Usefulness of a monoclonal ERG/FLI1 antibody for immunohistochemical discrimination of Ewing family tumors

American Journal of Clinical Pathology

Volumn 139, Issue 6, 2013, Pages 771-779

  Tomlins, Scott A ^a   Palanisamy, Nallasivam ^a   Brenner, J Chad ^a   Stall, Jennifer N ^a   Siddiqui, Javed ^a   Thomas, Dafydd G ^a   Lucas, David R ^a   Chinnaiyan, Arul M ^a   Kunju, Lakshmi P ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

EPR3864; ERG; Ewing tumor; EWSR1; FLI1

Indexed keywords

CD99 ANTIGEN; ERG FLI 1 MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY; TRANSCRIPTION FACTOR FLI 1; UNCLASSIFIED DRUG;

ADULT; ANTIGEN EXPRESSION; ARTICLE; BURKITT LYMPHOMA; EWING SARCOMA; FEMALE; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; LYMPHATIC LEUKEMIA; LYMPHOBLASTOMA; MALE; PRIORITY JOURNAL; SMALL ROUND BLUE CELL TUMOR; SYNOVIAL SARCOMA; TISSUE MICROARRAY; TUMOR CELL;

EPR3864; EWING TUMOR; EWSR1:ERG; EWSR1:FLI1;

ADOLESCENT; ADULT; ANTIBODIES, MONOCLONAL; ANTIGENS, CD; CALMODULIN-BINDING PROTEINS; CELL ADHESION MOLECULES; FEMALE; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; NEOPLASM PROTEINS; PROSTATIC NEOPLASMS; PROTO-ONCOGENE PROTEIN C-FLI-1; RNA-BINDING PROTEINS; SARCOMA, EWING; TISSUE ARRAY ANALYSIS; TRANS-ACTIVATORS;

EID: 84878417492     PISSN: 00029173     EISSN: 19437722     Source Type: Journal    
DOI: 10.1309/AJCPN4L1BMRQPEIT     Document Type: Article

References (62)

