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1 Ewing and Ewing like sarcomas Using Genetic Signatures in Refining Small Blue Round Cell Tumor Classification Cristina Antonescu, MD Department of Pathology Disclosure of Relevant Financial Relationships The USCAP requires that anyone in a position to influence or control the content of all CME activities disclose any relevant relationship(s) which they or their spouse/partner have, or have had within the past 12 months with a commercial interest(s) [or the products or services of a commercial interest] that relate to the content of this educational activity and create a conflict of interest. Complete disclosure information is maintained in the USCAP office and has been reviewed by the CME Advisory Committee. No conflict of interest to disclose. Classification of Small Blue Round Cell Sarcomas Ewing Sarcoma Ewing Sarcoma like Tumors Desmoplastic Small Round Cell Tumor Alveolar Rhabdomyosarcoma Small Cell Osteosarcoma Mesenchymal Chondrosarcoma Myxoid/Round cell sarcoma Poorly Differentiated Synovial Sarcoma Ewing Sarcoma Genetic Definition: positive for EWSR1 ETS (FUS ETS) fusions Family members: Ewing sarcoma PNET Adamantinoma like Ewing sarcoma Morphology Classic/atypical/ with complex epithelial differentiation IHC: strong and diffuse membranous staining 1

2 Ewing s Sarcoma Ewing Sarcoma James Ewing first described the tumor in 1921 Endothelioma of bone; endothelial myeloma The tumor was separated from lymphoma or neuroblastoma 2

3 Ewing Sarcoma Pathology Peripheral Neuroectodermal Tumor (PNET) Ewing Sarcoma Pathology Intra cytoplasmic pools of glycogen 3

4 Ewing Sarcoma Immunoprofile Genetic Hallmark Classic Ewing Sarcoma EWSR1 ETS Fusions Cytogenetic Variability: 90% t(11;22)(q24;q12): EWSR1 FLI1 5 8% t(21;22)(q22;q12): EWSR1 ERG 1 2% other ETS genes: ETV1, FEV, E1AF /O13 FLI1 Note: 20% positive for CK, rare cases positive S100 protein or desmin Molecular Variability EWSR1 FLI1 (different exon composition): NH 2 NH NTD EWS Transcriptional Activation Domain NTD EWS ETS D DNA Binding 8 9 COOH ETS D COOH EWSR1 ex7 FLI1 ex9 EWSR1 ex9 FLI1 ex4 Methodology Shift in Molecular Diagnosis of Ewing Sarcoma RT PCR primer design contamination Fusion Structure Variability of EWSR1 FLI1 type 2 type 1 FISH No info Re the partner gene EWSR1 ETS or other EWSR1 sarcomas EWSR1 gene family NH 2 EWSR1 ETS (FLI1; ERG; ETV1) EWSR1 WT1 EWSR1 ATF1 EWSR1 N3A4 EWSR1 CHOP EWSR1 CREB1 EWSR1 POU5F1/PBX1/ ZNF444 1 EWS NT D Transactivation Domain (strong promoter) ETS D Ewing sarcoma/pnet COOH DNA Binding (target specificity) DSRCT Clear cell sarcoma Extraskeletal Myxoid CS Myxoid/Round cell Liposarcoma AFH/GI Clear cell sarcoma Myoepithelial tumors PROMISCUITY of one gene partner/specificity of the other = novel transcription factor 4

5 When is the Molecular Diagnosis required? KER Diagnostic Pitfalls: Atypical morphology Unusual Immunoprofile Insufficient / Inadequate Material Unusual clinical presentation Molecular Diagnosis Differential Diagnosis: Lymphoma Neuroendocrine Ca other primitive sarcomas (DRCT, PD Synov Sarcoma) EWSR1 ERG positive Ewing sarcoma Incidence: 5 8% Similar clinical and pathologic findings as EWS FLi1 fusion IHC: & ERG strong reactivity EWSR1 ERG positive Ewing sarcomas pitfalls in the Molecular Diagnosis Use other method: RT PCR, NGS, FISH for ERG Chen S, Poster# 7, Monday am FUS rearranged Ewing sarcomas EWSR1 & FUS: RNA binding proteins with structural and functional overlap: myxoid liposarcoma AFH Ewing sarcoma Incidence: 7/85 (8%) of SBRCT cases lacking fusions 8 reported cases in the literature FUS positive Ewing s: gene partners: ERG, FEV, NFATC2 Limited pathologic data: similar to EWSR1 positive Ewing sarcoma Chen S, Poster# 7, Monday am 5

