Ewing sarcoma with ERG gene rearrangements: A molecular study focusing on the prevalence of FUS-ERG and common pitfalls in detecting EWSR1-ERG fusions by FISH

Genes Chromosomes and Cancer

Volumn 55, Issue 4, 2016, Pages 340-349

  Chen, Sonja ^a   Deniz, Kemal ^b   Sung, Yun Shao ^a   Zhang, Lei ^a   Dry, Sarah ^c   Antonescu, Cristina R ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b ERCIYES UNIVERSITY   (Turkey)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RNA; TRANSCRIPTION FACTOR ERG; CALMODULIN BINDING PROTEIN; ERG PROTEIN, HUMAN; EWSR1 PROTEIN, HUMAN; FUS PROTEIN, HUMAN; RNA BINDING PROTEIN; RNA BINDING PROTEIN FUS; TRANSACTIVATOR PROTEIN;

ADOLESCENT; ADULT; ARTICLE; CELL NUCLEUS MEMBRANE; CHILD; CLINICAL FEATURE; COHORT ANALYSIS; CONTROLLED STUDY; EWING SARCOMA; EWSR1 ERG FUSION GENE; FEMALE; FLUORESCENCE IN SITU HYBRIDIZATION; FUS ERG FUSION GENE; FUSION GENE; GENE FUSION; GENE REARRANGEMENT; GENETIC IDENTIFICATION; HUMAN; HUMAN TISSUE; MAJOR CLINICAL STUDY; MALE; MIDDLE AGED; MOLECULAR DIAGNOSIS; NEOPLASM; PRESCHOOL CHILD; PRIORITY JOURNAL; RNA SEQUENCE; SCHOOL CHILD; SMALL BLUE ROUND CELL TUMOR; YOUNG ADULT; GENETICS; META ANALYSIS; PATHOLOGY;

ADOLESCENT; ADULT; CALMODULIN-BINDING PROTEINS; CHILD; CHILD, PRESCHOOL; COHORT STUDIES; FEMALE; GENE REARRANGEMENT; HUMANS; IN SITU HYBRIDIZATION, FLUORESCENCE; MALE; MIDDLE AGED; RNA-BINDING PROTEIN FUS; RNA-BINDING PROTEINS; SARCOMA, EWING; TRANS-ACTIVATORS; TRANSCRIPTIONAL REGULATOR ERG; YOUNG ADULT;

EID: 84958762504     PISSN: 10452257     EISSN: 10982264     Source Type: Journal    
DOI: 10.1002/gcc.22336     Document Type: Article

References (36)

