Recurrent FOXK1::GRHL and GPS2::GRHL fusions in trichogerminoma

J Pathol. 2022 May;257(1):96-108. doi: 10.1002/path.5872. Epub 2022 Mar 28.

Abstract

We report 21 cases of trichogerminoma harbouring previously undescribed FOXK1::GRHL1/2 or GPS2::GRHL1/2/3 in-frame fusion transcripts. Microscopic examination of a preliminary set of five cases revealed well-delimitated tumours located in the dermis with frequent extension to the subcutaneous tissue. Tumours presented a massive and nodular architecture and consisted of a proliferation of basaloid cells. A biphasic pattern sometime resulting in tumour cell nests ('cell balls') was present. Immunohistochemistry demonstrated the expression of cytokeratins (CKs) 15, 17, and PHLDA1. In addition, numerous CK20-positive Merkel cells were detected. RNA sequencing (RNA-seq) revealed a FOXK1::GRHL1 chimeric transcript in three cases and a FOXK1::GRHL2 fusion in two cases. In a second series for validation (n = 88), FOXK1::GRHL1/2 fusion transcripts were detected by RT-qPCR or FISH in an additional 12 trichogerminomas and not in any other follicular tumour entities or basal cell carcinoma cases (n = 66). Additional RNA-seq analysis in trichogerminoma cases without detected FOXK1::GRHL1/2 rearrangements revealed GPS2::GRHL1 fusion transcripts in two cases, GPS2::GRHL2 in one case, and GPS2::GRHL3 fusion transcript in one case. Therefore, our study strongly suggests that GRHL1/2/3 gene rearrangements might represent the oncogenic driver in trichogerminoma, a subset of follicular tumours characterized by immature features and numerous Merkel cells. © 2022 The Pathological Society of Great Britain and Ireland.

Keywords: FOXK1; GRHL; GSP2; Merkel cells; fusion transcript; trichoblastoma; trichogerminoma.

MeSH terms

  • Forkhead Transcription Factors / genetics
  • Gene Rearrangement
  • Humans
  • Immunohistochemistry
  • Skin Neoplasms* / genetics
  • Skin Neoplasms* / pathology
  • United Kingdom

Substances

  • FOXK1 protein, human
  • Forkhead Transcription Factors