Limb reduction in an Esco2 cohesinopathy mouse model is mediated by p53-dependent apoptosis and vascular disruption

Nat Commun. 2024 Aug 21;15(1):7154. doi: 10.1038/s41467-024-51328-3.

Abstract

Roberts syndrome (RBS) is an autosomal recessive disorder with profound growth deficiency and limb reduction caused by ESCO2 loss-of-function variants. Here, we elucidate the pathogenesis of limb reduction in an Esco2fl/fl;Prrx1-CreTg/0 mouse model using bulk- and single-cell-RNA-seq and gene co-expression network analyses during embryogenesis. Our results reveal morphological and vascular defects culminating in hemorrhage of mutant limbs at E12.5. Underlying this abnormal developmental progression is a pre-apoptotic, mesenchymal cell population specific to mutant limb buds enriched for p53-related signaling beginning at E9.5. We then characterize these p53-related processes of cell cycle arrest, DNA damage, cell death, and the inflammatory leukotriene signaling pathway in vivo. In utero treatment with pifithrin-α, a p53 inhibitor, rescued the hemorrhage in mutant limbs. Lastly, significant enrichments were identified among genes associated with RBS, thalidomide embryopathy, and other genetic limb reduction disorders, suggesting a common vascular etiology among these conditions.

MeSH terms

  • Animals
  • Apoptosis* / genetics
  • Benzothiazoles / pharmacology
  • Cell Cycle Checkpoints / drug effects
  • Cell Cycle Checkpoints / genetics
  • Cell Cycle Proteins / genetics
  • Cell Cycle Proteins / metabolism
  • Chromosomal Proteins, Non-Histone* / genetics
  • Chromosomal Proteins, Non-Histone* / metabolism
  • Cohesins*
  • Craniofacial Abnormalities
  • DNA Damage
  • Disease Models, Animal*
  • Ectromelia / genetics
  • Ectromelia / metabolism
  • Ectromelia / pathology
  • Female
  • Hemorrhage / genetics
  • Hemorrhage / pathology
  • Homeodomain Proteins
  • Hypertelorism
  • Limb Buds / metabolism
  • Limb Deformities, Congenital* / genetics
  • Limb Deformities, Congenital* / metabolism
  • Limb Deformities, Congenital* / pathology
  • Male
  • Mice
  • Signal Transduction
  • Toluene / analogs & derivatives
  • Toluene / pharmacology
  • Tumor Suppressor Protein p53* / genetics
  • Tumor Suppressor Protein p53* / metabolism

Substances

  • Tumor Suppressor Protein p53
  • Cohesins
  • Chromosomal Proteins, Non-Histone
  • Trp53 protein, mouse
  • Cell Cycle Proteins
  • pifithrin
  • Toluene
  • Benzothiazoles
  • Prrx1 protein, mouse
  • Homeodomain Proteins

Supplementary concepts

  • Roberts Syndrome