Pro-tumoral behavior of omental adipocyte-derived fibroblasts in tumor microenvironment at the metastatic site of ovarian cancer

Int J Cancer. 2021 Dec 1;149(11):1961-1972. doi: 10.1002/ijc.33770. Epub 2021 Sep 16.

Abstract

Adipocyte-rich omentum offers "good soil" for disseminating ovarian cancer (OvCa), contributing to therapeutic difficulty. However, little is understood about the association between adipocytes and tumor growth at peritoneal dissemination site. Herein, we report the induction of adipocyte dedifferentiation by OvCa cells and pro-tumorigenic effects of resulted adipocyte-derived fibroblasts. We confirmed that malignant ascites promoted the dedifferentiation of the primary human adipocytes obtained from surgical omental specimen into omental adipocyte-derived fibroblast (O-ADF) that possess both mesenchymal stem cell and myofibroblast-like features. This promotion of dedifferentiation by malignant ascites was blocked by addition of Wnt signaling inhibitor. The effects of dedifferentiated adipocytes in proliferation and migration of OvCa cells were analyzed with in vitro coculturing experimental models and in vivo mice model, and we demonstrated that OvCa cell lines showed enhanced proliferative characteristics, as well as increased migratory abilities upon coculturing with O-ADF. Additionally, exogenous transforming growth factor-β1 augmented desmoplastic morphological change of O-ADF, leading to higher proliferative ability. Our results suggest that OvCa cells promote dedifferentiation of peritoneal adipocytes by activating Wnt/β-catenin signaling, and generated O-ADFs exhibit pro-tumoral hallmarks.

Keywords: adipocyte; dedifferentiation; ovarian cancer; tumor microenvironment.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 3T3-L1 Cells
  • Actins / metabolism
  • Adipocytes / drug effects
  • Adipocytes / metabolism
  • Adipocytes / pathology*
  • Animals
  • Ascites / metabolism
  • Cancer-Associated Fibroblasts / metabolism
  • Cancer-Associated Fibroblasts / pathology*
  • Cell Dedifferentiation / drug effects
  • Cell Movement
  • Cell Proliferation
  • Female
  • Humans
  • Imides / pharmacology
  • Mesenchymal Stem Cells / metabolism
  • Mesenchymal Stem Cells / pathology
  • Mice
  • Myofibroblasts / metabolism
  • Myofibroblasts / pathology
  • Omentum / metabolism
  • Omentum / pathology*
  • Ovarian Neoplasms / metabolism
  • Ovarian Neoplasms / pathology*
  • Peritoneal Neoplasms / metabolism
  • Peritoneal Neoplasms / secondary
  • Quinolines / pharmacology
  • Tumor Microenvironment*
  • Wnt Signaling Pathway / drug effects
  • Wnt3A Protein / metabolism

Substances

  • ACTA2 protein, human
  • Actins
  • IWR-1 compound
  • Imides
  • Quinolines
  • WNT3A protein, human
  • Wnt3A Protein