC Genome Browser database: extensions and updates 2013. Nucleic Acids Res. 41, D64-D69 (2013).