Ewing sarcoma inhibition by disruption of EWSR1-FLI1 transcriptional activity and reactivation of p53

Journal of Pathology

Volumn 233, Issue 4, 2014, Pages 415-424

  Van Der Ent, Wietske ^a,b   Jochemsen, Aart G ^b   Teunisse, Amina F A S ^b   Krens, S F Gabriel ^a   Szuhai, Karoly ^b   Spaink, Herman P ^a   Hogendoorn, Pancras C W ^b   Snaar Jagalska, B Ewa ^a,c  

^a LEIDEN UNIVERSITY   (Netherlands)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^c Department of Molecular Cell Biology Leiden University Medical Center ^*  (Netherlands)

Author keywords

anti cancer drug screen; drug synergism; Ewing sarcoma; molecular targeted therapy; p53; tumour growth; zebrafish

Indexed keywords

HYBRID PROTEIN; NUTLIN 3; PROTEIN P53; TRANSCRIPTION FACTOR FLI 1; UNCLASSIFIED DRUG; YK 4 279;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CANCER GROWTH; CANCER INHIBITION; CELL PROLIFERATION; CONTROLLED STUDY; DRUG MECHANISM; DRUG POTENTIATION; EMBRYO; EWING SARCOMA; EWING SARCOMA CELL LINE; EWSR1 GENE; GENE; GENE DELETION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; MIGRATION INHIBITION; MITOSIS INHIBITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN STABILITY; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; TUMOR ENGRAFTMENT; TUMOR MODEL; TUMOR SUPPRESSOR GENE; TUMOR VOLUME; WILD TYPE; ZEBRA FISH;

ANTI-CANCER DRUG SCREEN; DRUG SYNERGISM; EWING SARCOMA; MOLECULAR TARGETED THERAPY; P53; TUMOUR GROWTH; ZEBRAFISH;

ANIMALS; ANTINEOPLASTIC AGENTS; BONE NEOPLASMS; CELL LINE, TUMOR; CELLS, CULTURED; DISEASE MODELS, ANIMAL; DRUG SYNERGISM; HETEROGRAFTS; HUMANS; IMIDAZOLES; INDOLES; PIPERAZINES; RNA-BINDING PROTEINS; SARCOMA, EWING; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC; TUMOR SUPPRESSOR PROTEIN P53; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84904248655     PISSN: 00223417     EISSN: 10969896     Source Type: Journal    
DOI: 10.1002/path.4378     Document Type: Article

References (48)

