Deconstruction of the SS18-SSX Fusion Oncoprotein Complex: Insights into Disease Etiology and Therapeutics

Cancer Cell

Volumn 21, Issue 3, 2012, Pages 333-347

  Su, Le ^a   Sampaio, Arthur V ^a   Jones, Kevin B ^c   Pacheco, Marina ^b   Goytain, Angela ^b   Lin, Shujun ^a   Poulin, Neal ^b   Yi, Lin ^a   Rossi, Fabio M ^a   Kast, Juergen ^a   Capecchi, Mario R ^c   Underhill, T Michael ^a   Nielsen, Torsten O ^b  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b Genetic Pathology Evaluation Centre   (Canada)

^c UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 2; HISTONE DEACETYLASE INHIBITOR; PEPTIDES AND PROTEINS; PLASMID DNA; SMALL INTERFERING RNA; SS18 SSX FUSION ONCOPROTEIN; TRANSCRIPTION FACTOR; TRANSDUCIN LIKE ENHANCER OF SPLIT 1; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CANCER CELL; CANCER INHIBITION; CARCINOGENESIS; GENE EXPRESSION; GENE REPRESSION; GENE TARGETING; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN ANALYSIS; PROTEIN DNA BINDING; PROTEIN EXPRESSION; PROTEIN PURIFICATION; RNA INTERFERENCE; SYNOVIAL SARCOMA;

EID: 84863337645     PISSN: 15356108     EISSN: 18783686     Source Type: Journal    
DOI: 10.1016/j.ccr.2012.01.010     Document Type: Article

References (44)

