Glucocorticoid receptor inhibits Müller glial galectin-1 expression via DUSP1-dependent and -independent deactivation of AP-1 signalling

J Cell Mol Med. 2019 Oct;23(10):6785-6796. doi: 10.1111/jcmm.14559. Epub 2019 Jul 21.

Abstract

Galectin-1/LGALS1 is a hypoxia-induced angiogenic factor associated with diabetic retinopathy (DR). Recently, we elucidated a hypoxia-independent pathway to produce galectin-1 in Müller glial cells stimulated by interleukin (IL)-1β. Here we revealed glucocorticoid receptor (GR)-mediated inhibitory mechanisms for Müller glial galectin-1/LGALS1 expression. Activator protein (AP)-1 site in the LGALS1 enhancer region, to which activating transcription factor2, c-Fos and c-Jun bind, was shown to be essential for IL-1β-induced galectin-1/LGALS1 expression in Müller cells. Ligand (dexamethasone or triamcinolone acetonide)-activated GR induced dual specificity phosphatase (DUSP)1 expression via the glucocorticoid response element and attenuated IL-1β-induced galectin-1/LGALS1 expression by reducing phosphorylation of these AP-1 subunits following AKT and extracellular signal-regulated kinase (ERK)1/2 deactivation. Moreover, activated GR also caused DUSP1-independent down-regulation of IL-1β-induced LGALS1 expression via its binding to AP-1. Administration of glucocorticoids to mice attenuated diabetes-induced retinal galectin-1/Lgals1 expression together with AKT/AP-1 and ERK/AP-1 pathways. Supporting these in vitro and in vivo findings, immunofluorescence analyses showed co-localization of galectin-1 with GR and phosphorylated AP-1 in DUSP1-positive glial cells in fibrovascular tissues from patients with DR. Our present data demonstrated the inhibitory effects of glucocorticoids on glial galectin-1 expression via DUSP1-dependent and -independent deactivation of AP-1 signalling (transactivation and transrepression), highlighting therapeutic implications for DR.

Keywords: Müller glia; activator protein-1; diabetic retinopathy; dual specificity phosphatase 1; galectin-1; glucocorticoid receptor; interleukin-1β; transactivation; transrepression.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Line
  • Diabetes Mellitus / genetics
  • Down-Regulation / drug effects
  • Dual Specificity Phosphatase 1 / metabolism*
  • Ependymoglial Cells / metabolism*
  • Galectin 1 / metabolism*
  • Humans
  • Interleukin-1beta / pharmacology
  • MAP Kinase Signaling System
  • Mice, Inbred C57BL
  • Protein Binding / drug effects
  • Proto-Oncogene Proteins c-akt / metabolism
  • Receptors, Glucocorticoid / metabolism*
  • Retina / metabolism
  • Signal Transduction*
  • Transcription Factor AP-1 / metabolism*

Substances

  • Galectin 1
  • Interleukin-1beta
  • Receptors, Glucocorticoid
  • Transcription Factor AP-1
  • Proto-Oncogene Proteins c-akt
  • Dual Specificity Phosphatase 1