Identification of increased dedifferentiation along the Prom1+ cancer cells in Müllerian adenosarcoma with sarcomatous overgrowth

Br J Cancer. 2025 Mar;132(5):438-449. doi: 10.1038/s41416-025-02943-4. Epub 2025 Feb 7.

Abstract

Background: Müllerian adenosarcoma (MA) is a rare tumour accounts for 5-7% of uterine sarcomas. Tumours with sarcomatous overgrowth (MASO) or high-grade tend to be aggressive. However, the tumour aetiology is elusive.

Methods: Single-cell RNA sequencing and bioinformatics were used to analyse the MASO and paired normal tissues. Expression and clinical significance of key genes were analysed by TCGA data and immunohistochemistry. In vitro experiment was used to verify the effect of E2F1 in cell dedifferentiation.

Results: We prove malignant stromal cells originate from fibrous tissue, Prom1-derived with complex intra-tumoral heterogeneity. Along the developmental trajectory, we discover three phenotypes of Prom1+ cancer cells (differentiation-like, intermediate-like, dedifferentiation-like). A distinct HMGB2/3+ subtype of Prom1+ cluster is predominant dedifferentiation-like cancer cells, with high proliferation and stemness traits at the tail of trajectory. E2F1 is a master transcription factor for Prom1 lineage dedifferentiation, which could occupy the HMGB2/3 promoter to enhance their transcription, facilitating the stemness and self-renewal of cancer cells. Gene signature of Prom1 lineage is associated with poorer prognosis in uterine malignancies. The expression of Prom1 and HMGB3 was verified by immunohistochemistry.

Conclusions: Our study reveal the heterogeneity and dynamics of Prom1 lineage cells, which are key to tailor efficient therapies for MASO.

MeSH terms

  • AC133 Antigen* / genetics
  • AC133 Antigen* / metabolism
  • Adenosarcoma* / genetics
  • Adenosarcoma* / metabolism
  • Adenosarcoma* / pathology
  • Biomarkers, Tumor / genetics
  • Biomarkers, Tumor / metabolism
  • Cell Dedifferentiation* / genetics
  • Cell Line, Tumor
  • Cell Proliferation
  • E2F1 Transcription Factor / genetics
  • E2F1 Transcription Factor / metabolism
  • Female
  • Gene Expression Regulation, Neoplastic
  • Humans
  • Single-Cell Analysis
  • Uterine Neoplasms* / genetics
  • Uterine Neoplasms* / metabolism
  • Uterine Neoplasms* / pathology

Substances

  • PROM1 protein, human
  • AC133 Antigen
  • E2F1 Transcription Factor
  • E2F1 protein, human
  • Biomarkers, Tumor

Supplementary concepts

  • Adenosarcoma of the uterus