Deciphering the role of FUS::DDIT3 expression and tumor microenvironment in myxoid liposarcoma development

J Transl Med. 2024 Apr 26;22(1):389. doi: 10.1186/s12967-024-05211-w.

Abstract

Background: Myxoid liposarcoma (MLS) displays a distinctive tumor microenvironment and is characterized by the FUS::DDIT3 fusion oncogene, however, the precise functional contributions of these two elements remain enigmatic in tumor development.

Methods: To study the cell-free microenvironment in MLS, we developed an experimental model system based on decellularized patient-derived xenograft tumors. We characterized the cell-free scaffold using mass spectrometry. Subsequently, scaffolds were repopulated using sarcoma cells with or without FUS::DDIT3 expression that were analyzed with histology and RNA sequencing.

Results: Characterization of cell-free MLS scaffolds revealed intact structure and a large variation of protein types remaining after decellularization. We demonstrated an optimal culture time of 3 weeks and showed that FUS::DDIT3 expression decreased cell proliferation and scaffold invasiveness. The cell-free MLS microenvironment and FUS::DDIT3 expression both induced biological processes related to cell-to-cell and cell-to-extracellular matrix interactions, as well as chromatin remodeling, immune response, and metabolism. Data indicated that FUS::DDIT3 expression more than the microenvironment determined the pre-adipocytic phenotype that is typical for MLS.

Conclusions: Our experimental approach opens new means to study the tumor microenvironment in detail and our findings suggest that FUS::DDIT3-expressing tumor cells can create their own extracellular niche.

Keywords: Extracellular matrix; FET fusion oncogenes; FUS::DDIT3; Microenvironment; Myxoid liposarcoma; Scaffold.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Line, Tumor
  • Cell Proliferation
  • Cell-Free System
  • Extracellular Matrix / metabolism
  • Gene Expression Regulation, Neoplastic
  • Humans
  • Liposarcoma, Myxoid* / genetics
  • Liposarcoma, Myxoid* / metabolism
  • Liposarcoma, Myxoid* / pathology
  • Mice
  • Oncogene Proteins, Fusion* / genetics
  • Oncogene Proteins, Fusion* / metabolism
  • RNA-Binding Protein FUS* / genetics
  • RNA-Binding Protein FUS* / metabolism
  • Tissue Scaffolds / chemistry
  • Tumor Microenvironment*

Substances

  • RNA-Binding Protein FUS
  • Oncogene Proteins, Fusion
  • FUS-DDIT3 fusion protein, human
  • FUS protein, human