6 Ewing Sarcomas with FUS ERG & FUS FEV fusion 19/F, 2 cm well circumscribed superficial thigh mass FUS ERG FEV Ewing Sarcoma with FUS ERG fusion and aberrant neuroectodermal markers Ewing Sarcoma with FUS ERG fusion and aberrant neuroectodermal markers FUS B/A ERG B/A S100 SOX10 6

7 Ewing Sarcoma with Complex Epithelial Differentiation Adamantinoma like Ewing sarcoma (Bridge JA, AJSP 1999) Ewing sarcoma with unusual pathologic features, but typical genetics AE1:AE3 3/F knee soft tissue EMA Ewing Sarcoma with Complex Epithelial Differentiation Adamantinoma like Ewing Sarcoma FISH Analysis showed EWSR1 and FLI1 gene rearrangements Head and Neck Adamantinoma like Ewing Sarcoma # Site Age Sex 1 Ethmoid 37 F 2 Ethmoid 21 M 3 Orbit 7 F 4 Parotid 56 F 5 Parotid 40 F 6 Thyroid 19 M FLI1 Break apart signal by FISH Squamous pearls Nested or micro cystic growth Intra epithelial growth Lezcano C, Head Neck Pathol 2015; Bishop JA, AJSP

8 Head and Neck Adamantinoma like Ewing Sarcoma IHC profile: Head and Neck Adamantinoma like ES Differential Diagnosis: NUT midline carcinoma Myoepithelial carcinoma Basal cell adenocarcinoma Solid Adenoid Cystic ca SNUC Olfactory Neuroblastoma Medullary carcinoma CASTLE CK p40 synapto Lezcano C, Head Neck Pathol 2015; Bishop JA, AJSP 2015 Head and Neck Adamantinoma like ES EWSR1 FLI1 fusion Adamantinoma like Ewing sarcoma with FUS FEV 23/M, anterior mediastinum (NUT neg carcinoma) P40 EWSR1 FLI1 Synapato Chromo 8

9 Ewing sarcoma like tumors (lack the classic EWSR1 ETS fusion) WHO Undifferentiated Round Cell and Spindle Cell Sarcomas 1. EWSR1 fusion to an non ETS transcription factor 2. Alternative (non EWSR1 ) fusions 3. Fusion negative Ewing Sarcoma like Tumors 1. EWSR1 fusion with a non ETS transcription factor EWSR1 NFATc2 (TF, T cell & neuronal development) EWSR1 SMARCA5 (chromatin remodeling gene) EWSR1 SP3 (ZNF transcription factor) Szuhai K et al. Clin Cancer Res 2009 Ewing Sarcoma like Tumors with EWSR1 NFATc2 t(20;22) Ewing Sarcoma like Tumors EWSR1 NFATc2 Fusion and Amplification EWSR1 NFATc2 Amplification of EWSR1 and NFATC2 O13 Amplification of EWSR1 and NFATc2 42/M R femur lesion Szuhai K et al. Clin Cancer Res 2009 NFATc2, nuclear factor of activated T cells, cytoplasmic, calcineurin dependent 2 9

10 EWSR1 NFATc2 Fusion and Amplification 36 year old man with a deep neck soft tissue mass Ewing Sarcoma like Tumors 2. Alternative Fusions (non EWSR1/non ETS) CIC DUX4/CIC FOXO4 BCOR abnormalities IHC profile: pos (diffuse) CK neg S100 protein neg BCOR CCNB3 inversion BCOR MAML3 fusions BCOR Internal Tandem Duplications (ITDs) NFATc2 CIC DUX4 Fusions CIC DUX4 positive Ewing sarcoma like tumors CIC on 19q13.1 Clinical and Pathologic Features: t(4;19) t(10;19) DUX4 on 4q35 DUX4 on 10q26 CIC fusion positive in 68% of EWSR1 negative SBRCT Age: (mean 29 years) M/F ratio: 2 Location: soft tissue (93%) extremities(53%) diffuse / patchy / negative Mixed response to neo/ adjuvant chemotherapy FU: 53% metastases (most in lung) Kawamura Saito M, Hum Mol Genet 2006; Italiano A, Genes Chrom Cancer 2012 Italiano A, Genes Chrom Cancer

11 CIC DUX4 positive Ewing sarcoma like tumors Ewing Sarcoma like Tumors CIC DUX4 Fusion 59/M, Scapular/axilla mass, s/p chemo (20 30% necrosis) 21/M, neck ST Ewing Sarcoma like Tumors CIC DUX4 Fusion A B C Macronucleoli D E F 43/F, buttock rhabdoid abundant cytoplasm 17/M buttock Italiano A, Genes Chrom Cancer

