Cellular Microenvironment Stiffness Regulates Eicosanoid Production and Signaling Pathways

Am J Respir Cell Mol Biol. 2020 Dec;63(6):819-830. doi: 10.1165/rcmb.2020-0227OC.

Abstract

Pathological changes in the biomechanical environment are implicated in the progression of idiopathic pulmonary fibrosis (IPF). Stiffened matrix augments fibroblast proliferation and differentiation and activates TGF-β1 (transforming growth factor-β1). Stiffened matrix impairs the synthesis of the antifibrogenic lipid mediator prostaglandin E2 (PGE2) and reduces the expression of the rate-limiting prostanoid biosynthetic enzyme cyclooxygenase-2 (COX-2). We now show that prostaglandin E synthase (PTGES), the final enzyme in the PGE2 biosynthetic pathway, is expressed at lower levels in the lungs of patients with IPF. We also show substantial induction of COX-2, PTGES, prostaglandin E receptor 4 (EP4), and cytosolic phospholipase A2 (cPLA2) expression in human lung fibroblasts cultured in soft collagen hydrogels or in spheroids compared with conventional culture on stiff plastic culture plates. Induction of COX-2, cPLA2, and PTGES expression in spheroid cultures was moderately inhibited by the p38 mitogen-activated protein kinase inhibitor SB203580. The induction of prostanoid biosynthetic enzyme expression was accompanied by an increase in PGE2 levels only in non-IPF-derived fibroblast spheroids. Our study reveals an extensive dysregulation of prostanoid biosynthesis and signaling pathways in IPF-derived fibroblasts, which are only partially abrogated by culture in soft microenvironments.

Keywords: IPF; PGE2; PTGES; cPLA2; stiffness.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cellular Microenvironment / drug effects*
  • Cyclooxygenase 2 / drug effects
  • Cyclooxygenase 2 / metabolism
  • Dinoprostone / metabolism
  • Fibroblasts / drug effects*
  • Fibroblasts / metabolism
  • Humans
  • Idiopathic Pulmonary Fibrosis / pathology
  • Imidazoles / pharmacology*
  • Lung / drug effects
  • Lung / pathology
  • Prostaglandin-E Synthases / metabolism
  • Pyridines / pharmacology*
  • Signal Transduction / drug effects*

Substances

  • Imidazoles
  • Pyridines
  • Cyclooxygenase 2
  • Prostaglandin-E Synthases
  • Dinoprostone
  • SB 203580