1. Ali S.A., Zaidi S.K., Dobson J.R., Shakoori A.R., Lian J.B., Stein J.L., van Wijnen A.J., Stein G.S. Transcriptional corepressor TLE1 functions with Runx2 in epigenetic repression of ribosomal RNA genes. Proc. Natl. Acad. Sci. USA 2010, 107:4165-4169.
2. Baird K., Davis S., Antonescu C.R., Harper U.L., Walker R.L., Chen Y., Glatfelter A.A., Duray P.H., Meltzer P.S. Gene expression profiling of human sarcomas: insights into sarcoma biology. Cancer Res. 2005, 65:9226-9235.
3. Berger A.J., Kluger H.M., Li N., Kielhorn E., Halaban R., Ronai Z., Rimm D.L. Subcellular localization of activating transcription factor 2 in melanoma specimens predicts patient survival. Cancer Res. 2003, 63:8103-8107.
4. Bhoumik A., Fichtman B., Derossi C., Breitwieser W., Kluger H.M., Davis S., Subtil A., Meltzer P., Krajewski S., Jones N., Ronai Z. Suppressor role of activating transcription factor 2 (ATF2) in skin cancer. Proc. Natl. Acad. Sci. USA 2008, 105:1674-1679.
5. Boyle P., Le Su E., Rochon A., Shearer H.L., Murmu J., Chu J.Y., Fobert P.R., Després C. The BTB/POZ domain of the Arabidopsis disease resistance protein NPR1 interacts with the repression domain of TGA2 to negate its function. Plant Cell 2009, 21:3700-3713.
6. Cao R., Wang L., Wang H., Xia L., Erdjument-Bromage H., Tempst P., Jones R.S., Zhang Y. Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science 2002, 298:1039-1043.
7. Chen G., Fernandez J., Mische S., Courey A.J. A functional interaction between the histone deacetylase Rpd3 and the corepressor groucho in Drosophila development. Genes Dev. 1999, 13:2218-2230.
8. Dasen J.S., Barbera J.P., Herman T.S., Connell S.O., Olson L., Ju B., Tollkuhn J., Baek S.H., Rose D.W., Rosenfeld M.G. Temporal regulation of a paired-like homeodomain repressor/TLE corepressor complex and a related activator is required for pituitary organogenesis. Genes Dev. 2001, 15:3193-3207.
9. de Bruijn D.R., Allander S.V., van Dijk A.H., Willemse M.P., Thijssen J., van Groningen J.J., Meltzer P.S., van Kessel A.G. The synovial-sarcoma-associated SS18-SSX2 fusion protein induces epigenetic gene (de)regulation. Cancer Res. 2006, 66:9474-9482.
10. Faour W.H., Alaaeddine N., Mancini A., He Q.W., Jovanovic D., Di Battista J.A. Early growth response factor-1 mediates prostaglandin E2-dependent transcriptional suppression of cytokine-induced tumor necrosis factor-alpha gene expression in human macrophages and rheumatoid arthritis-affected synovial fibroblasts. J. Biol. Chem. 2005, 280:9536-9546.
11. Foo W.C., Cruise M.W., Wick M.R., Hornick J.L. Immunohistochemical staining for TLE1 distinguishes synovial sarcoma from histologic mimics. Am. J. Clin. Pathol. 2011, 135:839-844.
12. Garcia C.B., Shaffer C.M., Alfaro M.P., Smith A.L., Sun J., Zhao Z., Young P.P., Vansaun M.N., Eid J.E. Reprogramming of mesenchymal stem cells by the synovial sarcoma-associated oncogene SYT-SSX2. Oncogene 2011, in press. Published online September 26, 2011. 10.1038/onc.2011.418.
13. Haldar M., Hancock J.D., Coffin C.M., Lessnick S.L., Capecchi M.R. A conditional mouse model of synovial sarcoma: insights into a myogenic origin. Cancer Cell 2007, 11:375-388.
14. Haldar M., Randall R.L., Capecchi M.R. Synovial sarcoma: from genetics to genetic-based animal modeling. Clin. Orthop. Relat. Res. 2008, 466:2156-2167.
15. Hayakawa J., Mittal S., Wang Y., Korkmaz K.S., Adamson E., English C., Ohmichi M., McClelland M., Mercola D. Identification of promoters bound by c-Jun/ATF2 during rapid large-scale gene activation following genotoxic stress. Mol. Cell 2004, 16:521-535.
16. Higa L.A., Wu M., Ye T., Kobayashi R., Sun H., Zhang H. CUL4-DDB1 ubiquitin ligase interacts with multiple WD40-repeat proteins and regulates histone methylation. Nat. Cell Biol. 2006, 8:1277-1283.
17. Ishida M., Miyamoto M., Naitoh S., Tatsuda D., Hasegawa T., Nemoto T., Yokozeki H., Nishioka K., Matsukage A., Ohki M., Ohta T. The SYT-SSX fusion protein down-regulates the cell proliferation regulator COM1 in t(x;18) synovial sarcoma. Mol. Cell. Biol. 2007, 27:1348-1355.
18. Ito T., Ouchida M., Morimoto Y., Yoshida A., Jitsumori Y., Ozaki T., Sonobe H., Inoue H., Shimizu K. Significant growth suppression of synovial sarcomas by the histone deacetylase inhibitor FK228 in vitro and in vivo. Cancer Lett. 2005, 224:311-319.
19. Jagdis A., Rubin B.P., Tubbs R.R., Pacheco M., Nielsen T.O. Prospective evaluation of TLE1 as a diagnostic immunohistochemical marker in synovial sarcoma. Am. J. Surg. Pathol. 2009, 33:1743-1751.
20. Junttila M.R., Puustinen P., Niemelä M., Ahola R., Arnold H., Böttzauw T., Ala-aho R., Nielsen C., Ivaska J., Taya Y., et al. CIP2A inhibits PP2A in human malignancies. Cell 2007, 130:51-62.
21. Kawasaki H., Schiltz L., Chiu R., Itakura K., Taira K., Nakatani Y., Yokoyama K.K. ATF-2 has intrinsic histone acetyltransferase activity which is modulated by phosphorylation. Nature 2000, 405:195-200.
