The C terminus of the synovial sarcoma-associated SSX proteins interacts with the LIM homeobox protein LHX4

Oncogene

Volumn 27, Issue 5, 2008, Pages 653-662

  De Bruijn, D R H ^a   Van Dijk, A H A ^a   Willemse, M P ^a   Van Kessel, A Geurts ^a  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

LHX4; SS18SSX; SSX; Synovial sarcoma; Transcription regulation

Indexed keywords

GLYCOPROTEIN; HOMEODOMAIN PROTEIN; HYBRID PROTEIN; LIM HOMEOBOX PROTEIN LHX4; PROTEIN; PROTEIN SSX; SS18 SSX FUSION PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CARCINOGENESIS; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DNA BINDING MOTIF; FUNCTIONAL PROTEOMICS; HUMAN; HUMAN CELL; MOLECULAR CLONING; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN DOMAIN; PROTEIN ISOLATION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SYNOVIAL SARCOMA; TRANSCRIPTION REGULATION;

ANIMALS; CERCOPITHECUS AETHIOPS; COS CELLS; GENE EXPRESSION REGULATION; HAPLORHINI; HELA CELLS; HOMEODOMAIN PROTEINS; HUMANS; NEOPLASM PROTEINS; PROMOTER REGIONS (GENETICS); PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTO-ONCOGENE PROTEINS; REPRESSOR PROTEINS; SARCOMA, SYNOVIAL; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

MAMMALIA;

EID: 38549157970     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/sj.onc.1210688     Document Type: Article

References (56)

