The Biology of Ewing sarcoma

Cancer Letters

Volumn 254, Issue 1, 2007, Pages 1-10

  Riggi, Nicolò ^a,b   Stamenkovic, Ivan ^a,b  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

^b SWISS INST FOR EXP CANCER RESEARCH   (Switzerland)

Author keywords

Ewing sarcoma; EWS FLI 1; Mesenchymal progenitor cells; Transformation

Indexed keywords

HYBRID PROTEIN; TRANSCRIPTION FACTOR FLI 1;

CANCER RESEARCH; CARCINOGENESIS; CHROMATIN IMMUNOPRECIPITATION; CHROMOSOME TRANSLOCATION; EWING SARCOMA; GENE; GENE EXPRESSION; GENE MUTATION; HISTOLOGY; HUMAN; IMMUNOHISTOCHEMISTRY; MOLECULAR GENETICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; RNA BINDING; SHORT SURVEY; STEM CELL;

EID: 34447324657     PISSN: 03043835     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.canlet.2006.12.009     Document Type: Review

References (74)

1. S. Ushigome, R. Machinami, P.H. Sorensen, Ewing sarcoma/primitive neuroectodermal tumor, in: C.D.M. Fletcher, K.K. Unni, F. Mertens, (Eds.), WHO Classification of Tumors, Pathology and Genetics, Tumors of Soft Tissue and Bone, 2003.
2. Dejana E. Endothelial cell-cell junctions: happy together. Nat. Rev. Mol. Cell. Biol. 5 (2004) 261-270
3. 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 359 (1992) 162-165
4. Helman L.J., and Meltzer P. Mechanisms of sarcoma development. Nat. Rev. Cancer 3 (2003) 685-694
5. Bertolotti A., Lutz Y., Heard D.J., Chambon P., and Tora L. hTAF(II)68, a novel RNA/ssDNA-binding protein with homology to the pro-oncoproteins TLS/FUS and EWS is associated with both TFIID and RNA polymerase II. EMBO J. 15 (1996) 5022-5031
6. Arvand A., and Denny C.T. Biology of EWS/ETS fusions in Ewing's family tumors. Oncogene 20 (2001) 5747-5754
7. Ohno T., Ouchida M., Lee L., Gatalica Z., Rao V.N., and Reddy E.S. The EWS gene, involved in Ewing family of tumors, malignant melanoma of soft parts and desmoplastic small round cell tumors, codes for an RNA binding protein with novel regulatory domains. Oncogene 9 (1994) 3087-3097
8. Bertolotti A., Melot T., Acker J., Vigneron M., Delattre O., and Tora L. EWS, but not EWS-FLI-1, is associated with both TFIID and RNA polymerase II: interactions between two members of the TET family, EWS and hTAFII68, and subunits of TFIID and RNA polymerase II complexes. Mol. Cell. Biol. 18 (1998) 1489-1497
9. Knoop L.L., and Baker S.J. EWS/FLI alters 5′-splice site selection. J. Biol. Chem. 276 (2001) 22317-22322
10. Yang L., Chansky H.A., and Hickstein D.D. EWS.Fli-1 fusion protein interacts with hyperphosphorylated RNA polymerase II and interferes with serine-arginine protein-mediated RNA splicing. J. Biol. Chem. 275 (2000) 37612-37618
11. Felsch J.S., Lane W.S., and Peralta E.G. Tyrosine kinase Pyk2 mediates G-protein-coupled receptor regulation of the Ewing sarcoma RNA-binding protein EWS. Curr. Biol. 9 (1999) 485-488
12. Perrotti D., Iervolino A., Cesi V., Cirinna M., Lombardini S., Grassilli E., Bonatti S., Claudio P.P., and Calabretta B. BCR-ABL prevents c-jun-mediated and proteasome-dependent FUS (TLS) proteolysis through a protein kinase CbetaII-dependent pathway. Mol. Cell. Biol. 20 (2000) 6159-6169
13. Hicks G.G., Singh N., Nashabi A., Mai S., Bozek G., Klewes L., Arapovic D., White E.K., Koury M.J., Oltz E.M., Van Kaer L., and Ruley H.E. Fus deficiency in mice results in defective B-lymphocyte development and activation, high levels of chromosomal instability and perinatal death. Nat. Genet. 24 (2000) 175-179
