EWS-FLI1Utilizes Divergent Chromatin Remodeling Mechanisms to Directly Activate or Repress Enhancer Elements in Ewing Sarcoma

Cancer Cell

Volumn 26, Issue 5, 2014, Pages 668-681

  Riggi, Nicolò ^a,b   Knoechel, Birgit ^a,b,c,d   Gillespie, Shawn M ^a,b,e   Rheinbay, Esther ^a,b   Boulay, Gaylor ^a,b   Suvà, Mario L ^a,b   Rossetti, Nikki E ^a   Boonseng, Wannaporn E ^a   Oksuz, Ozgur ^a   Cook, Edward B ^a   Formey, Aurélie ^f   Patel, Anoop ^a,e   Gymrek, Melissa ^b,g,h   Thapar, Vishal ⁱ   Deshpande, Vikram ^a   Ting, David T ⁱ   Hornicek, Francis J ^a   Nielsen, G Petur ^a   Stamenkovic, Ivan ^f   Aryee, Martin J ^a,b   Bernstein, Bradley E ^a,b,e   Rivera, Miguel N ^a,b   more..

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^c DANA FARBER CANCER INSTITUTE   (United States)

^d BOSTON CHILDREN S HOSPITAL   (United States)

^e HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^f LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^g WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

^h MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

ⁱ HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN KINASE C BETA; TRANSCRIPTION FACTOR ELF 1; EWS-FLI FUSION PROTEIN; ONCOPROTEIN; PROTEIN BINDING; RNA BINDING PROTEIN EWS; TRANSCRIPTION FACTOR FLI 1;

ARTICLE; BINDING SITE; CANCER SURVIVAL; CELL CYCLE; CELL DIFFERENTIATION; CELL SURVIVAL; CELL TYPE; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DEVELOPMENT; DNA SEQUENCE; ENHANCER REGION; EWING SARCOMA; EWING SARCOMA CELL LINE; G2 PHASE CELL CYCLE CHECKPOINT; GENE ACTIVATION; GENE EXPRESSION; GENETIC CONSERVATION; HISTONE ACETYLATION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; MESENCHYMAL STEM CELL; ONCOGENE; PRIMARY TUMOR; WILD TYPE; ANIMAL; BONE TUMOR; CANCER TRANSPLANTATION; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; NONOBESE DIABETIC MOUSE; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; SCID MOUSE; TUMOR CELL LINE;

ANIMALS; BASE SEQUENCE; BONE NEOPLASMS; CELL LINE, TUMOR; CHROMATIN ASSEMBLY AND DISASSEMBLY; ENHANCER ELEMENTS, GENETIC; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MICE, INBRED NOD; MICE, SCID; NEOPLASM TRANSPLANTATION; ONCOGENE PROTEINS, FUSION; PROTEIN BINDING; PROTO-ONCOGENE PROTEIN C-FLI-1; RNA-BINDING PROTEIN EWS; SARCOMA, EWING;

EID: 84912064689     PISSN: 15356108     EISSN: 18783686     Source Type: Journal    
DOI: 10.1016/j.ccell.2014.10.004     Document Type: Article

References (50)

