Evolving structure-function relations during aortic maturation and aging revealed by multiphoton microscopy

Mech Ageing Dev. 2021 Jun:196:111471. doi: 10.1016/j.mad.2021.111471. Epub 2021 Mar 16.

Abstract

The evolving microstructure and mechanical properties that promote homeostasis in the aorta are fundamental to age-specific adaptations and disease progression. We combine ex vivo multiphoton microscopy and biaxial biomechanical phenotyping to quantify and correlate layer-specific microstructural parameters, for the primary extracellular matrix components (fibrillar collagen and elastic lamellae) and cells (endothelial, smooth muscle, and adventitial), with mechanical properties of the mouse aorta from weaning through natural aging up to one year. The aging endothelium was characterized by progressive reductions in cell density and altered cellular orientation. The media similarly showed a progressive decrease in smooth muscle cell density and alignment though with inter-lamellar widening from intermediate to older ages, suggesting cell hypertrophy, matrix accumulation, or both. Despite not changing in tissue thickness, the aging adventitia exhibited a marked thickening and straightening of collagen fiber bundles and reduction in cell density, suggestive of age-related remodeling not growth. Multiple microstructural changes correlated with age-related increases in circumferential and axial material stiffness, among other mechanical metrics. Because of the importance of aging as a risk factor for cardiovascular diseases, understanding the normal progression of structural and functional changes is essential when evaluating superimposed disease-related changes as a function of the age of onset.

Keywords: Biaxial mechanics; Homeostasis; Layer-specific microstructure; Mouse; Natural aging.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Aging / physiology*
  • Animals
  • Aorta* / cytology
  • Aorta* / growth & development
  • Aorta* / ultrastructure
  • Biomechanical Phenomena / physiology*
  • Cellular Senescence / physiology
  • Collagen / metabolism
  • Endothelial Cells* / pathology
  • Endothelial Cells* / physiology
  • Extracellular Matrix / physiology*
  • Fibroblasts / pathology
  • Fibroblasts / physiology
  • Image Processing, Computer-Assisted / methods
  • Mice
  • Microscopy, Fluorescence, Multiphoton / methods
  • Myocytes, Smooth Muscle* / pathology
  • Myocytes, Smooth Muscle* / physiology

Substances

  • Collagen