The synovial sarcoma-associated SYT-SSX2 oncogene antagonizes the polycomb complex protein Bmi1

PLoS ONE

Volumn 4, Issue 4, 2009, Pages

  Barco, Roy ^a   Garcia, Christina B ^a   Eid, Josiane E ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BMI1 PROTEIN; CHIMERIC PROTEIN; HISTONE H2A; ONCOPROTEIN; SYNOVIAL SARCOMA ASSOCIATE PROTEIN 1; SYNOVIAL SARCOMA ASSOCIATE PROTEIN 2; UNCLASSIFIED DRUG; BMI1 PROTEIN, HUMAN; HISTONE; NUCLEAR PROTEIN; PRIMER DNA; REPRESSOR PROTEIN; SYT SSX FUSION PROTEIN; SYT-SSX FUSION PROTEIN;

ANIMAL CELL; ARTICLE; CARCINOGENESIS; CONTROLLED STUDY; GENE ACTIVATION; GENE ACTIVITY; GENE EXPRESSION; GENE FUNCTION; GENE INTERACTION; GENE SILENCING; GENE TARGETING; GENE TRANSLOCATION; GENETIC ASSOCIATION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PROTEIN QUATERNARY STRUCTURE; SYNOVIAL SARCOMA; UBIQUITINATION; CHROMATIN IMMUNOPRECIPITATION; CONNECTIVE TISSUE TUMOR; DRUG ANTAGONISM; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; METABOLISM; NUCLEOTIDE SEQUENCE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR CELL LINE;

BASE SEQUENCE; CELL LINE, TUMOR; CHROMATIN IMMUNOPRECIPITATION; DNA PRIMERS; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; HISTONES; HUMANS; NUCLEAR PROTEINS; ONCOGENE PROTEINS, FUSION; PROTO-ONCOGENE PROTEINS; REPRESSOR PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SARCOMA, SYNOVIAL; UBIQUITINATION;

EID: 64249153080     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0005060     Document Type: Article

References (40)