1. Abecasis G.R., Auton A., Brooks L.D., DePristo M.A., Durbin R.M., Handsaker R.E., Kang H.M., Marth G.T., McVean G.A. An integrated map of genetic variation from 1,092 human genomes. Nature 2012, 491:56-65. 1000 Genomes Project Consortium.
2. Aiden A.P., Rivera M.N., Rheinbay E., Ku M., Coffman E.J., Truong T.T., Vargas S.O., Lander E.S., Haber D.A., Bernstein B.E. Wilms tumor chromatin profiles highlight stem cell properties and a renal developmental network. Cell Stem Cell 2010, 6:591-602.
3. Arnason T., Pino M.S., Yilmaz O., Kirley S.D., Rueda B.R., Chung D.C., Zukerberg L.R. Cables1 is a tumor suppressor gene that regulates intestinal tumor progression in Apc(Min) mice. Cancer Biol. Ther. 2013, 14:672-678.
4. Baylin S.B., Jones P.A. A decade of exploring the cancer epigenome - biological and translational implications. Nat. Rev. Cancer 2011, 11:726-734.
5. Beck R., Monument M.J., Watkins W.S., Smith R., Boucher K.M., Schiffman J.D., Jorde L.B., Randall R.L., Lessnick S.L. EWS/FLI-responsive GGAA microsatellites exhibit polymorphic differences between European and African populations. Cancer genetics 2012, 205:304-312.
6. Bilke S., Schwentner R., Yang F., Kauer M., Jug G., Walker R.L., Davis S., Zhu Y.J., Pineda M., Meltzer P.S., Kovar H. Oncogenic ETS fusions deregulate E2F3 target genes in Ewing sarcoma and prostate cancer. Genome Res. 2013, 23:1797-1809.
7. Chamberlain G., Fox J., Ashton B., Middleton J. Concise review: mesenchymal stem cells: their phenotype, differentiation capacity, immunological features, and potential for homing. Stem Cells 2007, 25:2739-2749.
8. Cobaleda C., Pérez-Caro M., Vicente-Dueñas C., Sánchez-García I. Function of the zinc-finger transcription factor SNAI2 in cancer and development. Annu. Rev. Genet. 2007, 41:41-61.
9. Delattre O., Zucman J., Plougastel B., Desmaze C., Melot T., Peter M., Kovar H., Joubert I., de Jong P., Rouleau G., et al. Gene fusion with an ETS DNA-binding domain caused by chromosome translocation in human tumours. Nature 1992, 359:162-165.
10. Di C., Liao S., Adamson D.C., Parrett T.J., Broderick D.K., Shi Q., Lengauer C., Cummins J.M., Velculescu V.E., Fults D.W., et al. Identification of OTX2 as a medulloblastoma oncogene whose product can be targeted by all-trans retinoic acid. Cancer Res. 2005, 65:919-924.
11. Duncan C.G., Killela P.J., Payne C.A., Lampson B., Chen W.C., Liu J., Solomon D., Waldman T., Towers A.J., Gregory S.G., et al. Integrated genomic analyses identify ERRFI1 and TACC3 as glioblastoma-targeted genes. Oncotarget 2010, 1:265-277.
12. An integrated encyclopedia of DNA elements in the human genome. Nature 2012, 489:57-74. ENCODE Project Consortium.
13. Gangwal K., Sankar S., Hollenhorst P.C., Kinsey M., Haroldsen S.C., Shah A.A., Boucher K.M., Watkins W.S., Jorde L.B., Graves B.J., Lessnick S.L. Microsatellites as EWS/FLI response elements in Ewing's sarcoma. Proc. Natl. Acad. Sci. USA 2008, 105:10149-10154.
14. Gangwal K., Close D., Enriquez C.A., Hill C.P., Lessnick S.L. Emergent Properties of EWS/FLI Regulation via GGAA Microsatellites in Ewing's Sarcoma. Genes & cancer 2010, 1:177-187.
15. Guillon N., Tirode F., Boeva V., Zynovyev A., Barillot E., Delattre O. The oncogenic EWS-FLI1 protein binds invivo GGAA microsatellite sequences with potential transcriptional activation function. PLoS ONE 2009, 4:e4932.
16. Hollenhorst P.C., McIntosh L.P., Graves B.J. Genomic and biochemical insights into the specificity of ETS transcription factors. Annu. Rev. Biochem. 2011, 80:437-471.
