Loss of Ewing sarcoma EWS allele promotes tumorigenesis by inducing chromosomal instability in zebrafish

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Park, Hyewon ^a   Galbraith, Richard ^b   Turner, Thaddeus ^b   Mehojah, Justin ^a   Azuma, Mizuki ^a  

^a UNIVERSITY OF KANSAS   (United States)

^b Lawrence Memorial Hospital   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN P53; RNA BINDING PROTEIN EWS; ZEBRAFISH PROTEIN;

ALLELE; ANIMAL; BONE TUMOR; CELL TRANSFORMATION; EWING SARCOMA; GENETICS; METABOLISM; PATHOLOGY; ZEBRA FISH;

ALLELES; ANIMALS; BONE NEOPLASMS; CELL TRANSFORMATION, NEOPLASTIC; RNA-BINDING PROTEIN EWS; SARCOMA, EWING; TUMOR SUPPRESSOR PROTEIN P53; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84983738815     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep32297     Document Type: Article

References (36)

1. Delattre, O. et al. Gene fusion with an ETS DNA-binding domain caused by chromosome translocation in human tumours. Nature 359, 162-165, doi: 10.1038/359162a0 (1992).
2. Sankar, S. & Lessnick, S. L. Promiscuous partnerships in Ewing's sarcoma. Cancer genetics 204, 351-365, doi: 10.1016/j. cancergen.2011.07.008 (2011).
3. Lawlor, E. R. & Sorensen, P. H. Twenty Years on: What Do We Really Know about Ewing Sarcoma and What Is the Path Forward? Critical reviews in oncogenesis 20, 155-171 (2015).
4. Romeo, S. & Dei Tos, A. P. Soft tissue tumors associated with EWSR1 translocation. Virchows Archiv: an international journal of pathology 456, 219-234, doi: 10.1007/s00428-009-0854-3 (2010).
5. Lessnick, S. L. & Ladanyi, M. Molecular pathogenesis of Ewing sarcoma: new therapeutic and transcriptional targets. Annual review of pathology 7, 145-159, doi: 10.1146/annurev-pathol-011110-130237 (2012).
6. Tomazou, E. M. et al. Epigenome mapping reveals distinct modes of gene regulation and widespread enhancer reprogramming by the oncogenic fusion protein EWS-FLI1. Cell reports 10, 1082-1095, doi: 10.1016/j.celrep.2015.01.042 (2015).
7. Svoboda, L. K. et al. Overexpression of HOX genes is prevalent in Ewing sarcoma and is associated with altered epigenetic regulation of developmental transcription programs. Epigenetics 9, 1613-1625, doi: 10.4161/15592294.2014.988048 (2014).
8. Dylla, L., Moore, C. & Jedlicka, P. MicroRNAs in Ewing Sarcoma. Frontiers in oncology 3, 65, doi: 10.3389/fonc.2013.00065 (2013).
9. Park, J. H. et al. A multifunctional protein, EWS, is essential for early brown fat lineage determination. Developmental cell 26, 393-404, doi: 10.1016/j.devcel.2013.07.002 (2013).
10. Li, H. et al. Ewing sarcoma gene EWS is essential for meiosis and B lymphocyte development. J Clin Invest 117, 1314-1323, doi: 10.1172/JCI31222 (2007).
11. Merkes, C. et al. Ewing sarcoma ewsa protein regulates chondrogenesis of Meckel's cartilage through modulation of Sox9 in zebrafish. PloS one 10, e0116627, doi: 10.1371/journal.pone.0116627 (2015).
12. Sanchez, G. et al. Alteration of cyclin D1 transcript elongation by a mutated transcription factor up-regulates the oncogenic D1b splice isoform in cancer. Proceedings of the National Academy of Sciences of the United States of America 105, 6004-6009, doi: 10.1073/pnas.0710748105 (2008).
13. Yang, L., Chansky, H. A. & 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, 37612-37618, doi: 10.1074/jbc.M005739200 (2000).
14. Azuma, M., Embree, L. J., Sabaawy, H. & Hickstein, D. D. Ewing sarcoma protein ewsr1 maintains mitotic integrity and proneural cell survival in the zebrafish embryo. PloS one 2, e979, doi: 10.1371/journal.pone.0000979 (2007).
15. Park, H. et al. Ewing sarcoma EWS protein regulates midzone formation by recruiting Aurora B kinase to the midzone. Cell cycle 13 (2014).
16. Hindriksen, S., Meppelink, A. & Lens, S. M. Functionality of the chromosomal passenger complex in cancer. Biochemical Society transactions 43, 23-32, doi: 10.1042/BST20140275 (2015).
