Identification of target genes in their native cellular context: An analysis of EWS/FLI in Ewing's sarcoma

Cell Cycle

Volumn 5, Issue 18, 2006, Pages 2049-2053

  Owen, Leah A ^a   Lessnick, Stephen L ^a,b  

^a UNIVERSITY OF UTAH   (United States)

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

Author keywords

Ewing's sarcoma; EWS FLI; Microarray; NKX2.2; T(11; 22)(q24; q12); Translocation

Indexed keywords

HYBRID PROTEIN; ONCOPROTEIN; PROTEIN FLI; RNA BINDING PROTEIN EWS; UNCLASSIFIED DRUG;

BONE TUMOR; CHROMOSOME 11; CHROMOSOME 22; EWING SARCOMA; GENE IDENTIFICATION; GENE TARGETING; RNA INTERFERENCE; SHORT SURVEY;

EID: 33749661948     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.5.18.3213     Document Type: Short Survey

References (47)

1. Ewing J. Diffuse endothelioma of bone. Proceedings of the New York Pathological Society 1921; 21:17-24.
2. Arndt CA, Crist WM. Common musculoskeletal tumors of childhood and adolescence. N Engl J Med 1999; 341:342-52.
3. Grier HE. The Ewing family of tumors. Ewing's sarcoma and primitive neuroectodermal tumors. Pediatr Clin North Am 1997; 44:991-1004.
4. Gurney JG, Swensen AR, Bulterys M. Malignant bone tumors. In: Ries LAG, Smith MA, Gurney JG, Linet M, Tamra T, Young JL, Bunin GR, eds. Cancer incidence and survival among children and adolescents: United States SEER Program 1975-1995. Bethesda, MD: National Cancer Institute, SEER Program, NIH Pub. No. 99-4649, 1999:99-110.
5. Horowitz ME, Malawer MM, Woo SY, Hicks MJ. Ewing's sarcoma family of tumors: Ewing's sarcoma of bone and soft tissue and the peripheral primitive neuroectodermal tumors. In: Pizzo PA, Poplack DG, eds. Principles and Practice of Pediatric Oncology. 3rd ed. Philadelphia: Lippincott-Raven Publishers, 1997:831-63.
6. Turc-Carel C, Aurias A, Mugneret F, Lizard S, Sidaner I, Volk C, Thiery JP, Olschwang S, Philip I, Berger MP, et al. Chromosomes in Ewing's sarcoma. I. An evaluation of 85 cases of remarkable consistency of t(11;22)(q24;q12). Cancer Genet Cytogenet 1988; 32:229-38.
7. Kovar H. Ewing's sarcoma and peripheral primitive neuroectodermal tumors after their genetic union. Current Opinion in Oncology 1998; 10:334-42.
8. Kadin ME, Bensch KG. On the origin of Ewing's tumor. Cancer 1971; 27:257-73.
9. Dickman PS, Liotta LA, Triche TJ. Ewing's sarcoma: Characterization in established cultures and evidence of its histogenesis. Laboratory Investigation 1982; 47:375-82.
10. Cavenzzana AO, Miser JS, Jefferson J, Triche TJ. Experimental evidence for a neural origin of Ewing's sarcoma of bone. Am J Pathol 1987; 127:507-18.
11. Navas-Palacios JJ, Aparicio-Duque R, Valdes MD. On the histogenesis of Ewing's sarcoma. An ultrastructural, immunohistochemical, and cytochemical study. Cancer 1984; 53:1882-901.
12. Torchia EC, Jaishankar S, Baker SJ. Ewing tumor fusion proteins block the differentiation of pluripotent marrow stromal cells. Cancer Res 2003; 63:3464-8.
13. Riggi N, Cironi L, Provero P, Suva ML, 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; 65:11459-68.
