Gene inactivation of lysyl oxidase in smooth muscle cells reduces atherosclerosis burden and plaque calcification in hyperlipidemic mice

Atherosclerosis. 2024 Oct:397:118582. doi: 10.1016/j.atherosclerosis.2024.118582. Epub 2024 Aug 31.

Abstract

Background and aims: Lysyl oxidase (LOX) catalyzes the crosslinking of collagen and elastin to maintain tensile strength and structural integrity of the vasculature. Excessive LOX activity increases vascular stiffness and the severity of occlusive diseases. Herein, we investigated the mechanisms by which LOX controls atherogenesis and osteogenic differentiation of vascular smooth muscle cells (SMC) in hyperlipidemic mice.

Methods: Gene inactivation of Lox in SMC was achieved in conditional knockout mice after tamoxifen injections. Atherosclerosis burden and vascular calcification were assessed in hyperlipidemic conditional [Loxf/fMyh11-CreERT2ApoE-/-] and sibling control mice [Loxwt/wtMyh11-CreERT2ApoE-/-]. Mechanistic studies were performed with primary aortic SMC from Lox mutant and wild type mice.

Results: Inactivation of Lox in SMCs decreased > 70 % its RNA expression and protein level in the aortic wall and significantly reduced LOX activity without compromising vascular structure and function. Moreover, LOX deficiency protected mice against atherosclerotic burden (13 ± 2 versus 23 ± 1 %, p < 0.01) and plaque calcification (5 ± 0.4 versus 11.8 ± 3 %, p < 0.05) compared to sibling controls. Interestingly, gene inactivation of Lox in SMCs preserved the contractile phenotype of vascular SMC under hyperlipidemic conditions as demonstrated by single-cell RNA sequencing and immunofluorescence. Mechanistically, the absence of LOX in SMC prevented excessive collagen crosslinking and the subsequent activation of the pro-osteogenic FAK/β-catenin signaling axis.

Conclusions: Lox inactivation in SMC protects mice against atherosclerosis and plaque calcification by reducing SMC modulation and FAK/β-catenin signaling.

Keywords: Atherosclerosis; Lysyl oxidase; Single cell RNA sequencing; Smooth muscle cell; Vascular calcification.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Animals
  • Aorta / enzymology
  • Aorta / metabolism
  • Aorta / pathology
  • Aortic Diseases / enzymology
  • Aortic Diseases / genetics
  • Aortic Diseases / metabolism
  • Aortic Diseases / pathology
  • Aortic Diseases / prevention & control
  • Atherosclerosis* / enzymology
  • Atherosclerosis* / genetics
  • Atherosclerosis* / metabolism
  • Atherosclerosis* / pathology
  • Cells, Cultured
  • Disease Models, Animal*
  • Extracellular Matrix Proteins
  • Hyperlipidemias* / complications
  • Hyperlipidemias* / enzymology
  • Hyperlipidemias* / genetics
  • Hyperlipidemias* / metabolism
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout*
  • Muscle, Smooth, Vascular* / enzymology
  • Muscle, Smooth, Vascular* / metabolism
  • Muscle, Smooth, Vascular* / pathology
  • Myocytes, Smooth Muscle* / enzymology
  • Myocytes, Smooth Muscle* / metabolism
  • Myocytes, Smooth Muscle* / pathology
  • Osteogenesis
  • Plaque, Atherosclerotic*
  • Protein-Lysine 6-Oxidase* / genetics
  • Protein-Lysine 6-Oxidase* / metabolism
  • Signal Transduction
  • Vascular Calcification* / enzymology
  • Vascular Calcification* / genetics
  • Vascular Calcification* / metabolism
  • Vascular Calcification* / pathology
  • Vascular Calcification* / prevention & control
  • beta Catenin / metabolism

Substances

  • Protein-Lysine 6-Oxidase
  • Lox protein, mouse
  • beta Catenin
  • Extracellular Matrix Proteins