Ewing sarcoma ewsa protein regulates chondrogenesis of meckel's cartilage through modulation of Sox9 in zebrafish

PLoS ONE

Volumn 10, Issue 1, 2015, Pages

  Merkes, Chris ^a   Turkalo, Timothy K ^a   Wilder, Nicole ^a   Park, Hyewon ^a   Wenger, Luke W ^a   Lewin, Seth J ^a   Azuma, Mizuki ^a  

^a UNIVERSITY OF KANSAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN 4; CONNECTIVE TISSUE GROWTH FACTOR; EWSA PROTEIN; RNA BINDING PROTEIN EWS; TRANSCRIPTION FACTOR SOX9; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; BINDING SITE; BMP4 GENE; CARTILAGE; CARTILAGE CELL; CELL DIFFERENTIATION; CHONDROGENESIS; COL2A1A GENE; COL2A1B GENE; CONTROLLED STUDY; CTGFA GENE; CTGFB GENE; DOWN REGULATION; EMBRYO; GENE; MECKEL CARTILAGE; NOG1 GENE; NOG2 GENE; NONHUMAN; PROMOTER REGION; PROTEIN PROTEIN INTERACTION; SOX5 GENE; TRANSCRIPTION REGULATION; UPREGULATION; ZEBRA FISH; ANIMAL; CHONDROCYTE; CHROMATIN IMMUNOPRECIPITATION; CYTOLOGY; EMBRYOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY;

DANIO RERIO;

ANIMALS; CARTILAGE; CELL DIFFERENTIATION; CHONDROCYTES; CHONDROGENESIS; CHROMATIN IMMUNOPRECIPITATION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; RNA-BINDING PROTEIN EWS; SOX9 TRANSCRIPTION FACTOR; ZEBRAFISH;

EID: 84922041664     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0116627     Document Type: Article

References (55)