14. Staege MS, Hutter C, Neumann I, Foja S, Hattenhorst UE, Hansen G, Afar D, Burdach SE. DNA microarrays reveal relationship of Ewing family tumors to both endothelial and fetal neural crest-derived cells and define novel targets. Cancer Res 2004; 64:8213-21.
15. Rorie CJ, Thomas VD, Chen P, Pierce HH, O'Bryan JP, Weissman BE. The Ews/Fli-1 fusion gene switches the differentiation program of neuroblastomas to Ewing sarcoma/peripheral primitive neuroectodermal tumors. Cancer Res 2004; 64:1266-77.
16. Teitell MA, Thompson AD, Sorensen PH, Shimada H, Triche TJ, Denny CT. EWS/ETS fusion genes induce epithelial and neuroectodermal differentiation in NIH 3T3 fibroblasts. Lab Invest 1999; 79:1535-43.
17. Hu-Lieskovan S, Zhang J, Wu L, Shimada H, Schofield DE, Triche TJ. 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 2005; 65:4633-44.
18. Lessnick SL, Dacwag CS, Golub TR. The Ewing's sarcoma oncoprotein EWS/FLI induces a p53-dependent growth arrest in primary human fibroblasts. Cancer Cell 2002; 1:393-401.
19. Sorensen PH, Shimada H, Liu XF, Lim JF, Thomas G, Triche TJ. Biphenotypic sarcomas with myogenic and neural differentiation express the Ewing's sarcoma EWS/FLI1 fusion gene. Cancer Res 1995; 55:1385-92.
20. Delattre O, Zucman J, Plougastel B, Desmaze C, Melot T, Peter M, Heinrich K, Houbert I, de Jong P, Rouleau G, Aurias A, Thomas G. Gene fusion with an ETS DNA-binding domain caused by chromosome translocation in human tumours. Nature 1992; 359:162-5.
21. May WA, Gishizky ML, Lessnick SL, Lunsford LB, Lewis BC, Delattre O, Zucman J, Thomas G, Denny CT. 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 1993; 90:5752-6.
22. May WA, Lessnick SL, Braun BS, Klemsz M, Lewis BC, Lunsford LB, Hromas R, Denny CT. The Ewing's sarcoma EWS/FLI-1 fusion gene encodes a more potent transcriptional activator and is a more powerful transforming gene than FLI-1. Mol Cell Biol 1993; 13:7393-8.
23. Lessnick SL, Braun BS, Denny CT, May WA. Multiple domains mediate transformation by the Ewing's sarcoma EWS/FLI- 1 fusion gene. Oncogene 1995; 10:423-31.
24. Van Rompaey L, Holland E, Grosveld G. TEL induces aggregation in transformed cells and induces tube formation in NIH3T3-UCLA cells. Biochem Biophys Res Commun 2002; 291:820-8.
25. Arvand A, Bastians H, Welford SM, Thompson AD, Ruderman JV, Denny CT. EWS/FLI1 up regulates mE2-C, a cyclin-selective ubiquitin conjugating enzyme involved in cyclin B destruction. Oncogene 1998; 17:2039-45.
26. Lessnick SL. Structural and functional requirements for transformation mediated by the Ewing's sarcoma EWS/FLI-1 fusion protein. Ph.D. Thesis. Los Angeles: Molecular Biology, University of California, 1994.
27. Braun BS. The Transcriptional response to the Ewing's sarcoma fusion oncogene EWS/FLI. Ph.D. Thesis, Molecular Biology, University of California, Los Angeles. 1997.
28. Deneen B, Denny CT. Loss of p16 pathways stabilizes EWS/FLI1 expression and complements EWS/FLI1 mediated transformation. Oncogene 2001; 20:6731-41.
29. Kovar H. Context matters: The hen or egg problem in Ewing's sarcoma. Semin Cancer Biol 2005; 15:189-96.
30. Ouchida M, Ohno T, Fujimura Y, Rao VN, Reddy ES. Loss of tumorigenicity of Ewing's sarcoma cells expressing antisense RNA to EWS-fusion transcripts. Oncogene 1995; 11:1049-54.