12 WT1 IHC in CIC DUX4 fusion positive SBRCT ERG Green T CIC (19q13) Red C DUX4 (10q26) Specht K, Genes Chr Cancer 2014 CIC DUX4 SBRCT vs Classic Ewing Sarcoma Key Immunophenotypic features for CIC DUX4 SBRCT: positivity (86%)(but only 24% diffuse staining) WT1 pos (100%) Calretinin (70%) ERG pos (20%) NKX2.2 (0%) Distinct gene signature compared to Ewing sarcoma, other sarcoma types and normal tissue: upregulation of ETS transcription factors (ETV1, ETV4 and ETV5) and WT1 CIC DUX4 sarcoma distinct pathogenesis from Ewing sarcoma Kawamura Saito M, Hum Mol Genet 2006; Specht K, Genes Chr Cancer 2014; Yoshida A, AJSP 2016 Significantly worse survival in CIC rearranged sarcomas compared to Ewing sarcoma Overall Survival Ewing sarcomas (n = 53) CIC rearranged sarcomas (n = 20) Ewing Sarcoma like Tumors withbcor gene abnormalities BCOR CCNB3 inversion BCOR MAML3 fusions BCOR ITDs Kaplan Meier analysis of the overall survival log rank test (P < 0.001) Yoshida A, AJSP

13 Ewing Sarcoma like Tumors withbcor CCNB3 Fusions BCOR CCNB3 positive Ewing Sarcoma like Tumor intra X chromosome paracentric inversion RNA seq with paired end sequencing 24/594 (4%) fusion negative primitive sarcomas tested CCNB3 (testis specific cyclin B3) immunohistochemistry is a powerful diagnostic marker ES T2 Pierron G et al. Nature Genetics 2012 Femoral tumor with extraosseous extension T2 15/M Ewing Sarcoma like with BCOR CCNB3 Ewing Sarcoma like with BCOR CCNB3 ( ), Fli1 (+) 15/M Lower leg 13

14 Ewing Sarcoma like with BCOR CCNB3 (n=6 cases) BCOR CCNB3 positive Ewing Sarcoma like Tumor FISH Fusion Assay for detection of break/inversion all male children (7 13 years) 5/6 soft tissue location predominant spindle cell morphology or mixed round/spindle cell areas Possibly better outcome Peters TL, Modern Pathol 2015 Normal Red C, T CCNB3 Green T BCOR (9 Mb away, opposite directions) BCOR CCNB3 positive Ewing Sarcoma like Tumor Novel BCOR MAML3 Fusion Positive Ewing Sarcoma like RNA Sequencing Discovery t(x;4) Cyclin B3 BCOR exon15 CCNB3 exon 5 Specht K, Amer J Surg Pathol

15 BCOR MAML3 Fusion Positive Ewing Sarcoma like 44/M SBRCTs with BCOR Gene Rearrangements BCOR break apart abnormalities were detected in 11% (8/75) of EWSR1/FUS/CIC negative SBRCTs: BCOR MAML3 (n=2) BCOR ZC3H7B (n=2) BCOR (n=4) Morphology: round & spindled, no differerence between genetic subgroups 9/2012 1/2014 & 3/2014 Specht K, Amer J Surg Pathol 2016 immunohistochemistry variable Specht K, Amer J Surg Pathol 2016 SBRCTs with BCOR rearrangements SBRCT 5 SBRCT 5 BCOR MAML3 Fusion Positive Ewing Sarcoma like Mib1 ERG SBRCT 6 SBRCT 13 CCNB3 (cytoplasmic=neg) WT 1 Specht K, Amer J Surg Pathol

16 Infantile SBRCT harbor BCOR ITD similar to CCSK BCOR ITD (41%, 9/22) Overlapping phenotype in SBRCT with BCOR abnormalities BCOR ITD CCSK BCOR MAML3 BCOR CCNB3 Kao YC et al, Platform Tuesday am Summary Classic Ewing sarcomas with EWSR1 ETS fusions show a monotonous cytomorphology and diffuse reactivity Ewing sarcoma like tumors with CIC DUX4 are common in adults, soft tissue location, a less uniform cytomorphology, variable staining and often WT1 nuclear expression Ewing sarcoma like tumors with BCOR CCNB3 inversion occur more often in children, with a spindle or mixed round/spindle morphology, positive for CCNB3 and variable staining. 16

17 Points for Debate Nomenclature What should be the preferred nomenclature used in the next edition of the WHO? Ewing sarcoma like? SBRCT? Round cell sarcoma? How should we reconciliate the presence of spindle cell morphology in the BCOR related SBRCTs Goal a clear message for the Med Oncologists about the fusion positive primitive round cell phenotype most likely treated with Ewing sarcoma type neo adjuvant chemo 17

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