1. Delattre O, Zucman J, Plougastel B, Desmaze C, Melot T, et al. (1992) Gene fusion with an ETS DNAbinding domain caused by chromosome translocation in human tumours. Nature 359: 162-165. PMID: 1522903
2. Abaan OD, Levenson A, Khan O, Furth PA, Uren A, et al. (2005) PTPL1 is a direct transcriptional target of EWS-FLI1 and modulates Ewing's Sarcoma tumorigenesis. Oncogene 24: 2715-2722. PMID: 15782144
3. Smith R, Owen LA, Trem DJ, Wong JS, Whangbo JS, et al. (2006) Expression profiling of EWS/FLI identifies NKX2.2 as a critical target gene in Ewing's sarcoma. Cancer Cell 9: 405-416. PMID: 16697960
4. Zwerner JP, Joo J, Warner KL, Christensen L, Hu-Lieskovan S, et al. (2008) The EWS/FLI1 oncogenic transcription factor deregulates GLI1. Oncogene 27: 3282-3291. PMID: 18084326
5. Beauchamp E, Bulut G, Abaan O, Chen K, Merchant A, et al. (2009) GLI1 is a direct transcriptional target of EWS-FLI1 oncoprotein. J Biol Chem 284: 9074-9082. doi: 10.1074/jbc.M806233200 PMID: 19189974
6. Kinsey M, Smith R, Iyer AK, McCabe ER, Lessnick SL (2009) EWS/FLI and its downstream target NR0B1 interact directly to modulate transcription and oncogenesis in Ewing's sarcoma. Cancer Res 69: 9047-9055. doi: 10.1158/0008-5472.CAN-09-1540 PMID: 19920188
7. Sohn EJ, Li H, Reidy K, Beers LF, Christensen BL, et al. (2010) EWS/FLI1 oncogene activates caspase 3 transcription and triggers apoptosis in vivo. Cancer Res 70: 1154-1163. doi: 10.1158/0008-5472. CAN-09-1993 PMID: 20103643
8. Toomey EC, Schiffman JD, Lessnick SL (2010) Recent advances in the molecular pathogenesis of Ewing's sarcoma. Oncogene 29: 4504-4516. doi: 10.1038/onc.2010.205 PMID: 20543858
9. Toretsky JA, Erkizan V, Levenson A, Abaan OD, Parvin JD, et al. (2006) Oncoprotein EWS-FLI1 activity is enhanced by RNA helicase A. Cancer Res 66: 5574-5581. PMID: 16740692
10. Erkizan HV, Kong Y, Merchant M, Schlottmann S, Barber-Rotenberg JS, et al. (2009) A small molecule blocking oncogenic protein EWS-FLI1 interaction with RNA helicase A inhibits growth of Ewing's sarcoma. Nat Med 15: 750-756. doi: 10.1038/nm.1983 PMID: 19584866
11. McKinsey EL, Parrish JK, Irwin AE, Niemeyer BF, Kern HB, et al. (2011) A novel oncogenic mechanism in Ewing sarcoma involving IGF pathway targeting by EWS/Fli1-regulated microRNAs. Oncogene 30: 4910-4920. doi: 10.1038/onc.2011.197 PMID: 21643012
12. Liu F, Walmsley M, Rodaway A, Patient R (2008) Fli1 acts at the top of the transcriptional network driving blood and endothelial development. Curr Biol 18: 1234-1240. doi: 10.1016/j.cub.2008.07.048 PMID: 18718762
13. Yang L, Chansky HA, Hickstein DD (2000) 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. PMID: 10982800
14. Rossow KL, Janknecht R (2001) The Ewing's sarcoma gene product functions as a transcriptional activator. Cancer Res 61: 2690-2695. PMID: 11289149
15. Araya N, Hirota K, Shimamoto Y, Miyagishi M, Yoshida E, et al. (2003) Cooperative interaction of EWS with CREB-binding protein selectively activates hepatocyte nuclear factor 4-mediated transcription. J Biol Chem 278: 5427-5432. PMID: 12459554
16. Azuma M, Embree LJ, Sabaawy H, Hickstein DD (2007) Ewing sarcoma protein ewsr1 maintains mitotic integrity and proneural cell survival in the zebrafish embryo. PLoS One 2: e979. PMID: 17912356
17. Park H, Turkalo TK, Nelson K, Folmsbee SS, Robb C, et al. (2014) Ewing sarcoma EWS protein regulates midzone formation by recruiting Aurora B kinase to the midzone. Cell Cycle 13. doi: 10.4161/ 15384101.2014.949550 PMID: 25530323
18. Spahn L, Siligan C, Bachmaier R, Schmid JA, Aryee DN, et al. (2003) Homotypic and heterotypic interactions of EWS, FLI1 and their oncogenic fusion protein. Oncogene 22: 6819-6829. PMID: 14534527
