Rh-relaxin-2 attenuates degranulation of mast cells by inhibiting NF-κB through PI3K-AKT/TNFAIP3 pathway in an experimental germinal matrix hemorrhage rat model

J Neuroinflammation. 2020 Aug 28;17(1):250. doi: 10.1186/s12974-020-01926-x.

Abstract

Background: Mast cells play an important role in early immune reactions in the brain by degranulation and the consequent inflammatory response. Our aim of the study is to investigate the effects of rh-relaxin-2 on mast cells and the underlying mechanisms in a germinal matrix hemorrhage (GMH) rat model.

Methods: One hundred seventy-three P7 rat pups were subjected to GMH by an intraparenchymal injection of bacterial collagenase. Clodronate liposome was administered through intracerebroventricular (i.c.v.) injections 24 h prior to GMH to inhibit microglia. Rh-relaxin-2 was administered intraperitoneally at 1 h and 13 h after GMH. Small interfering RNA of RXFP1 and PI3K inhibitor LY294002 were given by i.c.v. injection. Post-GMH evaluation included neurobehavioral function, Western blot analysis, immunofluorescence, Nissl staining, and toluidine blue staining.

Results: Our results demonstrated that endogenous relaxin-2 was downregulated and that RXFP1 level peaked on the first day after GMH. Administration of rh-relaxin-2 improved neurological functions, attenuated degranulation of mast cells and neuroinflammation, and ameliorated post-hemorrhagic hydrocephalus (PHH) after GMH. These effects were associated with RXFP1 activation, increased expression of PI3K, phosphorylated AKT and TNFAIP3, and decreased levels of phosphorylated NF-κB, tryptase, chymase, IL-6, and TNF-α. However, knockdown of RXFP1 and PI3K inhibition abolished the protective effects of rh-relaxin-2.

Conclusions: Our findings showed that rh-relaxin-2 attenuated degranulation of mast cells and neuroinflammation, improved neurological outcomes, and ameliorated hydrocephalus after GMH through RXFP1/PI3K-AKT/TNFAIP3/NF-κB signaling pathway.

Keywords: Degranulation; Germinal matrix hemorrhage; Hydrocephalus; Inflammation; Mast cells; Relaxin-2.

MeSH terms

  • Animals
  • Disease Models, Animal
  • Intracranial Hemorrhages / metabolism*
  • Mast Cells / drug effects*
  • Mast Cells / metabolism
  • NF-kappa B / metabolism*
  • Phosphatidylinositol 3-Kinases / metabolism
  • Proto-Oncogene Proteins c-akt / metabolism
  • Rats
  • Rats, Sprague-Dawley
  • Receptors, G-Protein-Coupled / metabolism
  • Receptors, Peptide / metabolism
  • Recombinant Proteins / pharmacology*
  • Relaxin / pharmacology*
  • Signal Transduction / drug effects*
  • Signal Transduction / physiology
  • Tumor Necrosis Factor alpha-Induced Protein 3 / metabolism

Substances

  • NF-kappa B
  • RLN2 protein, human
  • Receptors, G-Protein-Coupled
  • Receptors, Peptide
  • Recombinant Proteins
  • Rxfp1 protein, rat
  • Relaxin
  • Proto-Oncogene Proteins c-akt
  • TNFAIP3 protein, rat
  • Tumor Necrosis Factor alpha-Induced Protein 3