MicroRNA-124-3p inhibits collagen synthesis in atherosclerotic plaques by targeting prolyl 4-hydroxylase subunit alpha-1 (P4HA1) in vascular smooth muscle cells

Atherosclerosis. 2018 Oct:277:98-107. doi: 10.1016/j.atherosclerosis.2018.08.034. Epub 2018 Aug 26.

Abstract

Background and aims: Collagen synthesis in vascular smooth muscle cells (VSMCs) is very important in atherosclerosis, as it affects plaque stability. In this study, we aim to assess whether miR-124-3p is involved in the collagen synthesis process in VSMCs and the role it might play in atherosclerotic development.

Methods: We modulated the miR-124-3p expression in the aortic root plaques of high-fat-diet fed ApoE-/- mice by lentivirus injection. To determine plaque size and the content of plaque-stability-related cells or molecules, stainings, including hematoxylin and eosin, Oil red O, Sirius Red and immunohistochemical staining, were performed. Fluorescence in situ hybridization (FISH) was used to locate miR-124-3p in atherosclerotic plaques. Western blotting and RT-qPCR were carried out to determine the level of P4HA1 as well as type I and type III collagen protein and mRNA expression.

Results: Results showed that collagen and VSMC content of plaques was inversely correlated with miR-124-3p levels. By FISH, we identified that miR-124-3p was primarily expressed by VSMCs. We also found that protein levels of type I and type III collagen in aortas and atherosclerotic plaques were decreased by miR-124-3p. We modulated miR-124-3p level in vitro and found it could inhibit collagen expression in HASMCs. This might be caused by the downregulation of P4HA1. P4HA1 was predicted as miR-124-3p's direct target, which was verified with a dual luciferase reporter assay and RIP test.

Conclusions: The results presented here provide evidence that miR-124-3p inhibits VSMC collagen synthesis by directly targeting P4HA1, which might decrease atherosclerotic plaque stability.

Keywords: Atherosclerotic plaques; Collagen synthesis; P4HA1; Vascular smooth muscle cells; miR-124-3p.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Atherosclerosis / enzymology*
  • Atherosclerosis / genetics
  • Atherosclerosis / pathology
  • Cell Line
  • Collagen / biosynthesis*
  • Disease Models, Animal
  • Gene Expression Regulation, Enzymologic
  • Genetic Predisposition to Disease
  • Humans
  • Lipoproteins, LDL / metabolism
  • Male
  • Mice, Knockout, ApoE
  • MicroRNAs / genetics
  • MicroRNAs / metabolism*
  • Muscle, Smooth, Vascular / enzymology*
  • Muscle, Smooth, Vascular / pathology
  • Myocytes, Smooth Muscle / enzymology*
  • Myocytes, Smooth Muscle / pathology
  • Phenotype
  • Plaque, Atherosclerotic*
  • Procollagen-Proline Dioxygenase / genetics
  • Procollagen-Proline Dioxygenase / metabolism*
  • Rupture, Spontaneous
  • Signal Transduction

Substances

  • Lipoproteins, LDL
  • MIRN124 microRNA, human
  • MicroRNAs
  • Mirn124 microRNA, mouse
  • Collagen
  • P4HA1 protein, human
  • P4ha1 protein, mouse
  • Procollagen-Proline Dioxygenase