1. Boyd KE, Wells J, Gutman J, Bartley SM, Farnham PJ. (1998). c-Myc target gene specificity is determined by a post-DNA binding mechanism. Proc Natl Acad Sci USA 95: 13887-13892.
2. Brett D, Whitehouse S, Antonson P, Shipley J, Cooper C, Goodwin G. (1997). The SYT protein involved in the t(X;18) synovial sarcoma translocation is a transcriptional activator localised in nuclear bodies. Hum Mol Genet 6: 1559-1564.
3. Clark J, Rocques PJ, Crew AJ, Gill S, Shipley J, Chan AM 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.
4. Crew AJ, Clark J, Fisher C, Gill S, Grimer R, Chand A et al. (1995). Fusion of SYT to two genes, SSX1 and SSX2, encoding proteins with homology to the Kruppel-associated box in human synovial sarcoma. EMBO J 14: 2333-2340.
5. Cronwright G, Le Blanc K, Gotherstrom C, Darcy P, Ehnman M, Brodin B. (2005). Cancer/testis antigen expression in human mesenchymal stem cells: down-regulation of SSX impairs cell migration and matrix metalloproteinase 2 expression. Cancer Res 65: 2207-2215.
6. de Bruijn DR, Allander SV, van Dijk AH, Willemse MP, Thijssen J, van Groningen JJ et al. (2006). The synovial sarcoma-associated SS18-SSX2 fusion protein induces epigenetic gene (de)regulation. Cancer Res 66: 9474-9482.
7. de Bruijn DR, Baats E, Zechner U, de Leeuw B, Balemans M, Olde Weghuis D et al. (1996). Isolation and characterization of the mouse homolog of SYT, a gene implicated in the development of human synovial sarcomas. Oncogene 13: 643-648.
8. de Bruijn DR, dos Santos NR, Kater-Baats E, Thijssen J, van den Berk L, Stap J et al. (2002). The cancer-related protein SSX2 interacts with the human homologue of a Ras-like GTPase interactor, RAB3IP, and a novel nuclear protein, SSX2IP. Genes Chromosomes Cancer 34: 285-298.
9. de Bruijn DR, dos Santos NR, Thijssen J, Balemans M, Debernardi S, Linder B et al. (2001a). The synovial sarcoma associated protein SYT interacts with the acute leukemia associated protein AF10. Oncogene 20: 3281-3289.
10. de Bruijn DR, Kater-Baats E, Eleveld M, Merkx G, Geurts van Kessel A. (2001b). Mapping and characterization of the mouse and human SS18 genes, two human SS18-like genes and a mouse Ss18 pseudogene. Cytogenet Cell Genet 92: 310-319.
11. de Leeuw B, Balemans M, Geurts van Kessel A. (1996). A novel Kruppel-associated box containing the SSX gene (SSX3) on the human X chromosome is not implicated in t(X;18)-positive synovial sarcomas. Cytogenet Cell Genet 73: 179-183.
12. de Leeuw B, Balemans M, Olde Weghuis D, Geurts van Kessel A. (1995). Identification of two alternative fusion genes, SYT-SSX1 and SYT-SSX2, in t(X;18)(p11.2;q11.2)-positive synovial sarcomas. Hum Mol Genet 4: 1097-1099.
13. de Leeuw B, Suijkerbuijk RF, Olde Weghuis D, Meloni AM, Stenman G, Kindblom LG et al. (1994). Distinct Xp11.2 breakpoint regions in synovial sarcoma revealed by metaphase and interphase FISH: relationship to histologic subtypes. Cancer Genet Cytogenet 73: 89-94.
14. Debernardi S, Bassini A, Jones LK, Chaplin T, Linder B, de Bruijn DR et al. (2002). The MLL fusion partner AF10 binds GAS41, a protein that interacts with the human SWI/SNF complex. Blood 99: 275-281.
15. Dong WF, Heng HH, Lowsky R, Xu Y, DeCoteau JF, Shi XM et al. (1997). Cloning, expression, and chromosomal localization to 11p12-13 of a human LIM/HOMEOBOX gene, hLim-1. DNA Cell Biol 16: 671-678.
16. dos Santos NR, de Bruijn DR, Balemans M, Janssen B, Gartner F, Lopes JM et al. (1997). Nuclear localization of SYT, SSX and the synovial sarcoma-associated SYT-SSX fusion proteins. Hum Mol Genet 6: 1549-1558.
17. dos Santos NR, de Bruijn DR, Geurts van Kessel A. (2001). Molecular mechanisms underlying human synovial sarcoma development. Genes Chromosomes Cancer 30: 1-14.
18. dos Santos NR, de Bruijn DR, Kater-Baats E, Otte AP, Geurts van Kessel A. (2000a). Delineation of the protein domains responsible for SYT, SSX, and SYT-SSX nuclear localization. Exp Cell Res 256: 192-202.
19. dos Santos NR, Torensma R, de Vries TJ, Schreurs MW, de Bruijn DR, Kater-Baats E et al. (2000b). Heterogeneous expression of the SSX cancer/testis antigens in human melanoma lesions and cell lines. Cancer Res 60: 1654-1662.
20. 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.
21. Guillou L, Benhattar J, Bonichon F, Gallagher G, Terrier P, Stauffer E et al. (2004). Histologic grade, but not SYT-SSX fusion type, is an important prognostic factor in patients with synovial sarcoma: a multicenter, retrospective analysis. J Clin Oncol 22: 4040-4050.
22. Gure AO, Türeci O, Sahin U, Tsang S, Scanlan MJ, Jager E et al. (1997). SSX: a multigene family with several members transcribed in normal testis and human cancer. Int J Cancer 72: 965-971.
23. Gure AO, Wei IJ, Old LJ, Chen YT. (2002). The SSX gene family: characterization of 9 complete genes. Int J Cancer 101: 448-453.
24. Howard PW, Maurer RA. (2000). Identification of a conserved protein that interacts with specific LIM homeodomain transcription factors. J Biol Chem 275: 13336-13342.
25. Huntley S, Baggott DM, Hamilton AT, Tran-Gyamfi M, Yang S, Kim J et al. (2006). A comprehensive catalog of human KRAB-associated zinc finger genes: insights into the evolutionary history of a large family of transcriptional repressors. Genome Res 16: 669-677.
26. Ito T, Ouchida M, Ito S, Jitsumori Y, Morimoto Y, Ozaki T et al. (2004). SYT, a partner of SYT-SSX oncoprotein in synovial sarcomas, interacts with mSin3A, a component of histone deacetylase complex. Lab Invest 84: 1484-1490.