19. Embree LJ, Azuma M, Hickstein DD (2009) Ewing sarcoma fusion protein EWSR1/FLI1 interacts with EWSR1 leading to mitotic defects in zebrafish embryos and human cell lines. Cancer Res 69: 4363-4371. doi: 10.1158/0008-5472.CAN-08-3229 PMID: 19417137
20. Li H, Watford W, Li C, Parmelee A, Bryant MA, et al. (2007) Ewing sarcoma gene EWS is essential for meiosis and B lymphocyte development. J Clin Invest 117: 1314-1323. PMID: 17415412
21. Noden DM (1983) The role of the neural crest in patterning of avian cranial skeletal, connective, and muscle tissues. Dev Biol 96: 144-165. PMID: 6825950
22. Kague E, Gallagher M, Burke S, Parsons M, Franz-Odendaal T, et al. (2012) Skeletogenic fate of zebrafish cranial and trunk neural crest. PLoS One 7: e47394. doi: 10.1371/journal.pone.0047394 PMID: 23155370
23. Bhatt S, Diaz R, Trainor PA (2013) Signals and switches in Mammalian neural crest cell differentiation. Cold Spring Harb Perspect Biol 5. doi: 10.1101/cshperspect.a019836 PMID: 24296172
24. Talbot JC, Johnson SL, Kimmel CB (2010) hand2 and Dlx genes specify dorsal, intermediate and ventral domains within zebrafish pharyngeal arches. Development 137: 2507-2517. doi: 10.1242/dev. 049700 PMID: 20573696
25. Karsenty G, Wagner EF (2002) Reaching a genetic and molecular understanding of skeletal development. Dev Cell 2: 389-406. PMID: 11970890
26. Akiyama H, Chaboissier MC, Martin JF, Schedl A, de Crombrugghe B (2002) The transcription factor Sox9 has essential roles in successive steps of the chondrocyte differentiation pathway and is required for expression of Sox5 and Sox6. Genes Dev 16: 2813-2828. PMID: 12414734
27. Cheung M, Briscoe J (2003) Neural crest development is regulated by the transcription factor Sox9. Development 130: 5681-5693. PMID: 14522876
28. Bi W, Deng JM, Zhang Z, Behringer RR, de Crombrugghe B (1999) Sox9 is required for cartilage formation. Nat Genet 22: 85-89. PMID: 10319868
29. Bi W, Huang W, Whitworth DJ, Deng JM, Zhang Z, et al. (2001) Haploinsufficiency of Sox9 results in defective cartilage primordia and premature skeletal mineralization. Proc Natl Acad Sci U S A 98: 6698-6703. PMID: 11371614
30. Henry SP, Liang S, Akdemir KC, de Crombrugghe B (2012) The postnatal role of Sox9 in cartilage. J Bone Miner Res 27: 2511-2525. doi: 10.1002/jbmr.1696 PMID: 22777888
31. Lefebvre V, Huang W, Harley VR, Goodfellow PN, de Crombrugghe B (1997) SOX9 is a potent activator of the chondrocyte-specific enhancer of the pro alpha1(II) collagen gene. Mol Cell Biol 17: 2336-2346. PMID: 9121483
32. Zhao Q, Eberspaecher H, Lefebvre V, De Crombrugghe B (1997) Parallel expression of Sox9 and Col2a1 in cells undergoing chondrogenesis. Dev Dyn 209: 377-386. PMID: 9264261
33. Hattori T, Kishino T, Stephen S, Eberspaecher H, Maki S, et al. (2013) E6-AP/UBE3A protein acts as a ubiquitin ligase toward SOX9 protein. J Biol Chem 288: 35138-35148. doi: 10.1074/jbc.M113.486795 PMID: 24155239
34. Akiyama H, Lyons JP, Mori-Akiyama Y, Yang X, Zhang R, et al. (2004) Interactions between Sox9 and beta-catenin control chondrocyte differentiation. Genes Dev 18: 1072-1087. PMID: 15132997
35. Tomita N, Hattori T, Itoh S, Aoyama E, Yao M, et al. (2013) Cartilage-specific over-expression of CCN family member 2/connective tissue growth factor (CCN2/CTGF) stimulates insulin-like growth factor expression and bone growth. PLoS One 8: e59226. doi: 10.1371/journal.pone.0059226 PMID: 23555635
36. Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF (1995) Stages of embryonic development of the zebrafish. Dev Dyn 203: 253-310. PMID: 8589427
