Mrgprb2-dependent Mast Cell Activation Plays a Crucial Role in Acute Colitis

Cell Mol Gastroenterol Hepatol. 2024;18(5):101391. doi: 10.1016/j.jcmgh.2024.101391. Epub 2024 Aug 22.

Abstract

Background & aims: Mast cells (MCs) are typically found at mucosal surfaces, where their immunoglobulin E (IgE)-dependent activation plays a central role in allergic diseases. Over the past years, signaling through Mas-related G protein-coupled receptor b2 (Mrgprb2) in mice and MRGPRX2 in humans has gained a lot of interest as an alternative MC activation pathway with high therapeutic potential. The aim of this study was to explore the relevance of such IgE-independent, Mrgprb2-mediated signaling in colonic MCs in the healthy and acutely inflamed mouse colon.

Methods: Mrgprb2 expression and functionality was studied using a genetic labeling strategy combined with advanced microscopic imaging. Furthermore, Mrgprb2 knockout (Mrgprb2-/-) mice were used to determine the role of this pathway in a preclinical dextran sodium sulphate (DSS) colitis model.

Results: We found that Mrgprb2 acts as a novel MC degranulation pathway in a large subset of connective tissue MCs in the mouse distal colon. Acute DSS colitis induced a pronounced increase of Mrgprb2-expressing MCs, which were found in close association with Substance P-positive nerve fibers. Loss of Mrgprb2-mediated signaling impaired DSS-induced neutrophil influx and significantly impacted on acute colitis progression.

Conclusions: Our findings uncover a novel, IgE-independent MC degranulation pathway in the mouse colon that plays a central role in acute colitis pathophysiology, mainly by safeguarding acute colitis progression and severity in mice. This pseudo allergic, Mrgprb2-induced signaling is part of a hitherto unconsidered colonic neuro-immune pathway and might have significant potential for the further development of effective therapeutic treatment strategies for gastrointestinal disorders, such as ulcerative colitis.

Keywords: Colitis; IgE-independent; Mas-related G Protein Coupled Receptor; Mast Cell.

MeSH terms

  • Acute Disease
  • Animals
  • Cell Degranulation
  • Colitis* / chemically induced
  • Colitis* / immunology
  • Colitis* / metabolism
  • Colitis* / pathology
  • Colon / immunology
  • Colon / metabolism
  • Colon / pathology
  • Dextran Sulfate* / toxicity
  • Disease Models, Animal*
  • Immunoglobulin E / immunology
  • Immunoglobulin E / metabolism
  • Mast Cells* / immunology
  • Mast Cells* / metabolism
  • Mast Cells* / pathology
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout*
  • Receptors, G-Protein-Coupled* / genetics
  • Receptors, G-Protein-Coupled* / metabolism
  • Receptors, Neuropeptide / genetics
  • Receptors, Neuropeptide / metabolism
  • Signal Transduction

Substances

  • Receptors, G-Protein-Coupled
  • Dextran Sulfate
  • Mrgprb2 protein, mouse
  • Receptors, Neuropeptide
  • Immunoglobulin E