1. de Alava E, Gerald WL. Molecular biology of the Ewing's sarcoma/primitive neuroectodermal tumor family. J Clin Oncol. 2000;18:204-213. (Pubitemid 30036354)
2. Khoury JD. Ewing sarcoma family of tumors. Adv Anat Pathol. 2005;12:212-220. (Pubitemid 41216052)
3. Sankar S, Lessnick SL. Promiscuous partnerships in Ewing's sarcoma. Cancer Genet. 2011;204:351-365.
4. Toomey EC, Schiffman JD, Lessnick SL. Recent advances in the molecular pathogenesis of Ewing's sarcoma. Oncogene. 2010;29:4504-4516.
5. Folpe AL, Hill CE, Parham DM, et al. Immunohistochemical detection of FLI-1 protein expression: a study of 132 round cell tumors with emphasis on CD99-positive mimics of Ewing's sarcoma/primitive neuroectodermal tumor. Am J Surg Pathol. 2000;24:1657-1662.
6. Llombart-Bosch A, Navarro S. Immunohistochemical detection of EWS and FLI-1 proteins in Ewing sarcoma and primitive neuroectodermal tumors: comparative analysis with CD99 (MIC-2) expression. Appl Immunohistochem Mol Morphol. 2001;9:255-260. (Pubitemid 32783049)
7. Rossi S, Orvieto E, Furlanetto A, et al. Utility of the immunohistochemical detection of FLI-1 expression in round cell and vascular neoplasm using a monoclonal antibody. Mod Pathol. 2004;17:547-552. (Pubitemid 38868421)
8. Folpe AL, Goldblum JR, Rubin BP, et al. Morphologic and immunophenotypic diversity in Ewing family tumors: a study of 66 genetically confirmed cases. Am J Surg Pathol. 2005;29:1025-1033. (Pubitemid 41045546)
9. Mhawech-Fauceglia P, Herrmann F, Penetrante R, et al. Diagnostic utility of FLI-1 monoclonal antibody and dual-colour, break-apart probe fluorescence in situ (FISH) analysis in Ewing's sarcoma/primitive neuroectodermal tumour (EWS/PNET): a comparative study with CD99 and FLI-1 polyclonal antibodies. Histopathology. 2006;49:569-575. (Pubitemid 44924288)
10. Llombart-Bosch A, Machado I, Navarro S, et al. Histological heterogeneity of Ewing's sarcoma/PNET: an immunohistochemical analysis of 415 genetically confirmed cases with clinical support. Virchows Arch. 2009;455:397-411.
11. Gamberi G, Cocchi S, Benini S, et al. Molecular diagnosis in Ewing family tumors: the Rizzoli experience - 222 consecutive cases in four years. J Mol Diagn. 2011;13:313-324.
12. Downing JR, Head DR, Parham DM, et al. Detection of the (11;22)(q24;q12) translocation of Ewing's sarcoma and peripheral neuroectodermal tumor by reverse transcription polymerase chain reaction. Am J Pathol. 1993;143:1294-1300. (Pubitemid 24057100)
13. Ladanyi M, Lewis R, Garin-Chesa P, et al. EWS rearrangement in Ewing's sarcoma and peripheral neuroectodermal tumor: molecular detection and correlation with cytogenetic analysis and MIC2 expression. Diagn Mol Pathol. 1993;2:141-146. (Pubitemid 23252431)
14. Yamaguchi U, Hasegawa T, Morimoto Y, et al. A practical approach to the clinical diagnosis of Ewing's sarcoma/primitive neuroectodermal tumour and other small round cell tumours sharing EWS rearrangement using new fluorescence in situ hybridisation probes for EWSR1 on formalin fixed, paraffin wax embedded tissue. J Clin Pathol. 2005;58:1051-1056. (Pubitemid 41416054)
15. Qian X, Jin L, Shearer BM, et al. Molecular diagnosis of Ewing's sarcoma/primitive neuroectodermal tumor in formalin-fixed paraffin-embedded tissues by RT-PCR and fluorescence in situ hybridization. Diagn Mol Pathol. 2005;14:23-28. (Pubitemid 40283858)
16. Kovar H, Dworzak M, Strehl S, et al. Overexpression of the pseudoautosomal gene MIC2 in Ewing's sarcoma and peripheral primitive neuroectodermal tumor. Oncogene. 1990;5:1067-1070.
17. Ambros IM, Ambros PF, Strehl S, et al. MIC2 is a specific marker for Ewing's sarcoma and peripheral primitive neuroectodermal tumors: evidence for a common histogenesis of Ewing's sarcoma and peripheral primitive neuroectodermal tumors from MIC2 expression and specific chromosome aberration. Cancer. 1991;67:1886-1893.
18. Hamilton G, Fellinger EJ, Schratter I, et al. Characterization of a human endocrine tissue and tumor-associated Ewing's sarcoma antigen. Cancer Res. 1988;48:6127-6131.