31. Kovar H, Aryee DN, Jug G, Henockl C, Schemper M, Delattre O, Thomas G, Gadner H. EWS/FLI-1 antagonists induce growth inhibition of Ewing tumor cells in vitro. Cell Growth Differ 1996; 7:429-37.
32. Tanaka K, Iwakuma T, Harimaya K, Sato H, Iwamoto Y. EWS-Fli1 antisense oligodeoxynucleotide inhibits proliferation of human Ewing's sarcoma and primitive neuroectodermal tumor cells. J Clin Invest 1997; 99:239-47.
33. Toretsky JA, Connell Y, Neckers L, Bhat NK. Inhibition of EWS-FLI-1 fusion protein with antisense oligodeoxynucleotides. J Neurooncol 1997; 31:9-16.
34. Chan D, Wilson TJ, Xu D, Cowdery HE, Sanij E, Hertzog PJ, Kola I. Transformation induced by Ewing's sarcoma associated EWS/FLI-1 is suppressed by KRAB/FLI-1. Br J Cancer 2003; 88:137-45.
35. Dohjima T, Lee NS, Li H, Ohno T, Rossi JJ. Small interfering RNAs expressed from a Pol III promoter suppress the EWS/Fli-1 transcript in an Ewing sarcoma cell line. Mol Ther 2003; 7:811-6.
36. Prieur A, Tirode F, Cohen P, 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 2004; 24:7275-83.
37. Bennett MR, Schwartz SM. Antisense therapy for angioplasty restenosis. Some critical considerations. Circulation 1995; 92:1981-93.
38. Laudet V, Hanni C, Stehelin D, Duterque-Coquillaud M. Molecular phylogeny of the ETS gene family. Oncogene 1999; 18:1351-9.
39. Smith R, Owen LA, Trem DJ, Wong JS, Whangbo JS, Golub TR, Lessnick SL. Expression profiling of EWS/FLI identifies NKX2.2 as a critical target gene in Ewing's sarcoma. Cancer Cell 2006; 9:405-16.
40. Jackson AL, Bartz SR, Schelter J, Kobayashi SV, Burchard J, Mao M, Li B, Cavet G, Linsley PS. Expression profiling reveals off-target gene regulation by RNAi. Nat Biotechnol 2003; 21:635-7.
41. Briscoe J, Sussel L, Serup P, Hartigan-O'Connor D, Jessell TM, Rubenstein JL, Ericson J. Homeobox gene Nkx2.2 and specification of neuronal identity by graded Sonic hedgehog signaling. Nature 1999; 398:622-7.
42. McMahon AP. Neural patterning: The role of Nkx genes in the ventral spinal cord. Genes Dev 2000; 14:2261-4.
43. Qi Y, Cai J, Wu Y, Wu R, Lee J, Fu H, Rao M, Sussel L, Rubenstein J, Qiu M. Control of oligodendrocyte differentiation by the Nkx2.2 homeodomain transcription factor. Development 2001; 128:2723-33.
44. Sussel L, Kalamaras J, Hartigan-O'Connor DJ, Meneses JJ, Pedersen RA, Rubenstein JL, German MS. Mice lacking the homeodomain transcription factor Nkx2.2 have diabetes due to arrested differentiation of pancreatic beta cells. Development 1998; 125:2213-21.
45. Price M, Lazzaro D, Pohl T, Mattei MG, Ruther U, Olivo JC, Duboule D, Di Lauro R. Regional expression of the homeobox gene Nkx-2.2 in the developing mammalian forebrain. Neuron 1992; 8:241-55.
46. Fellinger EJ, Garin-Chesa P, Triche TJ, Huvos AG, Rettig WJ. Immunohistochemical analysis of Ewing's sarcoma cell surface antigen p30/32MIC2. Am J Pathol 1991; 139:317-25.
47. Baird K, Davis S, Antonescu CR, Harper UL, Walker RL, Chen Y, Glatfelter AA, Duray PH, Meltzer PS. Gene expression profiling of human sarcomas: Insights into sarcoma biology. Cancer Res 2005; 65:9226-35.