17. Kadoch C., Crabtree G.R. Reversible disruption of mSWI/SNF (BAF) complexes by the SS18-SSX oncogenic fusion in synovial sarcoma. Cell 2013, 153:71-85.
18. Kaikkonen M.U., Spann N.J., Heinz S., Romanoski C.E., Allison K.A., Stender J.D., Chun H.B., Tough D.F., Prinjha R.K., Benner C., Glass C.K. Remodeling of the enhancer landscape during macrophage activation is coupled to enhancer transcription. Mol. Cell 2013, 51:310-325.
19. Kim I.J., Quigley D., To M.D., Pham P., Lin K., Jo B., Jen K.Y., Raz D., Kim J., Mao J.H., et al. Rewiring of human lung cell lineage and mitotic networks in lung adenocarcinomas. Nat. Commun. 2013, 4:1701.
20. Ku M., Koche R.P., Rheinbay E., Mendenhall E.M., Endoh M., Mikkelsen T.S., Presser A., Nusbaum C., Xie X., Chi A.S., et al. Genomewide analysis of PRC1 and PRC2 occupancy identifies two classes of bivalent domains. PLoS Genet. 2008, 4:e1000242.
21. Lawrence M.S., Stojanov P., Polak P., Kryukov G.V., Cibulskis K., Sivachenko A., Carter S.L., Stewart C., Mermel C.H., Roberts S.A., et al. Mutational heterogeneity in cancer and the search for new cancer-associated genes. Nature 2013, 499:214-218.
22. Lee T.I., Young R.A. Transcriptional regulation and its misregulation in disease. Cell 2013, 152:1237-1251.
23. Margueron R., Reinberg D. The Polycomb complex PRC2 and its mark in life. Nature 2011, 469:343-349.
24. Mikkelsen T.S., Ku M., Jaffe D.B., Issac B., Lieberman E., Giannoukos G., Alvarez P., Brockman W., Kim T.K., Koche R.P., et al. Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 2007, 448:553-560.
25. Molitor T.P., Traktman P. Molecular genetic analysis of VRK1 in mammary epithelial cells: depletion slows proliferation invitro and tumor growth and metastasis invivo. Oncogenesis 2013, 2:e48.
26. Morris E.J., Michaud W.A., Ji J.Y., Moon N.S., Rocco J.W., Dyson N.J. Functional identification of Api5 as a suppressor of E2F-dependent apoptosis invivo. PLoS Genet. 2006, 2:e196.
27. Patel M., Simon J.M., Iglesia M.D., Wu S.B., McFadden A.W., Lieb J.D., Davis I.J. Tumor-specific retargeting of an oncogenic transcription factor chimera results in dysregulation of chromatin and transcription. Genome Res. 2012, 22:259-270.
28. Ramakrishnan R., Fujimura Y., Zou J.P., Liu F., Lee L., Rao V.N., Reddy E.S. Role of protein-protein interactions in the antiapoptotic function of EWS-Fli-1. Oncogene 2004, 23:7087-7094.
29. Riggi N., Stamenkovic I. The Biology of Ewing sarcoma. Cancer Lett. 2007, 254:1-10.
30. Riggi N., Cironi L., Provero P., Suvà M.L., Kaloulis K., Garcia-Echeverria C., Hoffmann F., Trumpp A., Stamenkovic I. Development of Ewing's sarcoma from primary bone marrow-derived mesenchymal progenitor cells. Cancer Res. 2005, 65:11459-11468.
31. Riggi N., Suvà M.L., Suvà D., Cironi L., Provero P., Tercier S., Joseph J.M., Stehle J.C., Baumer K., Kindler V., Stamenkovic I. EWS-FLI-1 expression triggers a Ewing's sarcoma initiation program in primary human mesenchymal stem cells. Cancer Res. 2008, 68:2176-2185.
32. Riggi N., Suvà M.L., De Vito C., Provero P., Stehle J.C., Baumer K., Cironi L., Janiszewska M., Petricevic T., Suvà D., et al. EWS-FLI-1 modulates miRNA145 and SOX2 expression to initiate mesenchymal stem cell reprogramming toward Ewing sarcoma cancer stem cells. Genes Dev. 2010, 24:916-932.
33. Riveiro-Falkenbach E., Soengas M.S. Control of tumorigenesis and chemoresistance by the DEK oncogene. Clinical cancer research 2010, 16:2932-2938.
34. Roberts C.W., Galusha S.A., McMenamin M.E., Fletcher C.D., Orkin S.H. Haploinsufficiency of Snf5 (integrase interactor 1) predisposes to malignant rhabdoid tumors in mice. Proc. Natl. Acad. Sci. USA 2000, 97:13796-13800.