1. Antonescu C. 2014. Round cell sarcomas beyond Ewing: Emerging entities. Histopathology 64:26-37.
2. Antonescu CR, Zhang L, Chang NE, Pawel BR, Travis W, Katabi N, Edelman M, Rosenberg AE, Nielsen GP, Dal Cin P, Fletcher CD. 2010. EWSR1-POU5F1 fusion in soft tissue myoepithelial tumors. A molecular analysis of sixty-six cases, including soft tissue, bone, and visceral lesions, showing common involvement of the EWSR1 gene. Genes Chromosomes Cancer 49:1114-1124.
3. Berg T, Kalsaas AH, Buechner J, Busund LT. 2009. Ewing sarcoma-peripheral neuroectodermal tumor of the kidney with a FUS-ERG fusion transcript. Cancer Genet Cytogenet 194:53-57.
4. Bridge JA, Fidler ME, Neff JR, Degenhardt J, Wang M, Walker C, Dorfman HD, Baker KS, Seemayer TA. 1999. Adamantinoma-like Ewing's sarcoma: Genomic confirmation, phenotypic drift. Am J Surg Pathol 23:159-165.
5. Brohl AS, Solomon DA, Chang W, Wang J, Song Y, Sindiri S, Patidar R, Hurd L, Chen L, Shern JF, Liao H, Wen X, Gerard J, Kim JS, Lopez Guerrero JA, Machado I, Wai DH, Picci P, Triche T, Horvai AE, Miettinen M, Wei JS, Catchpool D, Llombart-Bosch A, Waldman T, Khan J. 2014. The genomic landscape of the Ewing Sarcoma family of tumors reveals recurrent STAG2 mutation. PLoS Genet 10:e1004475
6. Choi HW, Shin MG, Sawyer JR, Cho D, Kee SJ, Baek HJ, Kook H, Kim HJ, Shin JH, Suh SP, Hwang TJ, Ryang DW. 2006. Unusual type of TLS/FUS-ERG chimeric transcript in a pediatric acute myelocytic leukemia with 47, XX, +10, t(16;21)(p11;q22). Cancer Genet Cytogenet 167:172-176.
7. Delattre O, Zucman J, Plougastel B, Desmaze C, Melot T, Peter M, Kovar H, Joubert I, de Jong P, Rouleau G, et al. 1992. Gene fusion with an ETS DNA-binding domain caused by chromosome translocation in human tumours. Nature 359:162-165.
8. Delattre O, Zucman J, Melot T, Garau XS, Zucker JM, Lenoir GM, Ambros PF, Sheer D, Turc-Carel C, Triche TJ, et al. 1994. The Ewing family of tumors-a subgroup of small-round-cell tumors defined by specific chimeric transcripts. N Engl J Med 331:294-299.
9. Desmaze C, Brizard F, Turc-Carel C, Melot T, Delattre O, Thomas G, Aurias A. 1997. Multiple chromosomal mechanisms generate an EWS/FLI1 or an EWS/ERG fusion gene in Ewing tumors. Cancer Genet Cytogenet 97:12-19.
10. Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, Batut P, Chaisson M, Gingeras TR. 2013. STAR: Ultrafast universal RNA-seq aligner. Bioinformatics 29:15-21.
11. Ewing J. 1921. Diffuse endothelioma of bone. Proc NY Path Soc 21:17-24.
12. Fisher C. 2014. The diversity of soft tissue tumours with EWSR1 gene rearrangements: A review. Histopathology 64:134-150.
13. Folpe AL, Goldblum JR, Rubin BP, Shehata BM, Liu W, Dei Tos AP, Weiss SW. 2005. Morphologic and immunophenotypic diversity in Ewing family tumors: A study of 66 genetically confirmed cases. Am J Surg Pathol 29:1025-1033.
14. Ginsberg JP, de Alava E, Ladanyi M, Wexler LH, Kovar H, Paulussen M, Zoubek A, Dockhorn-Dworniczak B, Juergens H, Wunder JS, Andrulis IL, Malik R, Sorensen PH, Womer RB, Barr FG. 1999. EWS-FLI1 and EWS-ERG gene fusions are associated with similar clinical phenotypes in Ewing's sarcoma. J Clin Oncol 17:1809-1814.
15. Habegger L, Sboner A, Gianoulis TA, Rozowsky J, Agarwal A, Snyder M, Gerstein M. 2011. RSEQtools: A modular framework to analyze RNA-Seq data using compact, anonymized data summaries. Bioinformatics 27:281-283.
16. Italiano A, Sung YS, Zhang L, Singer S, Maki RG, Coindre JM, Antonescu CR. 2012. High prevalence of CIC fusion with double-homeobox (DUX4) transcription factors in EWSR1-negative undifferentiated small blue round cell sarcomas. Genes Chromosomes Cancer 51:207-218.
17. Jeon IS, Davis JN, Braun BS, Sublett JE, Roussel MF, Denny CT, Shapiro DN. 1995. A variant Ewing's sarcoma translocation (7;22) fuses the EWS gene to the ETS gene ETV1. Oncogene 10:1229-1234.
18. Kaneko Y, Yoshida K, Handa M, Toyoda Y, Nishihira H, Tanaka Y, Sasaki Y, Ishida S, Higashino F, Fujinaga K. 1996. Fusion of an ETS-family gene, EIAF, to EWS by t(17;22)(q12;q12) chromosome translocation in an undifferentiated sarcoma of infancy. Genes Chromosomes Cancer 15:115-121.
19. Kaneko Y, Kobayashi H, Handa M, Satake N, Maseki N. 1997. EWS-ERG fusion transcript produced by chromosomal insertion in a Ewing sarcoma. Genes Chromosomes Cancer 18:228-231.