22. Kawase T., Ohki R., Shibata T., Tsutsumi S., Kamimura N., Inazawa J., Ohta T., Ichikawa H., Aburatani H., Tashiro F., Taya Y. PH domain-only protein PHLDA3 is a p53-regulated repressor of Akt. Cell 2009, 136:535-550.
23. Knösel T., Heretsch S., Altendorf-Hofmann A., Richter P., Katenkamp K., Katenkamp D., Berndt A., Petersen I. TLE1 is a robust diagnostic biomarker for synovial sarcomas and correlates with t(X;18): analysis of 319 cases. Eur. J. Cancer 2010, 46:1170-1176.
24. Kosemehmetoglu K., Vrana J.A., Folpe A.L. TLE1 expression is not specific for synovial sarcoma: a whole section study of 163 soft tissue and bone neoplasms. Mod. Pathol. 2009, 22:872-878.
25. Ladanyi M. Fusions of the SYT and SSX genes in synovial sarcoma. Oncogene 2001, 20:5755-5762.
26. Lim F.L., Soulez M., Koczan D., Thiesen H.J., Knight J.C. A KRAB-related domain and a novel transcription repression domain in proteins encoded by SSX genes that are disrupted in human sarcomas. Oncogene 1998, 17:2013-2018.
27. Liu H., Deng X., Shyu Y.J., Li J.J., Taparowsky E.J., Hu C.D. Mutual regulation of c-Jun and ATF2 by transcriptional activation and subcellular localization. EMBO J. 2006, 25:1058-1069.
28. Liu S., Cheng H., Kwan W., Lubieniecka J.M., Nielsen T.O. Histone deacetylase inhibitors induce growth arrest, apoptosis, and differentiation in clear cell sarcoma models. Mol. Cancer Ther. 2008, 7:1751-1761.
29. Lopez-Bergami P., Lau E., Ronai Z. Emerging roles of ATF2 and the dynamic AP1 network in cancer. Nat. Rev. Cancer 2010, 10:65-76.
30. Lubieniecka J.M., de Bruijn D.R., Su L., van Dijk A.H., Subramanian S., van de Rijn M., Poulin N., van Kessel A.G., Nielsen T.O. Histone deacetylase inhibitors reverse SS18-SSX-mediated polycomb silencing of the tumor suppressor early growth response 1 in synovial sarcoma. Cancer Res. 2008, 68:4303-4310.
31. Maekawa T., Shinagawa T., Sano Y., Sakuma T., Nomura S., Nagasaki K., Miki Y., Saito-Ohara F., Inazawa J., Kohno T., et al. Reduced levels of ATF-2 predispose mice to mammary tumors. Mol. Cell. Biol. 2007, 27:1730-1744.
32. Maekawa T., Sano Y., Shinagawa T., Rahman Z., Sakuma T., Nomura S., Licht J.D., Ishii S. ATF-2 controls transcription of Maspin and GADD45 alpha genes independently from p53 to suppress mammary tumors. Oncogene 2008, 27:1045-1054.
33. Müller J., Hart C.M., Francis N.J., Vargas M.L., Sengupta A., Wild B., Miller E.L., O'Connor M.B., Kingston R.E., Simon J.A. Histone methyltransferase activity of a Drosophila Polycomb group repressor complex. Cell 2002, 111:197-208.
34. Nagai M., Tanaka S., Tsuda M., Endo S., Kato H., Sonobe H., Minami A., Hiraga H., Nishihara H., Sawa H., Nagashima K. 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. USA 2001, 98:3843-3848.
35. Nakayama R., Mitani S., Nakagawa T., Hasegawa T., Kawai A., Morioka H., Yabe H., Toyama Y., Ogose A., Toguchida J., et al. Gene expression profiling of synovial sarcoma: distinct signature of poorly differentiated type. Am. J. Surg. Pathol. 2010, 34:1599-1607.
36. Nielsen T.O., West R.B., Linn S.C., Alter O., Knowling M.A., O'Connell J.X., Zhu S., Fero M., Sherlock G., Pollack J.R., et al. Molecular characterisation of soft tissue tumours: a gene expression study. Lancet 2002, 359:1301-1307.
37. Pacheco M., Horsman D.E., Hayes M.M., Clarkson P.W., Huwait H., Nielsen T.O. Small blue round cell tumor of the interosseous membrane bearing a t(2;22)(q34;q12)/EWS-CREB1 translocation: a case report. Mol. Cytogenet. 2010, 3:12.
38. Shevchenko A., Jensen O.N., Podtelejnikov A.V., Sagliocco F., Wilm M., Vorm O., Mortensen P., Shevchenko A., Boucherie H., Mann M. Linking genome and proteome by mass spectrometry: large-scale identification of yeast proteins from two dimensional gels. Proc. Natl. Acad. Sci. USA 1996, 93:14440-14445.
39. Soulez M., Saurin A.J., Freemont P.S., Knight J.C. SSX and the synovial-sarcoma-specific chimaeric protein SYT-SSX co-localize with the human Polycomb group complex. Oncogene 1999, 18:2739-2746.
40. Su L., Cheng H., Sampaio A.V., Nielsen T.O., Underhill T.M. EGR1 reactivation by histone deacetylase inhibitors promotes synovial sarcoma cell death through the PTEN tumor suppressor. Oncogene 2010, 29:4352-4361.
41. Terry J., Saito T., Subramanian S., Ruttan C., Antonescu C.R., Goldblum J.R., Downs-Kelly E., Corless C.L., Rubin B.P., van de Rijn M., et al. TLE1 as a diagnostic immunohistochemical marker for synovial sarcoma emerging from gene expression profiling studies. Am. J. Surg. Pathol. 2007, 31:240-246.
42. Thaete C., Brett D., Monaghan P., Whitehouse S., Rennie G., Rayner E., Cooper C.S., Goodwin G. 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. 1999, 8:585-591.
43. Wong J.P., Reboul E., Molday R.S., Kast J. A carboxy-terminal affinity tag for the purification and mass spectrometric characterization of integral membrane proteins. J. Proteome Res. 2009, 8:2388-2396.
44. Woo I.S., Kohno T., Inoue K., Ishii S., Yokota J. Infrequent mutations of the activating transcription factor-2 gene in human lung cancer, neuroblastoma and breast cancer. Int. J. Oncol. 2002, 20:527-531.