Angiopoietin-Like Protein 2 Expression in Tumor Cells Supports Tumor-Associated Macrophage-Induced Tumor Progression in Esophageal Cancer

Ann Surg Oncol. 2024 Nov;31(12):7693-7704. doi: 10.1245/s10434-024-15557-6. Epub 2024 Jul 9.

Abstract

Background: Tumor-associated macrophages (TAM), a major component of the tumor microenvironment, play key roles in tumor formation and progression; however, mechanisms underlying TAM-induced tumor progression are complex and not well known. We previously reported that tumor cell-derived angiopoietin-like protein 2 (ANGPTL2) functions as a tumor promoter in some cancer contexts.

Methods: We examined ANGPTL2 expression in paraffin-embedded tumor samples from resected specimens of 221 patients with esophageal cancer. Patients were subdivided into four groups based on immunohistochemistry scores described above: ANGPTL2-low/TAM-low, ANGPTL2-low/TAM-high, ANGPTL2-high/TAM-low, and ANGPTL2-high/TAM-high groups. Gene expression datasets of esophageal cancer cell lines were obtained from the cancer cell line encyclopedia public database.

Results: In this study, we demonstrate that TAM infiltration is associated with poor prognosis in patients with esophageal cancer whose tumor cells show relatively higher ANGPTL2 expression levels; however, TAM infiltration did not affect prognosis in patients with ANGPTL2-low-expressing esophageal cancer, suggesting that ANGPTL2 expression in esophageal cancer cells is required for TAM-induced tumor progression. Our analysis of public datasets indicates a potential positive correlation of ANGPTL2 expression levels with that of transforming growth factor (TGF)-β, a TAM-activating factor, in esophageal cancer cell lines.

Conclusion: We conclude that ANGPTL2 signaling in tumor cells supports TAM-induced tumor progression and contributes to poor prognosis in patients with esophageal cancer. These findings overall provide novel insight into pro-tumor ANGPTL2 functions and illustrate the essential role of cancer cell/TAM crosstalk in cancer progression.

Keywords: Angiopoietin-like protein 2; Esophageal cancer; Immunity; Tumor microenvironment; Tumor-associated macrophages.

MeSH terms

  • Aged
  • Angiopoietin-Like Protein 2*
  • Angiopoietin-like Proteins* / genetics
  • Angiopoietin-like Proteins* / metabolism
  • Biomarkers, Tumor* / genetics
  • Biomarkers, Tumor* / metabolism
  • Cell Proliferation
  • Disease Progression*
  • Esophageal Neoplasms* / genetics
  • Esophageal Neoplasms* / metabolism
  • Esophageal Neoplasms* / pathology
  • Esophageal Neoplasms* / surgery
  • Female
  • Follow-Up Studies
  • Gene Expression Regulation, Neoplastic
  • Humans
  • Male
  • Middle Aged
  • Prognosis
  • Survival Rate
  • Tumor Cells, Cultured
  • Tumor Microenvironment*
  • Tumor-Associated Macrophages* / metabolism
  • Tumor-Associated Macrophages* / pathology

Substances

  • Angiopoietin-Like Protein 2
  • ANGPTL2 protein, human
  • Angiopoietin-like Proteins
  • Biomarkers, Tumor