14. Kuroda M., Sok J., Webb L., Baechtold H., Urano F., Yin Y., Chung P., de Rooij D.G., Akhmedov A., Ashley T., and Ron D. Male sterility and enhanced radiation sensitivity in TLS(-/-) mice. EMBO J. 19 (2000) 453-462
15. Shimizu K., Ichikawa H., Tojo A., Kaneko Y., Maseki N., Hayashi Y., Ohira M., Asano S., and Ohki M. An ets-related gene, ERG, is rearranged in human myeloid leukemia with t(16;21) chromosomal translocation. Proc. Natl. Acad. Sci. USA 90 (1993) 10280-10284
16. Ben-David Y., Giddens E.B., Letwin K., and Bernstein A. Erythroleukemia induction by Friend murine leukemia virus: insertional activation of a new member of the ets gene family, Fli-1, closely linked to c-ets-1. Genes. Dev. 5 (1991) 908-918
17. Blair D.G., and Athanasiou M. Ets and retroviruses - transduction and activation of members of the Ets oncogene family in viral oncogenesis. Oncogene 19 (2000) 6472-6481
18. Rao V.N., Ohno T., Prasad D.D., Bhattacharya G., and Reddy E.S. Analysis of the DNA-binding and transcriptional activation functions of human Fli-1 protein. Oncogene 8 (1993) 2167-2173
19. Truong A.H., and Ben-David Y. The role of Fli-1 in normal cell function and malignant transformation. Oncogene 19 (2000) 6482-6489
20. Melet F., Motro B., Rossi D.J., Zhang L., and Bernstein A. Generation of a novel Fli-1 protein by gene targeting leads to a defect in thymus development and a delay in Friend virus-induced erythroleukemia. Mol. Cell. Biol. 16 (1996) 2708-2718
21. Brown L.A., Rodaway A.R., Schilling T.F., Jowett T., Ingham P.W., Patient R.K., and Sharrocks A.D. Insights into early vasculogenesis revealed by expression of the ETS-domain transcription factor Fli-1 in wild-type and mutant zebrafish embryos. Mech. Dev. 90 (2000) 237-252
22. Spyropoulos D.D., Pharr P.N., Lavenburg K.R., Jackers P., Papas T.S., Ogawa M., and Watson D.K. Hemorrhage, impaired hematopoiesis, and lethality in mouse embryos carrying a targeted disruption of the Fli1 transcription factor. Mol. Cell. Biol. 20 (2000) 5643-5652
23. Zhang L., Eddy A., Teng Y.T., Fritzler M., Kluppel M., Melet F., and Bernstein A. An immunological renal disease in transgenic mice that overexpress Fli-1, a member of the ets family of transcription factor genes. Mol. Cell. Biol. 15 (1995) 6961-6970
24. Deveaux S., Filipe A., Lemarchandel V., Ghysdael J., Romeo P.H., and Mignotte V. Analysis of the thrombopoietin receptor (MPL) promoter implicates GATA and Ets proteins in the coregulation of megakaryocyte-specific genes. Blood 87 (1996) 4678-4685
25. Bastian L.S., Kwiatkowski B.A., Breininger J., Danner S., and Roth G. Regulation of the megakaryocytic glycoprotein IX promoter by the oncogenic Ets transcription factor Fli-1. Blood 93 (1999) 2637-2644
26. Howard J.C., Yousefi S., Cheong G., Bernstein A., and Ben-David Y. Temporal order and functional analysis of mutations within the Fli-1 and p53 genes during the erythroleukemias induced by F-MuLV. Oncogene 8 (1993) 2721-2729
27. Pereira R., Quang C.T., Lesault I., Dolznig H., Beug H., and Ghysdael J. FLI-1 inhibits differentiation and induces proliferation of primary erythroblasts. Oncogene 18 (1999) 1597-1608
28. Tamir A., Howard J., Higgins R.R., Li Y.J., Berger L., Zacksenhaus E., Reis M., and Ben-David Y. Fli-1, an Ets-related transcription factor, regulates erythropoietin-induced erythroid proliferation and differentiation: evidence for direct transcriptional repression of the Rb gene during differentiation. Mol. Cell. Biol. 19 (1999) 4452-4464
29. Codrington R., Pannell R., Forster A., Drynan L.F., Daser A., Lobato N., Metzler M., and Rabbitts T.H. The Ews-ERG fusion protein can initiate neoplasia from lineage-committed haematopoietic cells. PLoS Biol. 3 (2005) e242