19. Weidner N, Tjoe J. Immunohistochemical profile of monoclonal antibody O13: antibody that recognizes glycoprotein p30/32MIC2 and is useful in diagnosing Ewing's sarcoma and peripheral neuroepithelioma. Am J Surg Pathol. 1994;18:486-494. (Pubitemid 24134090)
20. Lin O, Filippa DA, Teruya-Feldstein J. Immunohistochemical evaluation of FLI-1 in acute lymphoblastic lymphoma (ALL): a potential diagnostic pitfall. Appl Immunohistochem Mol Morphol. 2009;17:409-412.
21. Buxton D, Bacchi CE, Gualco G, et al. Frequent expression of CD99 in anaplastic large cell lymphoma: a clinicopathologic and immunohistochemical study of 160 cases. Am J Clin Pathol. 2009;131:574-579.
22. Hartel PH, Fanburg-Smith JC, Frazier AA, et al. Primary pulmonary and mediastinal synovial sarcoma: a clinicopathologic study of 60 cases and comparison with five prior series. Mod Pathol. 2007;20:760-769. (Pubitemid 46933447)
23. Machen SK, Fisher C, Gautam RS, et al. Utility of cytokeratin subsets for distinguishing poorly differentiated synovial sarcoma from peripheral primitive neuroectodermal tumour. Histopathology. 1998;33:501-507. (Pubitemid 28563374)
24. Fellinger EJ, Garin-Chesa P, Triche TJ, et al. Immunohistochemical analysis of Ewing's sarcoma cell surface antigen p30/32MIC2. Am J Pathol. 1991;139:317-325.
25. Ramani P, Rampling D, Link M. Immunocytochemical study of 12E7 in small round-cell tumours of childhood: an assessment of its sensitivity and specificity. Histopathology. 1993;23:557-561. (Pubitemid 24034824)
26. Li L, Li J, Hao C, et al. Immunohistochemical evaluation of solid pseudopapillary tumors of the pancreas: the expression pattern of CD99 is highly unique. Cancer Lett. 2011;310:9-14.
27. McCluggage WG, Kennedy K, Busam KJ. An immunohistochemical study of cervical neuroendocrine carcinomas: neoplasms that are commonly TTF1 positive and which may express CK20 and P63. Am J Surg Pathol. 2010;34:525-532.
28. Chen G, Folpe AL, Colby TV, et al. Angiomatoid fibrous histiocytoma: unusual sites and unusual morphology. Mod Pathol. 2011;24:1560-1570.
29. Chen H, Zeng XW, Wu JS, et al. Solitary fibrous tumor of the central nervous system: a clinicopathologic study of 24 cases. Acta Neurochir (Wien). 2012;154:237-248.
30. Magro G, Caltabiano R, Kacerovska D, et al. Vulvovaginal myofibroblastoma: expanding the morphological and immunohistochemical spectrum: a clinicopathologic study of 10 cases. Hum Pathol. 2012;43:243-253.
31. 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.
32. May WA, Gishizky ML, Lessnick SL, et al. 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 U S A. 1993;90:5752-5756. (Pubitemid 23176240)
33. Potikyan G, France KA, Carlson MR, et al. Genetically defined EWS/FLI1 model system suggests mesenchymal origin of Ewing's family tumors. Lab Invest. 2008;88:1291-1302.
34. Jimenez RE, Folpe AL, Lapham RL, et al. Primary Ewing's sarcoma/primitive neuroectodermal tumor of the kidney: a clinicopathologic and immunohistochemical analysis of 11 cases. Am J Surg Pathol. 2002;26:320-327. (Pubitemid 34184455)
35. Mhawech-Fauceglia P, Herrmann FR, Bshara W, et al. Friend leukaemia integration-1 expression in malignant and benign tumours: a multiple tumour tissue microarray analysis using polyclonal antibody. J Clin Pathol. 2007;60:694-700. (Pubitemid 46975228)
36. Nilsson G, Wang M, Wejde J, et al. Detection of EWS/FLI-1 by immunostaining: an adjunctive tool in diagnosis of Ewing's sarcoma and primitive neuroectodermal tumour on cytological samples and paraffin-embedded archival material. Sarcoma. 1999;3:25-32. (Pubitemid 29185461)
37. Lee AF, Hayes MM, Lebrun D, et al. FLI-1 distinguishes Ewing sarcoma from small cell osteosarcoma and mesenchymal chondrosarcoma. Appl Immunohistochem Mol Morphol. 2011;19:233-238.
38. Terrier-Lacombe MJ, Guillou L, Chibon F, et al. Superficial primitive Ewing's sarcoma: a clinicopathologic and molecular cytogenetic analysis of 14 cases. Mod Pathol. 2009;22:87-94.
39. Folpe AL, Chand EM, Goldblum JR, et al. Expression of Fli-1, a nuclear transcription factor, distinguishes vascular neoplasms from potential mimics. Am J Surg Pathol. 2001;25:1061-1066. (Pubitemid 32685904)