1. Sparmann A, van Lohuizen M (2006) Polycomb silencers control cell fate, development and cancer. Nat Rev Cancer 6: 846-856.
2. Ringrose L, Paro R (2004) Epigenetic regulation of cellular memory by the Polycomb and Trithorax group proteins. Annu Rev Genet 38: 413-443.
3. van der Vlag J, Otte AP (1999) Transcriptional repression mediated by the human polycomb-group protein EED involves histone deacetylation. Nat Genet 23: 474-478.
4. Viré E, Brenner C, Deplus R, Blanchon L, Fraga M, et al. (2006) The Polycomb group protein EZH2 directly controls DNA methylation. Nature 439: 871-874.
5. Czermin B, Melfi R, McCabe D, Seitz V, Imhof A, Pirrotta V (2002) Drosophila enhancer of Zeste/ESC complexes have a histone H3 methyltransferase activity that marks chromosomal Polycomb sites. Cell 111: 185-196.
6. Müller J, Hart CM, Francis NJ, Vargas ML, Sengupta A, et al. (2002) Histone methyltransferase activity of a Drosophila Polycomb group repressor complex. Cell 111: 197-208.
7. Pasquale EB (2005) Eph receptor signaling casts a wide net on cell behavior. Nat Rev Mol Cell Biol 6: 462-475.
8. Cao R, Tsukada Y, Zhang Y (2005) Role of Bmi-1 and Ring1A in H2A ubiquitylation and Hox gene silencing. Mol Cell 20: 845-854.
9. Boyer LA, Plath K, Zeitlinger J, Brambrink T, Medeiros, et al. (2006) Polycomb complexes repress developmental regulators in murine embryonic stem cells. Nature 441: 349-353.
10. Bracken AP, Dietrich N, Pasini D, Hansen KH, Helin K (2006) Genome-wide mapping of Polycomb target genes unravels their roles in cell fate transitions. Genes Dev 20: 1123-1136.
11. Lee TI, Jenner RG, Boyer LA, Guenther MG, Levine SS, et al. (2006) Control of developmental regulators by Polycomb in human embryonic stem cells. Cell 125: 301-313.
12. Leung C, Lingbeek M, Shakhova O, Liu J, Tanger E, et al. (2004) Bmi1 is essential for cerebellar development and is overexpressed in human medulloblastomas. Nature 428: 337-341.
13. Varambally S, Dhanasekaran SM, Zhou M, Barrette TR, Kumar-Sinha C, et al. (2002) The polycomb group protein EZH2 is involved in progression of prostate cancer. Nature 419: 624-629.
14. Kirmizis A, Bartley SM, Farnham PJ (2003) Identification of the polycomb group protein SU(Z)12 as a potential molecular target for human cancer therapy. Mol Cancer Ther 2: 113-121.
15. Jacobs JJ, Kieboom K, Marino S, DePinho RA, van Lohuizen M (1999) The oncogene and Polycomb-group gene bmi-1 regulates cell proliferation and senescence through the ink4a locus. Nature 397: 164-168.
16. Sánchez-Beato M, Sánchez E, González-Carreró J, Morente M, Díez A, et al. (2006) Variability in the expression of polycomb proteins in different normal and tumoral tissues. A pilot study using tissue microarrays. Mod Pathol 19: 684-694.
17. Guo WJ, Zeng MS, Yadav A, Song LB, Guo BH, et al. (2007) Mel-18 acts as a tumor suppressor by repressing Bmi-1 expression and down-regulating Akt activity in breast cancer cells. Cancer Res 67: 5083-5089.
18. Vider BZ, Zimber A, Chastre E, Gespach C, Halperin M, et al. (2000) Deregulated expression of homeobox-containing genes, HOXB6, B8, C8, C9, and Cdx-1, in human colon cancer cell lines. Biochem. Biophys Res Commun 272: 513-518.
19. Abramovich C, Pineault N, Ohta H, Humphries RK (2005) Hox genes: from leukemia to hematopoietic stem cell expansion. Ann N Y Acad Sci 1044: 109-116.
20. Satijn DP, Gunster MJ, van der Vlag J, Hamer KM, Schul W, et al. (1997) RING1 is associated with the polycomb group protein complex and acts as a transcriptional repressor. Mol Cell Biol 17: 4105-4113.
21. Zhu P, Zhou W, Wang J, Puc J, Ohgi KA, et al. (2007) A histone H2A deubiquitinase complex coordinating histone acetylation and H1 dissociation in transcriptional regulation. Mol Cell 27: 609-621.
22. Clark J, Rocques PJ, Crew AJ, Gill S, Shipley J, et al. (1994) Identification of novel genes, SYT and SSX, involved in the t(X;18) (p11.2;q11.2) translocation found in human synovial sarcoma. Nat Genet 7: 502-508.
23. Nagai M, Tanaka S, Tsuda M, Endo S, Kato H, et al. (2001) Analysis of transforming activity of human synovial sarcoma-associated chimeric protein SYT-SSX1 bound to chromatin remodeling factor hBRM/hSNF2 alpha. Proc Natl Acad Sci U S A 98: 3843-3848.
24. Haldar M, Hancock JD, Coffin CM, Lessnick SL, Capecchi MR (2007) A conditional mouse model of synovial sarcoma: insights into a myogenic origin. Cancer Cell 11: 375-388.
25. Barco R, Hun LB, Frump AL, Garcia CB, Benesh A, et al. (2007) The synovial sarcoma SYT-SSX2 oncogene remodels the cytoskeleton through activation of the ephrin pathway. Mol Biol Cell 18: 4003-4012.
26. Thaete C, Brett D, Monaghan P, Whitehouse S, Rennie G, et al. (1999) Functional domains of the SYT and SYT-SSX synovial sarcoma translocation proteins and co-localization with the SNF protein BRM in the nucleus. Hum Mol Genet 8: 585-591.
27. Kato H, Tjernberg A, Zhang W, Krutchinsky AN, An W, et al. (2002) SYT associates with human SNF/SWI complexes and the C-terminal region of its fusion partner SSX1 targets histones. J Biol Chem 277: 5498-5505.
28. Perani M, Ingram CJ, Cooper CS, Garrett MD, Goodwin GH (2003) Conserved SNH domain of the proto-oncoprotein SYT interacts with components of the human chromatin remodelling complexes, while the QPGY repeat domain forms homo-oligomers. Oncogene 22: 8156-8167.
29. Eid JE, Kung AL, Scully R, Livingston DM (2000) p300 interacts with the nuclear proto-oncoprotein SYT as part of the active control of cell adhesion. Cell 102: 839-848.
30. Soulez M, Saurin AJ, Freemont PS, Knight JC (1999) SSX and the synovial-sarcoma specific chimaeric protein SYT-SSX co-localize with the human Polycomb group complex. Oncogene 18: 2739-2746.
31. Lubieniecka JM, de Bruijn DR, Su L, van Dijk AH, Subramanian S, et al. (2008) Histone deacetylase inhibitors reverse SS18-SSX-mediated polycomb silencing of the tumor suppressor early growth response 1 in synovial sarcoma. Cancer Res 68: 4303-4310.
32. de bruijn DR, Allander SV, van Dijk AH, Willemse MP, Thijssen J, et al. (2006) The synovial-sarcoma-associated SS18-SSX2 fusion protein induces epigenetic gene (de)regulation. Cancer Res 66: 9474-9482.
33. Nielsen TO, West RB, Linn, Alter O, Knowling MA, et al. (2002) SC Molecular characterization of soft tissue tumors: a gene expression study. Lancet 359: 1301-1307.
34. Nagayama S, Katagiri T, Tsunoda T, Hosaka T, Nakashima Y, et al. (2002) Genome-wide analysis of gene expression in synovial sarcomas using a cDNA microarray. Cancer Res 62: 5859-5866.
35. lee Y-F, John M, Edwards S, Clark J, Flohr P, et al. (2003) Molecular classification of synovial sarcomas, leiomyosarcomas and malignant fibrous histiocytomas by gene expression profiling. Br J Cancer 88: 510-515.
36. Subramaniam MM, Navarro S, Pellin A, Lopez-Guerrero JA, Carda C, et al. (2006) Tissue microarray profiling of primary and xenotransplanted synovial sarcomas demonstrates the immunophenotypic similarities existing between SYT-SSX fusion gene confirmed, biphasic, and monophasic fibrous variants. Virchows Arch 449: 435-447.
37. Nielsen TO, Hsu FD, O'Connell JX, Gilks CB, Sorensen PH, et al. (2003) Tissue microarray validation of epidermal growth factor receptor and SALL2 in synovial sarcoma with comparison to tumors of similar histology. Am J Pathol 163: 1449-1456.
38. Wu F, Stutzman A, Mo YY (2007) Notch signaling and its role in breast cancer. Front Biosci 12: 4370-4383.
39. Pretto D, Barco R, Rivera J, Neel N, Gustavson MD, Eid JE (2006) The synovial sarcoma translocation protein SYT-SSX2 recruits beta-catenin to the nucleus and associates with it in an active complex. Oncogene 25: 3661-3669.
40. Boyer LA, Lee TI, Cole MF, Jhonstone SE, Levine SS, et al. (2005) Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 122: 947-956.