Cancer-associated fibroblasts regulate endothelial adhesion protein LPP to promote ovarian cancer chemoresistance

J Clin Invest. 2018 Feb 1;128(2):589-606. doi: 10.1172/JCI95200. Epub 2017 Dec 18.

Abstract

The molecular mechanism by which cancer-associated fibroblasts (CAFs) confer chemoresistance in ovarian cancer is poorly understood. The purpose of the present study was to evaluate the roles of CAFs in modulating tumor vasculature, chemoresistance, and disease progression. Here, we found that CAFs upregulated the lipoma-preferred partner (LPP) gene in microvascular endothelial cells (MECs) and that LPP expression levels in intratumoral MECs correlated with survival and chemoresistance in patients with ovarian cancer. Mechanistically, LPP increased focal adhesion and stress fiber formation to promote endothelial cell motility and permeability. siRNA-mediated LPP silencing in ovarian tumor-bearing mice improved paclitaxel delivery to cancer cells by decreasing intratumoral microvessel leakiness. Further studies showed that CAFs regulate endothelial LPP via a calcium-dependent signaling pathway involving microfibrillar-associated protein 5 (MFAP5), focal adhesion kinase (FAK), ERK, and LPP. Thus, our findings suggest that targeting endothelial LPP enhances the efficacy of chemotherapy in ovarian cancer. Our data highlight the importance of CAF-endothelial cell crosstalk signaling in cancer chemoresistance and demonstrate the improved efficacy of using LPP-targeting siRNA in combination with cytotoxic drugs.

Keywords: Cancer; Cell Biology; Oncology.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Animals
  • Cancer-Associated Fibroblasts / metabolism*
  • Cell Line, Tumor
  • Cell Movement
  • Cytoskeletal Proteins / metabolism*
  • Disease Progression
  • Drug Resistance, Neoplasm*
  • Endothelial Cells / metabolism
  • Female
  • Fibrosis
  • Focal Adhesions
  • Gene Expression Profiling
  • Gene Expression Regulation, Neoplastic
  • Gene Silencing
  • Humans
  • LIM Domain Proteins / metabolism*
  • Mice
  • Microcirculation
  • Neovascularization, Pathologic
  • Ovarian Neoplasms / drug therapy*
  • Ovarian Neoplasms / metabolism*
  • Permeability
  • RNA, Small Interfering / metabolism
  • Signal Transduction
  • Treatment Outcome
  • Up-Regulation

Substances

  • Cytoskeletal Proteins
  • LIM Domain Proteins
  • LPP protein, human
  • Lpp protein, mouse
  • RNA, Small Interfering