35. Sanchez G., Delattre O., Auboeuf D., Dutertre M. Coupled alteration of transcription and splicing by a single oncogene: boosting the effect on cyclin D1 activity. Cell Cycle 2008, 7:2299-2305.
36. Schwartzentruber J., Korshunov A., Liu X.Y., Jones D.T., Pfaff E., Jacob K., Sturm D., Fontebasso A.M., Quang D.A., Tönjes M., et al. Driver mutations in histone H3.3 and chromatin remodelling genes in paediatric glioblastoma. Nature 2012, 482:226-231.
37. Sebens Müerköster S., Rausch A.V., Isberner A., Minkenberg J., Blaszczuk E., Witt M., Fölsch U.R., Schmitz F., Schäfer H., Arlt A. The apoptosis-inducing effect of gastrin on colorectal cancer cells relates to an increased IEX-1 expression mediating NF-kappa B inhibition. Oncogene 2008, 27:1122-1134.
38. Smith R., Owen L.A., Trem D.J., Wong J.S., Whangbo J.S., Golub T.R., Lessnick S.L. Expression profiling of EWS/FLI identifies NKX2.2 as a critical target gene in Ewing's sarcoma. Cancer Cell 2006, 9:405-416.
39. Smith E., Lin C., Shilatifard A. The super elongation complex (SEC) and MLL in development and disease. Genes Dev. 2011, 25:661-672.
40. Surdez D., Benetkiewicz M., Perrin V., Han Z.Y., Pierron G., Ballet S., Lamoureux F., Rédini F., Decouvelaere A.V., Daudigeos-Dubus E., et al. Targeting the EWSR1-FLI1 oncogene-induced protein kinase PKC-β abolishes ewing sarcoma growth. Cancer Res. 2012, 72:4494-4503.
41. Tanaka M., Yamazaki Y., Kanno Y., Igarashi K., Aisaki K., Kanno J., Nakamura T. Ewing's sarcoma precursors are highly enriched in embryonic osteochondrogenic progenitors. J.Clin. Invest. 2014, 124:3061-3074.
42. Willems T., Gymrek M., Highnam G., The 1000 Genomes Project Consortium, Mittelman D., Erlich Y. The landscape of human STR variation. Genome Res. 2014, Published online August 18, 2014. 10.1101/gr.177774.114.
43. Thurman R.E., Rynes E., Humbert R., Vierstra J., Maurano M.T., Haugen E., Sheffield N.C., Stergachis A.B., Wang H., Vernot B., et al. The accessible chromatin landscape of the human genome. Nature 2012, 489:75-82.
44. Torchia E.C., Jaishankar S., Baker S.J. Ewing tumor fusion proteins block the differentiation of pluripotent marrow stromal cells. Cancer Res. 2003, 63:3464-3468.
45. Valbuena A., Sanz-García M., López-Sánchez I., Vega F.M., Lazo P.A. Roles of VRK1 as a new player in the control of biological processes required for cell division. Cell. Signal. 2011, 23:1267-1272.
46. Vicente-Dueñas C., Romero-Camarero I., González-Herrero I., Alonso-Escudero E., Abollo-Jiménez F., Jiang X., Gutierrez N.C., Orfao A., Marín N., Villar L.M., et al. A novel molecular mechanism involved in multiple myeloma development revealed by targeting MafB to haematopoietic progenitors. EMBO J. 2012, 31:3704-3717.
47. Visel A., Rubin E.M., Pennacchio L.A. Genomic views of distant-acting enhancers. Nature 2009, 461:199-205.
48. Wang N., Zhang H., Yao Q., Wang Y., Dai S., Yang X. TGFBI promoter hypermethylation correlating with paclitaxel chemoresistance in ovarian cancer. J.Exp. Clin. Cancer Res. 2012, 31:6.
49. Wei G.H., Badis G., Berger M.F., Kivioja T., Palin K., Enge M., Bonke M., Jolma A., Varjosalo M., Gehrke A.R., et al. Genome-wide analysis of ETS-family DNA-binding invitro and invivo. EMBO J. 2010, 29:2147-2160.
50. Zhang Y., Xie R.L., Gordon J., LeBlanc K., Stein J.L., Lian J.B., van Wijnen A.J., Stein G.S. Control of mesenchymal lineage progression by microRNAs targeting skeletal gene regulators Trps1 and Runx2. J.Biol. Chem. 2012, 287:21926-21935.