The orphan receptor GPRC5B activates pro-inflammatory signaling in the vascular wall via Fyn and NFκB

Biochem Biophys Res Commun. 2022 Feb 12:592:60-66. doi: 10.1016/j.bbrc.2022.01.009. Epub 2022 Jan 7.

Abstract

Background and aims: Atherosclerosis is driven by an inflammatory process of the vascular wall. The novel orphan G-protein coupled receptor 5B of family C (GPRC5B) is involved in drosophila sugar and lipid metabolism as well as mice adipose tissue inflammation. Here, we investigated the role of GPRC5B in the pro-atherogenic mechanisms of hyperglycemia and vascular inflammation.

Methods: Immortalized and primary endothelial cells (ECs) and vascular smooth muscle cells (VSMCs) were used for stimulation with high glucose or different cytokines. Adenoviral- or plasmid-driven GPRC5B overexpression and siRNA-mediated knockdown were performed in these cells to analyze functional and mechanistic pathways of GPRC5B.

Results: In ECs and VSMCs, stimulation with high glucose, TNFα or LPS induced a significant upregulation of endogenous GPRC5B mRNA and protein levels. GPRC5B overexpression and knockdown increased and attenuated, respectively, the expression of the pro-inflammatory cytokines TNFα, IL-1β, IL-6 as well as the pro-atherogenic vascular adhesion molecules ICAM-1 and VCAM-1. Furthermore, the expression and activity of the metalloproteinase MMP-9, a component of atherosclerotic plaque stabilization, were significantly enhanced by GPRC5B overexpression. Mechanistically, GPRC5B increased the phosphorylation of ERK1/2 and activated NFκB through a direct interaction with the tyrosine kinase Fyn.

Conclusions: Our findings demonstrate that GPRC5B is upregulated in response to high glucose and pro-inflammatory signaling. GPRC5B functionally modulates the inflammatory activity in cells of the vascular wall, suggesting a pro-atherogenic GPRC5B-dependent positive feedback loop via Fyn and NFκB. Thus, GPRC5B warrants further attention as a novel pharmacological target for the treatment of vascular inflammation and possibly atherogenesis.

Keywords: Atherosclerosis; GPCR; GPRC5B; Hyperglycemia; Vascular inflammation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Atherosclerosis / metabolism
  • Atherosclerosis / pathology
  • Blood Vessels / drug effects
  • Blood Vessels / metabolism*
  • Blood Vessels / pathology*
  • Cell Adhesion Molecules / metabolism
  • Cytokines / adverse effects
  • Enzyme Activation / drug effects
  • Glucose / toxicity
  • Human Umbilical Vein Endothelial Cells / drug effects
  • Human Umbilical Vein Endothelial Cells / metabolism
  • Humans
  • Hyperglycemia / pathology
  • Inflammation / metabolism*
  • Inflammation / pathology
  • Matrix Metalloproteinases / metabolism
  • Mice
  • NF-kappa B / metabolism*
  • Proto-Oncogene Proteins c-fyn / metabolism*
  • Receptors, G-Protein-Coupled / metabolism*
  • Signal Transduction* / drug effects

Substances

  • Cell Adhesion Molecules
  • Cytokines
  • GPRC5B receptor, mouse
  • NF-kappa B
  • Receptors, G-Protein-Coupled
  • Proto-Oncogene Proteins c-fyn
  • Matrix Metalloproteinases
  • Glucose