1. Fletcher CDM, Bridge JA, Hogendoorn PCW, et al., WHO Classification of Tumours of Soft Tissue and Bone, 4th edn. IARC: Lyon, 2013.
2. Burchill SA,. Molecular abnormalities in Ewing's sarcoma. Expert Rev Anticancer Ther 2008; 8: 1675-1687.
3. Delattre O, Zucman J, Plougastel B, et al., Gene fusion with an ETS DNA-binding domain caused by chromosome translocation in human tumours. Nature 1992; 359: 162-165.
4. Sorensen PH, Lessnick SL, Lopez-Terrada D, et al., A second Ewing's sarcoma translocation, t(21;22), fuses the EWS gene to another ETS-family transcription factor, ERG. Nat genet 1994; 6: 146-151.
5. Verhoeven DH, de Hooge AS, Mooiman EC, et al., NK cells recognize and lyse Ewing sarcoma cells through NKG2D and DNAM-1 receptor dependent pathways. Mol Immunol 2008; 45: 3917-3925.
6. Balamuth NJ, Womer RB,. Ewing's sarcoma. Lancet Oncol 2010; 11: 184-192.
7. Neilsen PM, Pishas KI, Callen DF, et al., Targeting the p53 pathway in Ewing sarcoma. Sarcoma 2011; 2011: 746939.
8. Vassilev LT, Vu BT, Graves B, et al., In vivo activation of the p53 pathway by small-molecule antagonists of MDM2. Science 2004; 303: 844-848.
9. Erkizan HV, Kong Y, Merchant M, et al., A small molecule blocking oncogenic protein EWS-FLI1 interaction with RNA helicase A inhibits growth of Ewing's sarcoma. Nat Med 2009; 15: 750-756.
10. Sonnemann J, Palani CD, Wittig S, et al., Anticancer effects of the p53 activator nutlin-3 in Ewing's sarcoma cells. Eur J Cancer 2011; 47: 1432-1441.
11. Liu S, Leach SD,. Zebrafish models for cancer. Annu Rev Pathol 2011; 6: 71-93.
12. Goessling W, North TE, Zon LI,. New waves of discovery: modeling cancer in zebrafish. J Clin Oncol 2007; 25: 2473-2479.
13. Ung CY, Lam SH, Gong Z,. Comparative transcriptome analyses revealed conserved biological and transcription factor target modules between the zebrafish and human tumors. Zebrafish 2009; 6: 425-431.
14. Feitsma H, Cuppen E,. Zebrafish as a cancer model. Mol Cancer Res 2008; 6: 685-694.
15. Amatruda JF, Shepard JL, Stern HM, et al., Zebrafish as a cancer model system. Cancer Cell 2002; 1: 229-231.
16. Lam SH, Chua HL, Gong Z, et al., Development and maturation of the immune system in zebrafish, Danio rerio: a gene expression profiling, in situ hybridization and immunological study. Dev Comp Immunol 2004; 28: 9-28.
17. Goessling W, North TE, Zon LI,. New waves of discovery: modeling cancer in zebrafish. J Clin Oncol 2007; 25: 2473-2479.
18. Kari G, Rodeck U, Dicker AP,. Zebrafish: an emerging model system for human disease and drug discovery. Clin Pharmacol Ther 2007; 82: 70-80.
19. den Hertog J., Chemical genetics: drug screens in zebrafish. Biosci Rep 2005; 25: 289-297.
20. Zon LI, Peterson RT,. In vivo drug discovery in the zebrafish. Nat Rev Drug Discov 2005; 4: 35-44.
21. Parng C, Seng WL, Semino C, et al., Zebrafish: a preclinical model for drug screening. Assay Drug Dev Technol 2002; 1: 41-48.
22. Lawson ND, Weinstein BM,. In vivo imaging of embryonic vascular development using transgenic zebrafish. Dev Biol 2002; 248: 307-318.
23. Renshaw SA, Loynes CA, Trushell DM, et al., A transgenic zebrafish model of neutrophilic inflammation. Blood 2006; 108: 3976-3978.
24. Langenau DM, Feng H, Berghmans S, et al., Cre/lox-regulated transgenic zebrafish model with conditional myc-induced T cell acute lymphoblastic leukemia. Proc Natl Acad Sci USA 2005; 102: 6068-6073.
25. Ghotra VP, He S, de Bont H, et al., Automated whole animal bio-imaging assay for human cancer dissemination. PloS One 2012; 7: e31281.
26. Chou TC,. Theoretical basis, experimental design, and computerized simulation of synergism and antagonism in drug combination studies. Pharmacol Rev 2006; 58: 621-681.
27. Lam S, Lodder K, Teunisse AF, et al., Role of Mdm4 in drug sensitivity of breast cancer cells. Oncogene 2010; 29: 2415-2426.
28. Krens SF, He S, Lamers GE, et al., Distinct functions for ERK1 and ERK2 in cell migration processes during zebrafish gastrulation. Dev Biol 2008; 319: 370-383.
29. Forbes SA, Tang G, Bindal N, et al., COSMIC (the Catalogue of Somatic Mutations in Cancer): a resource to investigate acquired mutations in human cancer. Nucleic Acids Res 2010; 38: D652-657.
30. Szuhai K, Ijszenga M, Tanke HJ, et al., Molecular cytogenetic characterization of four previously established and two newly established Ewing sarcoma cell lines. Cancer Genet Cytogenet 2006; 166: 173-179.
31. 1 checkpoint after DNA damage. Mol Cell Biol 1996; 16: 1126-1137.
32. Ottaviano L, Schaefer KL, Gajewski M, et al., Molecular characterization of commonly used cell lines for bone tumor research: a trans-European EuroBoNet effort. Genes Chromosomes Cancer 2010; 49: 40-51.
33. Whang-Peng J, Triche TJ, Knutsen T, et al., Cytogenetic characterization of selected small round cell tumors of childhood. Cancer Genet Cytogenet 1986; 21: 185-208.
34. Nicoli S, Presta M,. The zebrafish/tumor xenograft angiogenesis assay. Nat Protoc 2007; 2: 2918-2923.
35. Nicoli S, Ribatti D, Cotelli F, et al., Mammalian tumor xenografts induce neovascularization in zebrafish embryos. Cancer Res 2007; 67: 2927-2931.
36. White RM, Sessa A, Burke C, et al., Transparent adult zebrafish as a tool for in vivo transplantation analysis. Cell Stem Cell 2008; 2: 183-189.
37. Pishas KI, Al-Ejeh F, Zinonos I, et al., Nutlin-3a is a potential therapeutic for Ewing sarcoma. Clin Cancer Res 2011; 17: 494-504.
38. Stern HM, Zon LI,. Cancer genetics and drug discovery in the zebrafish. Nat Rev Cancer 2003; 3: 533-539.
39. Peirce SK, Findley HW,. The MDM2 antagonist nutlin-3 sensitizes p53-null neuroblastoma cells to doxorubicin via E2F1 and TAp73. Int J Oncol 2009; 34: 1395-1402.
40. Ray RM, Bhattacharya S, Johnson LR,. Mdm2 inhibition induces apoptosis in p53-deficient human colon cancer cells by activating p73- and E2F1-mediated expression of PUMA and Siva-1. Apoptosis 2011; 16: 35-44.
41. Rentzsch F, Kramer C, Hammerschmidt M,. Specific and conserved roles of TAp73 during zebrafish development. Gene 2003; 323: 19-30.
42. Kovar H, Pospisilova S, Jug G, et al., Response of Ewing tumor cells to forced and activated p53 expression. Oncogene 2003; 22: 3193-3204.
43. Wei G, Antonescu CR, de Alava E, et al., Prognostic impact of INK4A deletion in Ewing sarcoma. Cancer 2000; 89: 793-799.
44. Lopez-Guerrero JA, Pellin A, Noguera R, et al., Molecular analysis of the 9p21 locus and p53 genes in Ewing family tumors. Lab Invest 2001; 81: 803-814.
45. Huang HY, Illei PB, Zhao Z, et al., Ewing sarcomas with p53 mutation or p16/p14ARF homozygous deletion: a highly lethal subset associated with poor chemoresponse. J Clin Oncol 2005; 23: 548-558.
46. Berghmans S, Murphey RD, Wienholds E, et al., tp53 mutant zebrafish develop malignant peripheral nerve sheath tumors. Proc Natl Acad Sci USA 2005; 102: 407-412.
47. Ji Z, Kumar R, Taylor M, et al., Vemurafenib synergizes with nutlin-3 to deplete survivin and suppresses melanoma viability and tumor growth. Clin Cancer Res 2013; 19: 4383-4391.
48. Barber-Rotenberg JS, Selvanathan SP, Kong Y, et al., Single enantiomer of YK-4-279 demonstrates specificity in targeting the oncogene EWS-FLI1. Onctarget 2012; 3: 172-182.