Overexpression of Basonuclin Zinc Finger Protein 2 in stromal cell is related to mesenchymal phenotype and immunosuppression of mucinous colorectal adenocarcinoma

Int Immunopharmacol. 2024 Dec 5;142(Pt B):113184. doi: 10.1016/j.intimp.2024.113184. Epub 2024 Sep 21.

Abstract

Background: Mucinous carcinoma (MC) is a distinct histologic subtype of colorectal cancer (CRC) that is less studied and associated with poor prognosis. This study aimed to identify MC-specific therapeutic targets and biomarkers to improve the prognosis of this aggressive disease.

Methods: CRC samples from The Cancer Genome Atlas (TCGA) were categorized into MC and non-MC (NMC) groups based on histologic type. A multi-scale embedded gene co-expression network analysis (MEGENA) was constructed to identify gene modules associated with the MC group. The potential functions of Basonuclin Zinc Finger Protein 2 (BNC2) were further analyzed using the Biomarker Exploration for Solid Tumors (BEST) database. In vivo and in vitro experiments were conducted to validate the predicted results.

Results: We identified the stromal component-related gene, BNC2, in the MC population. This gene is associated with a shorter progression-free interval (PFI) in CRC patients. BNC2 promotes FAP (encoding Fibroblast Activation Protein Alpha) transcription in cancer-associated fibroblasts (CAFs) and is involved in angiogenesis through two pathways. Additionally, BNC2 enhances tumor cell invasiveness in a CAF-dependent manner. Patients with high BNC2 expression benefited less from immunotherapy compared to those with low BNC2 expression.

Conclusions: Our study highlights the clinical importance of BNC2 in MC, and targeting BNC2 on stromal cells (fibroblasts and endothelial cells) may be an effective strategy for treating MC.

Keywords: Basonuclin zinc finger protein 2; Cancer-associated fibroblasts; Epithelial mesenchymal transition; Immune checkpoints; Mucinous adenocarcinoma; Tumor microenvironment.

MeSH terms

  • Adenocarcinoma, Mucinous* / genetics
  • Adenocarcinoma, Mucinous* / immunology
  • Adenocarcinoma, Mucinous* / metabolism
  • Adenocarcinoma, Mucinous* / pathology
  • Animals
  • Biomarkers, Tumor / genetics
  • Biomarkers, Tumor / metabolism
  • Cancer-Associated Fibroblasts / metabolism
  • Cell Line, Tumor
  • Colorectal Neoplasms* / genetics
  • Colorectal Neoplasms* / immunology
  • Colorectal Neoplasms* / metabolism
  • Colorectal Neoplasms* / pathology
  • Female
  • Gene Expression Regulation, Neoplastic
  • Humans
  • Immune Tolerance
  • Male
  • Mice
  • Mice, Nude
  • Stromal Cells / immunology
  • Stromal Cells / metabolism

Substances

  • Biomarkers, Tumor