Gasdermin D Deficiency in Vascular Smooth Muscle Cells Ameliorates Abdominal Aortic Aneurysm Through Reducing Putrescine Synthesis

Adv Sci (Weinh). 2023 Feb;10(5):e2204038. doi: 10.1002/advs.202204038. Epub 2022 Dec 25.

Abstract

Abdominal aortic aneurysm (AAA) is a common vascular disease associated with significant phenotypic alterations in vascular smooth muscle cells (VSMCs). Gasdermin D (GSDMD) is a pore-forming effector of pyroptosis. In this study, the role of VSMC-specific GSDMD in the phenotypic alteration of VSMCs and AAA formation is determined. Single-cell transcriptome analyses reveal Gsdmd upregulation in aortic VSMCs in angiotensin (Ang) II-induced AAA. VSMC-specific Gsdmd deletion ameliorates Ang II-induced AAA in apolipoprotein E (ApoE)-/- mice. Using untargeted metabolomic analysis, it is found that putrescine is significantly reduced in the plasma and aortic tissues of VSMC-specific GSDMD deficient mice. High putrescine levels trigger a pro-inflammatory phenotype in VSMCs and increase susceptibility to Ang II-induced AAA formation in mice. In a population-based study, a high level of putrescine in plasma is associated with the risk of AAA (p < 2.2 × 10-16 ), consistent with the animal data. Mechanistically, GSDMD enhances endoplasmic reticulum stress-C/EBP homologous protein (CHOP) signaling, which in turn promotes the expression of ornithine decarboxylase 1 (ODC1), the enzyme responsible for increased putrescine levels. Treatment with the ODC1 inhibitor, difluoromethylornithine, reduces AAA formation in Ang II-infused ApoE-/- mice. The findings suggest that putrescine is a potential biomarker and target for AAA treatment.

Keywords: abdominal aortic aneurysm; gasdermin D; putrescine; smooth muscle cells.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Aortic Aneurysm, Abdominal* / chemically induced
  • Apolipoproteins E / genetics
  • Apolipoproteins E / metabolism
  • Gasdermins* / genetics
  • Gasdermins* / metabolism
  • Mice
  • Muscle, Smooth, Vascular* / metabolism
  • Ornithine Decarboxylase / metabolism
  • Putrescine* / adverse effects
  • Putrescine* / metabolism
  • Single-Cell Analysis

Substances

  • Apolipoproteins E
  • Gasdermins
  • Gsdmd protein, mouse
  • Ornithine Decarboxylase
  • Putrescine