20. Kawamura-Saito M, Yamazaki Y, Kaneko K, Kawaguchi N, Kanda H, Mukai H, Gotoh T, Motoi T, Fukayama M, Aburatani H, Takizawa T, Nakamura T. 2006. Fusion between CIC and DUX4 up-regulates PEA3 family genes in Ewing-like sarcomas with t(4;19)(q35;q13) translocation. Hum Mol Genet 15:2125-2137.
21. Llombart-Bosch A, Blache R, Peydro-Olaya A. 1978. Ultrastructural study of 28 cases of Ewing's sarcoma: Typical and atypical forms. Cancer 41:1362-1373.
22. Llombart-Bosch A, Machado I, Navarro S, Bertoni F, Bacchini P, Alberghini M, Karzeladze A, Savelov N, Petrov S, Alvarado-Cabrero I, Mihaila D, Terrier P, Lopez-Guerrero JA, Picci P. 2009. Histological heterogeneity of Ewing's sarcoma/PNET: An immunohistochemical analysis of 415 genetically confirmed cases with clinical support. Virchows Arch 455:397-411.
23. Maire G, Brown CW, Bayani J, Pereira C, Gravel DH, Bell JC, Zielenska M, Squire JA. 2008. Complex rearrangement of chromosomes 19, 21, and 22 in Ewing sarcoma involving a novel reciprocal inversion-insertion mechanism of EWS-ERG fusion gene formation: A case analysis and literature review. Cancer Genet Cytogenet 181:81-92.
24. Mastrangelo T, Modena P, Tornielli S, Bullrich F, Testi MA, Mezzelani A, Radice P, Azzarelli A, Pilotti S, Croce CM, Pierotti MA, Sozzi G. 2000. A novel zinc finger gene is fused to EWS in small round cell tumor. Oncogene 19:3799-3804.
25. Ng TL, O'Sullivan MJ, Pallen CJ, Hayes M, Clarkson PW, Winstanley M, Sorensen PH, Nielsen TO, Horsman DE. 2007. Ewing sarcoma with novel translocation t(2;16) producing an in-frame fusion of FUS and FEV. J Mol Diagn 9:459-463.
26. Peter M, Couturier J, Pacquement H, Michon J, Thomas G, Magdelenat H, Delattre O. 1997. A new member of the ETS family fused to EWS in Ewing tumors. Oncogene 14:1159-1164.
27. Pierron G, Tirode F, Lucchesi C, Reynaud S, Ballet S, Cohen-Gogo S, Perrin V, Coindre JM, Delattre O. 2012. A new subtype of bone sarcoma defined by BCOR-CCNB3 gene fusion. Nat Genet 44:461-466.
28. Puls F, Niblett A, Marland G, Gaston CL, Douis H, Mangham DC, Sumathi VP, Kindblom LG. 2014. BCOR-CCNB3 (Ewing-like) sarcoma: A clinicopathologic analysis of 10 cases, in comparison with conventional Ewing sarcoma. Am J Surg Pathol 38:1307-1318.
29. Quail MA, Kozarewa I, Smith F, Scally A, Stephens PJ, Durbin R, Swerdlow H, Turner DJ. 2008. A large genome center's improvements to the Illumina sequencing system. Nat Methods 5:1005-1010.
30. Sboner A, Habegger L, Pflueger D, Terry S, Chen DZ, Rozowsky JS, Tewari AK, Kitabayashi N, Moss BJ, Chee MS, Demichelis F, Rubin MA, Gerstein MB. 2010. FusionSeq: A modular framework for finding gene fusions by analyzing paired-end RNA-sequencing data. Genome Biol 11:R104
31. Shing DC, McMullan DJ, Roberts P, Smith K, Chin SF, Nicholson J, Tillman RM, Ramani P, Cullinane C, Coleman N. 2003. FUS/ERG gene fusions in Ewing's tumors. Cancer Res 63:4568-4576.
32. Specht K, Sung YS, Zhang L, Richter GH, Fletcher CD, Antonescu CR. 2014. Distinct transcriptional signature and immunoprofile of CIC-DUX4 fusion-positive round cell tumors compared to EWSR1-rearranged Ewing sarcomas: Further evidence toward distinct pathologic entities. Genes Chromosomes Cancer 53:622-633.
33. Sumegi J, Nishio J, Nelson M, Frayer RW, Perry D, Bridge JA. 2011. A novel t(4;22)(q31;q12) produces an EWSR1-SMARCA5 fusion in extraskeletal Ewing sarcoma/primitive neuroectodermal tumor. Mod Pathol 24:333-342.
34. Szuhai K, Ijszenga M, Tanke HJ, Rosenberg C, Hogendoorn PC. 2006. Molecular cytogenetic characterization of four previously established and two newly established Ewing sarcoma cell lines. Cancer Genet Cytogenet 166:173-179.
35. Szuhai K, Ijszenga M, de Jong D, Karseladze A, Tanke HJ, Hogendoorn PC. 2009. The NFATc2 gene is involved in a novel cloned translocation in a Ewing sarcoma variant that couples its function in immunology to oncology. Clin Cancer Res 15:2259-2268.
36. Wang L, Bhargava R, Zheng T, Wexler L, Collins MH, Roulston D, Ladanyi M. 2007. Undifferentiated small round cell sarcomas with rare EWS gene fusions: Identification of a novel EWS-SP3 fusion and of additional cases with the EWS-ETV1 and EWS-FEV fusions. J Mol Diagn 9:498-509.