40. Kumar-Sinha C, Tomlins SA, Chinnaiyan AM. Recurrent gene fusions in prostate cancer. Nat Rev Cancer. 2008;8:497-511.
41. Tomlins SA, Bjartell A, Chinnaiyan AM, et al. ETS gene fusions in prostate cancer: from discovery to daily clinical practice. Eur Urol. 2009;56:275-286.
42. Rubin MA, Maher CA, Chinnaiyan AM. Common gene rearrangements in prostate cancer. J Clin Oncol. 2011;29:3659-3668.
43. Paulo P, Barros-Silva JD, Ribeiro FR, et al. FLI1 is a novel ETS transcription factor involved in gene fusions in prostate cancer. Genes Chromosomes Cancer. 2012;51:240-249.
44. Tomlins SA, Rhodes DR, Perner S, et al. Recurrent fusion of TMPRSS2 and ETS transcription factor genes in prostate cancer. Science. 2005;310:644-648. (Pubitemid 41528150)
45. Tomlins SA, Palanisamy N, Siddiqui J, et al. Antibody based detection of ERG rearrangements in prostate core biopsies, including diagnostically challenging cases: ERG staining in prostate core biopsies. Arch Pathol Lab Med. 2012;136:935-946.
46. Braun M, Goltz D, Shaikhibrahim Z, et al. ERG protein expression and genomic rearrangement status in primary and metastatic prostate cancer - a comparative study of two monoclonal antibodies. Prostate Cancer Prostatic Dis. 2012;15:165-169.
47. Yaskiv O, Zhang X, Simmerman K, et al. The utility of ERG/P63 double immunohistochemical staining in the diagnosis of limited cancer in prostate needle biopsies. Am J Surg Pathol. 2011;35:1062-1068.
48. van Leenders GJ, Boormans JL, Vissers CJ, et al. Antibody EPR3864 is specific for ERG genomic fusions in prostate cancer: implications for pathological practice. Mod Pathol. 2011;24:1128-1138.
49. Minner S, Enodien M, Sirma H, et al. ERG status is unrelated to PSA recurrence in radically operated prostate cancer in the absence of antihormonal therapy. Clin Cancer Res. 2011;17:5878-5888.
50. Hoogland AM, Jenster G, van Weerden WM, et al. ERG immunohistochemistry is not predictive for PSA recurrence, local recurrence or overall survival after radical prostatectomy for prostate cancer. Mod Pathol. 2012;25:471-479.
51. He H, Magi-Galluzzi C, Li J, et al. The diagnostic utility of novel immunohistochemical marker ERG in the workup of prostate biopsies with "atypical glands suspicious for cancer." Am J Surg Pathol. 2011;35:608-614.
52. Falzarano SM, Zhou M, Carver P, et al. ERG gene rearrangement status in prostate cancer detected by immunohistochemistry. Virchows Arch. 2011;459:441-447.
53. Park K, Tomlins SA, Mudaliar KM, et al. Antibody-based detection of ERG rearrangement-positive prostate cancer. Neoplasia. 2010;12:590-598.
54. Mohamed AA, Tan SH, Mikhalkevich N, et al. Ets family protein, erg expression in developing and adult mouse tissues by a highly specific monoclonal antibody. J Cancer. 2010;1:197-208.
55. Young A, Palanisamy N, Siddiqui J, et al. Correlation of urine TMPRSS2:ERG and PCA3 to ERG+ and total prostate cancer burden. Am J Clin Pathol. 2012;138:685-696.
56. Miettinen M, Wang ZF, Paetau A, et al. ERG transcription factor as an immunohistochemical marker for vascular endothelial tumors and prostatic carcinoma. Am J Surg Pathol. 2011;35:432-441.
57. Rosen P, Sesterhenn IA, Brassell SA, et al. Clinical potential of the ERG oncoprotein in prostate cancer. Nat Rev Urol. 2012;9:131-137.
58. Lucas DR, Bentley G, Dan ME, et al. Ewing sarcoma vs lymphoblastic lymphoma: a comparative immunohistochemical study. Am J Clin Pathol. 2001;115:11-17. (Pubitemid 33695086)
59. Ozdemirli M, Fanburg-Smith JC, Hartmann DP, et al. Differentiating lymphoblastic lymphoma and Ewing's sarcoma: lymphocyte markers and gene rearrangement. Mod Pathol. 2001;14:1175-1182. (Pubitemid 33063213)
60. Minner S, Luebke AM, Kluth M, et al. High level of Ets-related gene expression has high specificity for prostate cancer: a tissue microarray study of 11 483 cancers. Histopathology. 2012;61:445-453.
61. Wang WL, Patel NR, Caragea M, et al. Expression of ERG, an Ets family transcription factor, identifies ERG-rearranged Ewing sarcoma. Mod Pathol. 2012;25:1378-1383.
62. Yaskiv O, Rubin BP, He H, et al. ERG protein expression in human tumors detected with a rabbit monoclonal antibody. Am J Clin Pathol. 2012;138:803-810.