27. Kato H, Tjernberg A, Zhang W, Krutchinsky AN, An W, Takeuchi T 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. Kawai A, Naito N, Yoshida A, Morimoto Y, Ouchida M, Shimizu K et al. (2004). Establishment and characterization of a biphasic synovial sarcoma cell line, SYO-1. Cancer Lett 204: 105-113.
29. Kawai A, Woodruff J, Healey JH, Brennan MF, Antonescu CR, Ladanyi M. (1998). SYT-SSX gene fusion as a determinant of morphology and prognosis in synovial sarcoma. N Engl J Med 338: 153-160.
30. Kawamata N, Sakajiri S, Sugimoto KJ, Isobe Y, Kobayashi H, Oshimi K. (2002). A novel chromosomal translocation t(1;14)(q25;q32) in pre-B acute lymphoblastic leukemia involves the LIM homeodomain protein gene, Lhx4. Oncogene 21: 4983-4991.
31. Ladanyi M, Antonescu CR, Leung DH, Woodruff JM, Kawai A, Healey JH et al. (2002). Impact of SYT-SSX fusion type on the clinical behavior of synovial sarcoma: a multi-institutional retrospective study of 243 patients. Cancer Res 62: 135-140.
32. Lim FL, Soulez M, Koczan D, Thiesen HJ, Knight JC. (1998). A KRAB-related domain and a novel transcription repression domain in proteins encoded by SSX genes that are disrupted in human sarcomas. Oncogene 17: 2013-2018.
33. Liu Y, Fan M, Yu S, Zhou Y, Wang J, Yuan J et al. (2002). cDNA cloning, chromosomal localization and expression pattern analysis of human LIM-homeobox gene LHX4. Brain Res 928: 147-155.
34. Machinis K, Pantel J, Netchine I, Leger J, Camand OJ, Sobrier ML et al. (2001). Syndromic short stature in patients with a germline mutation in the LIM homeobox LHX4. Am J Hum Genet 69: 961-968.
35. Mischo A, Kubuschok B, Ertan K, Preuss KD, Romeike B, Regitz E et al. (2006). Prospective study on the expression of cancer testis genes and antibody responses in 100 consecutive patients with primary breast cancer. Int J Cancer 118: 696-703.
36. Nagai M, Tanaka S, Tsuda M, Endo S, Kato H, Sonobe 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 USA 98: 3843-3848.
37. Naka N, Araki N, Nakanishi H, Itoh K, Mano M, Ishiguro S et al. (2002). Expression of SSX genes in human osteosarcomas. Int J Cancer 98: 640-642.
38. 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.
39. Raetzman LT, Ward R, Camper SA. (2002). Lhx4 and Prop1 are required for cell survival and expansion of the pituitary primordia. Development 129: 4229-4239.
40. Richter K, Pinto do OP, Hagglund AC, Wahlin A, Carlsson L. (2003). Lhx2 expression in hematopoietic progenitor/stem cells in vivo causes a chronic myeloproliferative disorder and altered globin expression. Haematologica 88: 1336-1347.
41. Roberson MS, Schoderbek WE, Tremml G, Maurer RA. (1994). Activation of the glycoprotein hormone α-subunit promoter by a LIM-homeodomain transcription factor. Mol Cell Biol 14: 2985-2993.
42. Saito T, Nagai M, Ladanyi M. (2006). SYT-SSX1 and SYTSSX2 interfere with repression of E-cadherin by snail and slug: a potential mechanism for aberrant mesenchymal to epithelial transition in human synovial sarcoma. Cancer Res 66: 6919-6927.
43. Schuettengruber B, Chourrout D, Vervoort M, Leblanc B, Cavalli G. (2007). Genome regulation by polycomb and trithorax proteins. Cell 128: 735-745.
44. Schwartz YB, Pirrotta V. (2007). Polycomb silencing mechanisms and the management of genomic programmes. Nat Rev Genet 8: 9-22.
45. Sharma K, Sheng HZ, Lettieri K, Li H, Karavanov A, Potter S et al. (1998). LIM homeodomain factors Lhx3 and Lhx4 assign subtype identities for motor neurons. Cell 95: 817-828.
46. Sheng HZ, Moriyama K, Yamashita T, Li H, Potter SS, Mahon KA et al. (1997). Multistep control of pituitary organogenesis. Science 278: 1809-1812.
47. Skytting B, Nilsson G, Brodin B, Xie Y, Lundeberg J, Uhlen M et al. (1999). A novel fusion gene, SYT-SSX4, in synovial sarcoma. J Natl Cancer Inst 91: 974-975.
48. 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.
49. Taylor BJ, Reiman T, Pittman JA, Keats JJ, de Bruijn DR, Mant MJ et al. (2005). SSX cancer testis antigens are expressed in most multiple myeloma patients: co-expression of SSX1, 2, 4, and 5correlates with adverse prognosis and high frequencies of SSX-positive PCs. J Immunother 28: 564-575.
50. Thaete C, Brett D, Monaghan P, Whitehouse S, Rennie G, Rayner E 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.
51. Türeci O, Chen YT, Sahin U, Gure AO, Zwick C, Villena C et al. (1998). Expression of SSX genes in human tumors. Int J Cancer 77: 19-23.
52. Türeci O, Sahin U, Schobert I, Koslowski M, Scmitt H, Schild HJ et al. (1996). The SSX-2 gene, which is involved in the t(X;18) translocation of synovial sarcomas, codes for the human tumor antigen HOM-MEL-40. Cancer Res 56: 4766-4772.
53. Vogel MJ, Guelen L, de Wit E, Peric-Hupkes D, Loden M, Talhout W et al. (2006). Human heterochromatin proteins form large domains containing KRAB-ZNF genes. Genome Res 16: 1493-1504.
54. Wu HK, Heng HH, Siderovski DP, Dong WF, Okuno Y, Shi XM et al. (1996). Identification of a human LIM-Hox gene, hLH-2, aberrantly expressed in chronic myelogenous leukaemia and located on 9q33-34.1. Oncogene 12: 1205-1212.
55. Wu HK, Minden MD. (1997). Transcriptional activation of human LIM-HOX gene, hLH-2, in chronic myelogenous leukemia is due to a cis-acting effect of Bcr-Abl. Biochem Biophys Res Commun 233: 806-812.
56. Yamaguchi M, Yamamoto K, Miura O. (2003). Aberrant expression of the LHX4 LIM-homeobox gene caused by t(1;14)(q25;q32) in chronic myelogenous leukemia in biphenotypic blast crisis. Genes Chromosomes Cancer 38: 269-273.