30. Forster A., Pannell R., Drynan L.F., Codrington R., Daser A., Metzler M., Lobato M.N., and Rabbitts T.H. The invertor knock-in conditional chromosomal translocation mimic. Nat. Methods 2 (2005) 27-30
31. Keller C., Arenkiel B.R., Coffin C.M., El-Bardeesy N., DePinho R.A., and Capecchi M.R. Alveolar rhabdomyosarcomas in conditional Pax3:Fkhr mice: cooperativity of Ink4a/ARF and Trp53 loss of function. Genes Dev. 18 (2004) 2614-2626
32. Perez-Losada J., Pintado B., Gutierrez-Adan A., Flores T., Banares-Gonzalez B., del Campo J.C., Martin-Martin J.F., Battaner E., and Sanchez-Garcia I. The chimeric FUS/TLS-CHOP fusion protein specifically induces liposarcomas in transgenic mice. Oncogene 19 (2000) 2413-2422
33. May W.A., Gishizky M.L., Lessnick S.L., Lunsford L.B., Lewis B.C., Delattre O., Zucman J., Thomas G., and Denny C.T. Ewing sarcoma 11;22 translocation produces a chimeric transcription factor that requires the DNA-binding domain encoded by FLI1 for transformation. Proc. Natl. Acad. Sci. USA 90 (1993) 5752-5756
34. Thompson A.D., Teitell M.A., Arvand A., and Denny C.T. Divergent Ewing's sarcoma EWS/ETS fusions confer a common tumorigenic phenotype on NIH3T3 cells. Oncogene 18 (1999) 5506-5513
35. Eliazer S., Spencer J., Ye D., Olson E., and Ilaria Jr. R.L. Alteration of mesodermal cell differentiation by EWS/FLI-1, the oncogene implicated in Ewing's sarcoma. Mol. Cell. Biol. 23 (2003) 482-492
36. Hu-Lieskovan S., Zhang J., Wu L., Shimada H., Schofield D.E., and Triche T.J. EWS-FLI1 fusion protein up-regulates critical genes in neural crest development and is responsible for the observed phenotype of Ewing's family of tumors. Cancer Res. 65 (2005) 4633-4644
37. Rorie C.J., Thomas V.D., Chen P., Pierce H.H., O'Bryan J.P., and Weissman B.E. The Ews/Fli-1 fusion gene switches the differentiation program of neuroblastomas to Ewing sarcoma/peripheral primitive neuroectodermal tumors. Cancer Res. 64 (2004) 1266-1277
38. Deneen B., and Denny C.T. Loss of p16 pathways stabilizes EWS/FLI1 expression and complements EWS/FLI1 mediated transformation. Oncogene 20 (2001) 6731-6741
39. Lessnick S.L., Dacwag C.S., and Golub T.R. The Ewing's sarcoma oncoprotein EWS/FLI induces a p53-dependent growth arrest in primary human fibroblasts. Cancer Cell 1 (2002) 393-401
40. Kovar H., Aryee D.N., Jug G., Henockl C., Schemper M., Delattre O., Thomas G., and Gadner H. EWS/FLI-1 antagonists induce growth inhibition of Ewing tumor cells in vitro. Cell Growth Differ. 7 (1996) 429-437
41. Tanaka K., Iwakuma T., Harimaya K., Sato H., and Iwamoto Y. EWS-Fli1 antisense oligodeoxynucleotide inhibits proliferation of human Ewing's sarcoma and primitive neuroectodermal tumor cells. J. Clin. Invest. 99 (1997) 239-247
42. Matsunobu T., Tanaka K., Nakamura T., Nakatani F., Sakimura R., Hanada M., Li X., Okada T., Oda Y., Tsuneyoshi M., and Iwamoto Y. The possible role of EWS-Fli1 in evasion of senescence in Ewing family tumors. Cancer Res. 66 (2006) 803-811
43. Kim S., Denny C.T., and Wisdom R. Cooperative DNA binding with AP-1 proteins is required for transformation by EWS-Ets fusion proteins. Mol. Cell. Biol. 26 (2006) 2467-2478
44. Toretsky J.A., Erkizan V., Levenson A., Abaan O.D., Parvin J.D., Cripe T.P., Rice A.M., Lee S.B., and Uren A. Oncoprotein EWS-FLI1 activity is enhanced by RNA helicase A. Cancer Res. 66 (2006) 5574-5581
