Glucocorticoid-induced phosphorylation by CDK9 modulates the coactivator functions of transcriptional cofactor GRIP1 in macrophages

Nat Commun. 2017 Nov 23;8(1):1739. doi: 10.1038/s41467-017-01569-2.

Abstract

The glucocorticoid (GC) receptor (GR) suppresses inflammation by activating anti-inflammatory and repressing pro-inflammatory genes. GR-interacting protein-1 (GRIP1) is a GR corepressor in macrophages, however, whether GRIP1 mediates GR-activated transcription, and what dictates its coactivator versus corepressor properties is unknown. Here we report that GRIP1 loss in macrophages attenuates glucocorticoid induction of several anti-inflammatory targets, and that GC treatment of quiescent macrophages globally directs GRIP1 toward GR binding sites dominated by palindromic GC response elements (GRE), suggesting a non-redundant GRIP1 function as a GR coactivator. Interestingly, GRIP1 is phosphorylated at an N-terminal serine cluster by cyclin-dependent kinase-9 (CDK9), which is recruited into GC-induced GR:GRIP1:CDK9 hetero-complexes, producing distinct GRE-specific GRIP1 phospho-isoforms. Phosphorylation potentiates GRIP1 coactivator but, remarkably, not its corepressor properties. Consistently, phospho-GRIP1 and CDK9 are not detected at GR transrepression sites near pro-inflammatory genes. Thus, GR restricts actions of its own coregulator via CDK9-mediated phosphorylation to a subset of anti-inflammatory genes.

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

  • Adaptor Proteins, Signal Transducing / deficiency
  • Adaptor Proteins, Signal Transducing / genetics
  • Adaptor Proteins, Signal Transducing / metabolism*
  • Animals
  • Binding Sites / genetics
  • Carrier Proteins / antagonists & inhibitors
  • Carrier Proteins / genetics
  • Carrier Proteins / metabolism*
  • Cell Line
  • Cells, Cultured
  • Cyclin-Dependent Kinase 9 / metabolism*
  • Dexamethasone / pharmacology
  • Gene Knockdown Techniques
  • Glucocorticoids / metabolism*
  • Glucocorticoids / pharmacology
  • Humans
  • Inflammation / genetics
  • Inflammation / metabolism
  • Macrophages / drug effects
  • Macrophages / metabolism*
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Models, Biological
  • Nerve Tissue Proteins / antagonists & inhibitors
  • Nerve Tissue Proteins / deficiency
  • Nerve Tissue Proteins / genetics
  • Nerve Tissue Proteins / metabolism*
  • Phosphorylation
  • Receptors, Glucocorticoid / metabolism
  • Response Elements
  • Transcriptional Activation

Substances

  • Adaptor Proteins, Signal Transducing
  • Carrier Proteins
  • GRIP1 protein, human
  • Glucocorticoids
  • Grip1 protein, mouse
  • Nerve Tissue Proteins
  • Receptors, Glucocorticoid
  • Dexamethasone
  • CDK9 protein, human
  • Cdk9 protein, mouse
  • Cyclin-Dependent Kinase 9