Superficial Neurocristic EWSR1::FLI1 Fusion Tumor: A Distinctive, Clinically Indolent, S100 Protein/SOX10-Positive Neoplasm

Mod Pathol. 2024 Aug;37(8):100537. doi: 10.1016/j.modpat.2024.100537. Epub 2024 Jun 10.

Abstract

It is now understood that identical gene fusions may be shared by different entities. We report a distinctive neoplasm of the skin and subcutis, harboring the Ewing sarcoma-associated EWSR1::FLI1 fusion but differing otherwise from Ewing sarcoma. Slides and blocks for 5 cutaneous neoplasms coded as other than Ewing sarcoma and harboring EWSR1::FLI1 were retrieved. Immunohistochemical and molecular genetic results were abstracted from reports. Methylation profiling was performed. Clinical information was obtained. The tumors occurred in 4 men and 1 woman (median: 25 years of age; range: 19-69 years) and involved the skin/subcutis of the back (2), thigh, buttock, and chest wall (median: 2.4 cm; range: 1-11 cm). Two tumors were present "years" before coming to clinical attention. The lesions were multinodular and circumscribed and consisted of nests of bland, round cells admixed with hyalinized collagenous bands containing spindled cells. Hemorrhage and cystic change were often present; necrosis was absent. All were diffusely S100 protein/SOX10-positive; 4 of 5 were CD99-negative. One tested case was strongly positive for NKX2.2. A variety of other tested markers were either focally positive (glial fibrillary acidic protein, p63) or negative. Molecular genetic results were as follows: EWSR1 exon 7::FLI1 exon 8, EWSR1 exon 11::FLI1 exon 5, EWSR1 exon 11::FLI1 exon 6, EWSR1 exon 7::FLI1 exon 6, and EWSR1 exon 10::FLI1 exon 6. Methylation profiling (3 cases) showed these to form a unique cluster, distinct from Ewing sarcoma. All patients underwent excision with negative margins; one received 1 cycle of chemotherapy. Clinical follow-up showed all patients to be alive without disease (median: 17 months; range: 11-62 months). Despite similar gene fusions, the morphologic, immunohistochemical, epigenetic, and clinical features of these unique EWSR1::FLI1-fused neoplasms of the skin and subcutis differ substantially from Ewing sarcoma. Interestingly, EWSR1 rearrangements involved exons 10 or 11, only rarely seen in Ewing sarcoma, in a majority of cases. Superficial neurocristic EWSR1::FLI1 fusion tumors should be rigorously distinguished from true cutaneous Ewing sarcomas.

Keywords: EWSR1::FLI1; Ewing sarcoma; cutaneous neoplasms; immunohistochemistry; methylation profiling; next-generation sequencing.

MeSH terms

  • Adult
  • Aged
  • Biomarkers, Tumor* / genetics
  • DNA Methylation
  • Female
  • Homeobox Protein Nkx-2.2*
  • Homeodomain Proteins
  • Humans
  • Immunohistochemistry
  • Male
  • Middle Aged
  • Nuclear Proteins
  • Oncogene Proteins, Fusion* / genetics
  • Proto-Oncogene Protein c-fli-1 / genetics
  • RNA-Binding Protein EWS / genetics
  • RNA-Binding Proteins / genetics
  • S100 Proteins* / genetics
  • S100 Proteins* / metabolism
  • SOXE Transcription Factors* / genetics
  • Sarcoma, Ewing / genetics
  • Sarcoma, Ewing / pathology
  • Skin Neoplasms* / genetics
  • Skin Neoplasms* / pathology
  • Transcription Factors / genetics
  • Young Adult

Substances

  • Biomarkers, Tumor
  • EWSR1 protein, human
  • EWSR1-FLI1 fusion protein, human
  • Homeobox Protein Nkx-2.2
  • Homeodomain Proteins
  • NKX2-2 protein, human
  • nkx2.2b protein, zebrafish
  • Nuclear Proteins
  • Oncogene Proteins, Fusion
  • Proto-Oncogene Protein c-fli-1
  • RNA-Binding Protein EWS
  • RNA-Binding Proteins
  • S100 Proteins
  • SOX10 protein, human
  • SOXE Transcription Factors
  • Transcription Factors