17. White, R., Rose, K. & Zon, L. Zebrafish cancer: the state of the art and the path forward. Nature reviews. Cancer 13, 624-636, doi: 10.1038/nrc3589 (2013).
18. Huiting, L. N., Laroche, F. & Feng, H. The Zebrafish as a Tool to Cancer Drug Discovery. Austin journal of pharmacology and therapeutics 3, 1069 (2015).
19. Berghmans, S. et al. tp53 mutant zebrafish develop malignant peripheral nerve sheath tumors. Proceedings of the National Academy of Sciences of the United States of America 102, 407-412, doi: 10.1073/pnas.0406252102 (2005).
20. Leacock, S. W. et al. A zebrafish transgenic model of Ewing's sarcoma reveals conserved mediators of EWS-FLI1 tumorigenesis. Disease models & mechanisms 5, 95-106, doi: 10.1242/dmm.007401 (2012).
21. Carmena, M., Wheelock, M., Funabiki, H. & Earnshaw, W. C. The chromosomal passenger complex (CPC): from easy rider to the godfather of mitosis. Nature reviews. Molecular cell biology 13, 789-803, doi: 10.1038/nrm3474 (2012).
22. Douglas, M. E. & Mishima, M. Still entangled: assembly of the central spindle by multiple microtubule modulators. Seminars in cell & developmental biology 21, 899-908, doi: 10.1016/j.semcdb.2010.08.005 (2010).
23. Khmelinskii, A. & Schiebel, E. Assembling the spindle midzone in the right place at the right time. Cell cycle 7, 283-286 (2008).
24. Eckley, D. M., Ainsztein, A. M., Mackay, A. M., Goldberg, I. G. & Earnshaw, W. C. Chromosomal proteins and cytokinesis: patterns of cleavage furrow formation and inner centromere protein positioning in mitotic heterokaryons and mid-anaphase cells. The Journal of cell biology 136, 1169-1183 (1997).
25. Kovar, H. et al. The EWS protein is dispensable for Ewing tumor growth. Cancer research 61, 5992-5997 (2001).
26. Casper, A. M., Rosen, D. M. & Rajula, K. D. Sites of genetic instability in mitosis and cancer. Annals of the New York Academy of Sciences 1267, 24-30, doi: 10.1111/j.1749-6632.2012.06592.x (2012).
27. Sarni, D. & Kerem, B. The complex nature of fragile site plasticity and its importance in cancer. Current opinion in cell biology 40, 131-136, doi: 10.1016/j.ceb.2016.03.017 (2016).
28. Riggi, N., Suva, M. L. & Stamenkovic, I. The cancer stem cell paradigm in Ewing's sarcoma: what can we learn about these rare cells from a rare tumor? Expert review of anticancer therapy 11, 143-145, doi: 10.1586/era.10.235 (2011).
29. Tirode, F. et al. Mesenchymal stem cell features of Ewing tumors. Cancer cell 11, 421-429, doi: 10.1016/j.ccr.2007.02.027 (2007).
30. Lin, P. P. et al. EWS-FLI1 induces developmental abnormalities and accelerates sarcoma formation in a transgenic mouse model. Cancer research 68, 8968-8975, doi: 10.1158/0008-5472.CAN-08-0573 (2008).
31. Minas, T. Z. et al. Combined experience of six independent laboratories attempting to create an Ewing sarcoma mouse model. Oncotarget, doi: 10.18632/oncotarget.9388 (2016).
32. Embree, L. J., Azuma, M. & Hickstein, D. D. Ewing sarcoma fusion protein EWSR1/FLI1 interacts with EWSR1 leading to mitotic defects in zebrafish embryos and human cell lines. Cancer research 69, 4363-4371, doi: 10.1158/0008-5472.CAN-08-3229 (2009).
33. Spahn, L. et al. Homotypic and heterotypic interactions of EWS, FLI1 and their oncogenic fusion protein. Oncogene 22, 6819-6829, doi: 10.1038/sj.onc.1206810 (2003).
34. Selvanathan, S. P. et al. Oncogenic fusion protein EWS-FLI1 is a network hub that regulates alternative splicing. Proceedings of the National Academy of Sciences of the United States of America 112, E1307-1316, doi: 10.1073/pnas.1500536112 (2015).
35. Hornick, J. E., Karanjeet, K., Collins, E. S. & Hinchcliffe, E. H. Kinesins to the core: The role of microtubule-based motor proteins in building the mitotic spindle midzone. Seminars in cell & developmental biology 21, 290-299, doi: 10.1016/j.semcdb.2010.01.017 (2010).
36. Li, J. J. & Li, S. A. Mitotic kinases: the key to duplication, segregation, and cytokinesis errors, chromosomal instability, and oncogenesis. Pharmacology & therapeutics 111, 974-984, doi: 10.1016/j.pharmthera.2006.02.006 (2006).