45. Thompson A.D., Braun B.S., Arvand A., Stewart S.D., May W.A., Chen E., Korenberg J., and Denny C. EAT-2 is a novel SH2 domain containing protein that is up regulated by Ewing's sarcoma EWS/FLI1 fusion gene. Oncogene 13 (1996) 2649-2658
46. May W.A., Arvand A., Thompson A.D., Braun B.S., Wright M., and Denny C.T. EWS/FLI1-induced manic fringe renders NIH 3T3 cells tumorigenic. Nat. Genet. 17 (1997) 495-497
47. Arvand A., Bastians H., Welford S.M., Thompson A.D., Ruderman J.V., and Denny C.T. EWS/FLI1 up regulates mE2-C, a cyclin-selective ubiquitin conjugating enzyme involved in cyclin B destruction. Oncogene 17 (1998) 2039-2045
48. Bailly R.A., Bosselut R., Zucman J., Cormier F., Delattre O., Roussel M., Thomas G., and Ghysdael J. DNA-binding and transcriptional activation properties of the EWS-FLI-1 fusion protein resulting from the t(11;22) translocation in Ewing sarcoma. Mol. Cell. Biol. 14 (1994) 3230-3241
49. Fukuma M., Okita H., Hata J., and Umezawa A. Upregulation of Id2, an oncogenic helix-loop-helix protein, is mediated by the chimeric EWS/ets protein in Ewing sarcoma. Oncogene 22 (2003) 1-9
50. Nishimori H., Sasaki Y., Yoshida K., Irifune H., Zembutsu H., Tanaka T., Aoyama T., Hosaka T., Kawaguchi S., Wada T., Hata J., Toguchida J., Nakamura Y., and Tokino T. The Id2 gene is a novel target of transcriptional activation by EWS-ETS fusion proteins in Ewing family tumors. Oncogene 21 (2002) 8302-8309
51. Wai D.H., Schaefer K.L., Schramm A., Korsching E., Van Valen F., Ozaki T., Boecker W., Schweigerer L., Dockhorn-Dworniczak B., and Poremba C. Expression analysis of pediatric solid tumor cell lines using oligonucleotide microarrays. Int. J. Oncol. 20 (2002) 441-451
52. Zwerner J.P., and May W.A. PDGF-C is an EWS/FLI induced transforming growth factor in Ewing family tumors. Oncogene 20 (2001) 626-633
53. Nakatani F., Tanaka K., Sakimura R., Matsumoto Y., Matsunobu T., Li X., Hanada M., Okada T., and Iwamoto Y. Identification of p21WAF1/CIP1 as a direct target of EWS-Fli1 oncogenic fusion protein. J. Biol. Chem. 278 (2003) 15105-15115
54. Dauphinot L., De Oliveira C., Melot T., Sevenet N., Thomas V., Weissman B.E., and Delattre O. Analysis of the expression of cell cycle regulators in Ewing cell lines: EWS-FLI-1 modulates p57KIP2and c-Myc expression. Oncogene 20 (2001) 3258-3265
55. Hahm K.B. Repression of the gene encoding the TGF-beta type II receptor is a major target of the EWS-FLI1 oncoprotein. Nat. Genet. 23 (1999) 481
56. Im Y.H., Kim H.T., Lee C., Poulin D., Welford S., Sorensen P.H., Denny C.T., and Kim S.J. EWS-FLI1, EWS-ERG, and EWS-ETV1 oncoproteins of Ewing tumor family all suppress transcription of transforming growth factor beta type II receptor gene. Cancer Res. 60 (2000) 1536-1540
57. Prieur A., Tirode F., Cohen P., and Delattre O. EWS/FLI-1 silencing and gene profiling of Ewing cells reveal downstream oncogenic pathways and a crucial role for repression of insulin-like growth factor binding protein 3. Mol. Cell. Biol. 24 (2004) 7275-7283
58. Mendiola M., Carrillo J., Garcia E., Lalli E., Hernandez T., de Alava E., Tirode F., Delattre O., Garcia-Miguel P., Lopez-Barea F., Pestana A., and Alonso J. The orphan nuclear receptor DAX1 is up-regulated by the EWS/FLI1 oncoprotein and is highly expressed in Ewing tumors. Int. J. Cancer 118 (2006) 1381-1389
59. Kinsey M., Smith R., and Lessnick S.L. NR0B1 is required for the oncogenic phenotype mediated by EWS/FLI in Ewing's sarcoma. Mol. Cancer Res. 4 (2006) 851-859
60. Abaan O.D., Levenson A., Khan O., Furth P.A., Uren A., and Toretsky J.A. PTPL1 is a direct transcriptional target of EWS-FLI1 and modulates Ewing's Sarcoma tumorigenesis. Oncogene 24 (2005) 2715-2722
