Somatic RIT1 delins in arteriovenous malformations hyperactivate RAS-MAPK signaling amenable to MEK inhibition

Angiogenesis. 2024 Nov;27(4):739-752. doi: 10.1007/s10456-024-09934-8. Epub 2024 Jul 5.

Abstract

Arteriovenous malformations (AVM) are benign vascular anomalies prone to pain, bleeding, and progressive growth. AVM are mainly caused by mosaic pathogenic variants of the RAS-MAPK pathway. However, a causative variant is not identified in all patients. Using ultra-deep sequencing, we identified novel somatic RIT1 delins variants in lesional tissue of three AVM patients. RIT1 encodes a RAS-like protein that can modulate RAS-MAPK signaling. We expressed RIT1 variants in HEK293T cells, which led to a strong increase in ERK1/2 phosphorylation. Endothelial-specific mosaic overexpression of RIT1 delins in zebrafish embryos induced AVM formation, highlighting their functional importance in vascular development. Both ERK1/2 hyperactivation in vitro and AVM formation in vivo could be suppressed by pharmacological MEK inhibition. Treatment with the MEK inhibitor trametinib led to a significant decrease in bleeding episodes and AVM size in one patient. Our findings implicate RIT1 in AVM formation and provide a rationale for clinical trials with targeted treatments.

Keywords: Arteriovenous malformation; RAS-MAPK pathway; RIT1; Trametinib; Vascular anomalies; Vascular malformation.

MeSH terms

  • Animals
  • Arteriovenous Malformations* / drug therapy
  • Arteriovenous Malformations* / genetics
  • Arteriovenous Malformations* / metabolism
  • Arteriovenous Malformations* / pathology
  • Female
  • HEK293 Cells
  • Humans
  • MAP Kinase Signaling System* / drug effects
  • Male
  • Protein Kinase Inhibitors / pharmacology
  • Pyridones / pharmacology
  • Pyrimidinones / pharmacology
  • Zebrafish* / embryology
  • ras Proteins* / genetics
  • ras Proteins* / metabolism

Substances

  • RIT1 protein, human
  • ras Proteins
  • trametinib
  • Protein Kinase Inhibitors
  • Pyrimidinones
  • Pyridones