37. Javidan Y, Schilling TF (2004) Development of cartilage and bone. Methods Cell Biol 76: 415-436. PMID: 15602885
38. Neuhauss SC, Solnica-Krezel L, Schier AF, Zwartkruis F, Stemple DL, et al. (1996) Mutations affecting craniofacial development in zebrafish. Development 123: 357-367. PMID: 9007255
39. Strahle U, Blader P, Ingham PW (1996) Expression of axial and sonic hedgehog in wildtype and midline defective zebrafish embryos. Int J Dev Biol 40: 929-940. PMID: 8946241
40. Azuma M, Toyama R, Laver E, Dawid IB (2006) Perturbation of rRNA synthesis in the bap28 mutation leads to apoptosis mediated by p53 in the zebrafish central nervous system. J Biol Chem 281: 13309-13316. PMID: 16531401
41. Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3: 1101-1108. PMID: 18546601
42. Lindeman LC, Vogt-Kielland LT, Alestrom P, Collas P (2009) Fish'n ChIPs: chromatin immunoprecipitation in the zebrafish embryo. Methods Mol Biol 567: 75-86. doi: 10.1007/978-1-60327-414-2-5 PMID: 19588086
43. Robu ME, Larson JD, Nasevicius A, Beiraghi S, Brenner C, et al. (2007) p53 activation by knockdown technologies. PLoS Genet 3: e78. PMID: 17530925
44. Piotrowski T, Schilling TF, Brand M, Jiang YJ, Heisenberg CP, et al. (1996) Jaw and branchial arch mutants in zebrafish II: anterior arches and cartilage differentiation. Development 123: 345-356. PMID: 9007254
45. Eames BF, Yan YL, Swartz ME, Levic DS, Knapik EW, et al. (2011) Mutations in fam20b and xylt1 reveal that cartilage matrix controls timing of endochondral ossification by inhibiting chondrocyte maturation. PLoS Genet 7: e1002246. doi: 10.1371/journal.pgen.1002246 PMID: 21901110
46. Lee YH, Aoki Y, Hong CS, Saint-Germain N, Credidio C, et al. (2004) Early requirement of the transcriptional activator Sox9 for neural crest specification in Xenopus. Dev Biol 275: 93-103. PMID: 15464575
47. Yan YL, Miller CT, Nissen RM, Singer A, Liu D, et al. (2002) A zebrafish sox9 gene required for cartilage morphogenesis. Development 129: 5065-5079. PMID: 12397114
48. Dale RM, Topczewski J (2011) Identification of an evolutionarily conserved regulatory element of the zebrafish col2a1a gene. Dev Biol 357: 518-531. doi: 10.1016/j.ydbio.2011.06.020 PMID: 21723274
49. Lakiza O, Miller S, Bunce A, Lee EM, McCauleyDW (2011) SoxE gene duplication and development of the lamprey branchial skeleton: Insights into development and evolution of the neural crest. Dev Biol 359: 149-161. doi: 10.1016/j.ydbio.2011.08.012 PMID: 21889937
50. Oh CD, Maity SN, Lu JF, Zhang J, Liang S, et al. (2010) Identification of SOX9 interaction sites in the genome of chondrocytes. PLoS One 5: e10113. doi: 10.1371/journal.pone.0010113 PMID: 20404928
51. Hayashi MT, Karlseder J (2013) DNA damage associated with mitosis and cytokinesis failure. Oncogene 32: 4593-4601. doi: 10.1038/onc.2012.615 PMID: 23318447
52. Paronetto MP, Minana B, Valcarcel J (2011) The Ewing sarcoma protein regulates DNA damage-induced alternative splicing. Mol Cell 43: 353-368. doi: 10.1016/j.molcel.2011.05.035 PMID: 21816343
53. Furumatsu T, Tsuda M, Yoshida K, Taniguchi N, Ito T, et al. (2005) Sox9 and p300 cooperatively regulate chromatin-mediated transcription. J Biol Chem 280: 35203-35208. PMID: 16109717
54. Tsuda M, Takahashi S, Takahashi Y, Asahara H (2003) Transcriptional co-activators CREB-binding protein and p300 regulate chondrocyte-specific gene expression via association with Sox9. J Biol Chem 278: 27224-27229. PMID: 12732631
55. Anumanthan G, Halder SK, Friedman DB, Datta PK (2006) Oncogenic serine-threonine kinase recep-tor-associated protein modulates the function of Ewing sarcoma protein through a novel mechanism. Cancer Res 66: 10824-10832. PMID: 17108118