61. Nozawa S., Ohno T., Banno Y., Dohjima T., Wakahara K., Fan D.G., and Shimizu K. Inhibition of platelet-derived growth factor-induced cell growth signaling by a short interfering RNA for EWS-Fli1 via down-regulation of phospholipase D2 in Ewing sarcoma cells. J. Biol. Chem. 280 (2005) 27544-27551
62. Kikuchi R., Murakami M., Sobue S., Iwasaki T., Hagiwara K., Takagi A., Kojima T., Asano H., Suzuki M., Banno Y., Nozawa Y., and Murate T. Ewing's sarcoma fusion protein, EWS/Fli-1 and Fli-1 protein induce PLD2 but not PLD1 gene expression by binding to an ETS domain of 5' promoter. Oncogene (2006)
63. Smith R., Owen L.A., Trem D.J., Wong J.S., Whangbo J.S., Golub T.R., and Lessnick S.L. Expression profiling of EWS/FLI identifies NKX2.2 as a critical target gene in Ewing's sarcoma. Cancer Cell 9 (2006) 405-416
64. Owen L.A., and Lessnick S.L. Identification of target genes in their native cellular context: an analysis of EWS/FLI in Ewing's sarcoma. Cell Cycle 5 (2006) 2049-2053
65. Siligan C., Ban J., Bachmaier R., Spahn L., Kreppel M., Schaefer K.L., Poremba C., Aryee D.N., and Kovar H. EWS-FLI1 target genes recovered from Ewing's sarcoma chromatin. Oncogene 24 (2005) 2512-2524
66. Mackall C.L., Meltzer P.S., and Helman L.J. Focus on sarcomas. Cancer Cell 2 (2002) 175-178
67. Riggi N., Cironi L., Provero P., Suva M.L., Kaloulis K., Garcia-Echeverria C., Hoffmann F., Trumpp A., and Stamenkovic I. Development of Ewing's sarcoma from primary bone marrow-derived mesenchymal progenitor cells. Cancer Res. 65 (2005) 11459-11468
68. Castillero-Trejo Y., Eliazer S., Xiang L., Richardson J.A., and Ilaria Jr. R.L. Expression of the EWS/FLI-1 oncogene in murine primary bone-derived cells Results in EWS/FLI-1-dependent, ewing sarcoma-like tumors. Cancer Res. 65 (2005) 8698-8705
69. Torchia E.C., Jaishankar S., and Baker S.J. Ewing tumor fusion proteins block the differentiation of pluripotent marrow stromal cells. Cancer Res. 63 (2003) 3464-3468
70. Yee D., Favoni R.E., Lebovic G.S., Lombana F., Powell D.R., Reynolds C.P., and Rosen N. Insulin-like growth factor I expression by tumors of neuroectodermal origin with the t(11;22) chromosomal translocation. A potential autocrine growth factor. J. Clin. Invest. 86 (1990) 1806-1814
71. Mitsiades C.S., Mitsiades N.S., McMullan C.J., Poulaki V., Shringarpure R., Akiyama M., Hideshima T., Chauhan D., Joseph M., Libermann T.A., Garcia-Echeverria C., Pearson M.A., Hofmann F., Anderson K.C., and Kung A.L. Inhibition of the insulin-like growth factor receptor-1 tyrosine kinase activity as a therapeutic strategy for multiple myeloma, other hematologic malignancies, and solid tumors. Cancer Cell 5 (2004) 221-230
72. Scotlandi K., Manara M.C., Nicoletti G., Lollini P.L., Lukas S., Benini S., Croci S., Perdichizzi S., Zambelli D., Serra M., Garcia-Echeverria C., Hofmann F., and Picci P. Antitumor activity of the insulin-like growth factor-I receptor kinase inhibitor NVP-AEW541 in musculoskeletal tumors. Cancer Res. 65 (2005) 3868-3876
73. Toretsky J.A., Kalebic T., Blakesley V., LeRoith D., and Helman L.J. The insulin-like growth factor-I receptor is required for EWS/FLI-1 transformation of fibroblasts. J. Biol. Chem. 272 (1997) 30822-30827
74. Scotlandi K., Benini S., Nanni P., Lollini P.L., Nicoletti G., Landuzzi L., Serra M., Manara M.C., Picci P., and Baldini N. Blockage of insulin-like growth factor-I receptor inhibits the growth of Ewing's sarcoma in athymic mice. Cancer Res. 58 (1998) 4127-4131