AREG Upregulation in Cancer Cells via Direct Interaction with Cancer-Associated Fibroblasts Promotes Esophageal Squamous Cell Carcinoma Progression Through EGFR-Erk/p38 MAPK Signaling

Cells. 2024 Oct 19;13(20):1733. doi: 10.3390/cells13201733.

Abstract

Cancer-associated fibroblasts (CAFs) are a key component of the tumor microenvironment and significantly contribute to the progression of various cancers, including esophageal squamous cell carcinoma (ESCC). Our previous study established a direct co-culture system of human bone marrow-derived mesenchymal stem cells (progenitors of CAFs) and ESCC cell lines, which facilitates the generation of CAF-like cells and enhances malignancy in ESCC cells. In this study, we further elucidated the mechanism by which CAFs promote ESCC progression using cDNA microarray analysis of monocultured ESCC cells and those co-cultured with CAFs. We observed an increase in the expression and secretion of amphiregulin (AREG) and the expression and phosphorylation of its receptor EGFR in co-cultured ESCC cells. Moreover, AREG treatment of ESCC cells enhanced their survival and migration via the EGFR-Erk/p38 MAPK signaling pathway. Immunohistochemical analysis of human ESCC tissues showed a positive correlation between the intensity of AREG expression at the tumor-invasive front and the expression level of the CAF marker FAP. Bioinformatics analysis confirmed significant upregulation of AREG in ESCC compared with normal tissues. These findings suggest that AREG plays a crucial role in CAF-mediated ESCC progression and could be a novel therapeutic target for ESCC.

Keywords: amphiregulin (AREG); cancer-associated fibroblasts (CAFs); direct co-culture; epidermal growth factor receptor (EGFR); esophageal squamous cell carcinoma (ESCC).

MeSH terms

  • Amphiregulin* / genetics
  • Amphiregulin* / metabolism
  • Cancer-Associated Fibroblasts* / metabolism
  • Cancer-Associated Fibroblasts* / pathology
  • Cell Line, Tumor
  • Cell Movement / genetics
  • Disease Progression*
  • ErbB Receptors* / metabolism
  • Esophageal Neoplasms* / genetics
  • Esophageal Neoplasms* / metabolism
  • Esophageal Neoplasms* / pathology
  • Esophageal Squamous Cell Carcinoma* / genetics
  • Esophageal Squamous Cell Carcinoma* / metabolism
  • Esophageal Squamous Cell Carcinoma* / pathology
  • Female
  • Gene Expression Regulation, Neoplastic
  • Humans
  • MAP Kinase Signaling System*
  • Male
  • Middle Aged
  • Signal Transduction
  • Up-Regulation* / genetics
  • p38 Mitogen-Activated Protein Kinases* / metabolism

Substances

  • Amphiregulin
  • ErbB Receptors
  • AREG protein, human
  • p38 Mitogen-Activated Protein Kinases
  • EGFR protein, human