Structural dysregulation of the pulmonary autograft was associated with a greater density of p16INK4A-vascular smooth muscle cells

Cardiovasc Pathol. 2023 Mar-Apr:63:107512. doi: 10.1016/j.carpath.2022.107512. Epub 2022 Dec 15.

Abstract

The present study tested the hypothesis that a senescent phenotype of vascular smooth muscle cells (VSMCs) may represent the seminal event linked to maladaptive pulmonary autograft remodeling of a small number of patients that underwent the Ross procedure. The diameter of the pulmonary autograft (47±4 mm) of three male patients was significantly greater compared to the pulmonary artery (26±1 mm) excised from bicuspid aortic valve (BAV) patients. The pulmonary autograft was associated with a neointimal region and the adjacent medial region was significantly thinner compared to the pulmonary artery of BAV patients. Structural dysregulation was evident as elastin content of the medial region was significantly reduced in the pulmonary autograft compared to the pulmonary artery of BAV patients. By contrast, collagen content of the medial region of the pulmonary autograft and the pulmonary artery of BAV patients was not significantly different. Reduced medial elastin content of the pulmonary autograft was associated with increased protein levels of matrix metalloproteinase-9. The latter phenotype was not attributed to a robust inflammatory response as the percentage of Mac-2(+)-infiltrating monocytes/macrophages was similar between groups. A senescent phenotype was identified as protein levels of the cell cycle inhibitor p27kip1 were upregulated and the density of p16INK4A/non-muscle myosin IIB(+)-VSMCs was significantly greater in the pulmonary autograft compared to the pulmonary artery of BAV patients. Thus, senescent VSMCs may represent the predominant cellular source of increased matrix metalloproteinase-9 protein expression translating to maladaptive pulmonary autograft remodeling characterized by elastin degradation, medial thinning and neointimal formation.

Keywords: Aneurysm; Cell cycle inhibitors; Matrix metalloproteinases; Neointima; Pulmonary autograft; Ross procedure; Vascular smooth muscle cells.

MeSH terms

  • Aortic Valve / pathology
  • Autografts / metabolism
  • Bicuspid Aortic Valve Disease* / metabolism
  • Bicuspid Aortic Valve Disease* / pathology
  • Cyclin-Dependent Kinase Inhibitor p16 / metabolism
  • Elastin* / metabolism
  • Humans
  • Male
  • Matrix Metalloproteinase 9 / metabolism
  • Muscle, Smooth, Vascular / pathology
  • Transplantation, Autologous

Substances

  • Elastin
  • Cyclin-Dependent Kinase Inhibitor p16
  • Matrix Metalloproteinase 9