miR-424/322 regulates vascular smooth muscle cell phenotype and neointimal formation in the rat

Cardiovasc Res. 2013 Jun 1;98(3):458-68. doi: 10.1093/cvr/cvt045. Epub 2013 Feb 26.

Abstract

Aims: Our aim was to identify new microRNAs (miRNAs) implicated in pathological vascular smooth muscle cells (VSMCs) proliferation and characterize their mechanism of action.

Methods and results: MicroRNAs microarray and qRT-PCR results lead us to focus on miR-424 or its rat ortholog miR-322 (miR-424/322). In vitro mir-424/322 level was decreased shortly after the induction of proliferation and increased in a time-dependent manner later on. In vivo its expression increased in the rat carotid artery from Day 4 up to Day 30 after injury. miR-424/322 overexpression in vitro inhibited proliferation and migration without affecting apoptosis and prevented VSMC dedifferentiation. Furthermore, miR-424/322 overexpression resulted in decreased expression of its predicted targets: cyclin D1 and Ca(2+)-regulating proteins calumenin and stromal-interacting molecule 1 (STIM1). Using reporter luciferase assays, we confirmed that cyclin D1 and calumenin mRNAs were direct targets of miR-322, whereas miR-322 effect on STIM1 was indirect. Nevertheless, consistent with the decreased STIM1 level, the store-operated Ca(2+) entry was reduced. We hypothesized that miR-424/322 could be a negative regulator of proliferation overridden in pathological situations. Thus, we overexpressed miR-424/322 in injured rat carotid arteries using an adenovirus, and demonstrated a protective effect against restenosis.

Conclusion: Our results demonstrate that miR-424/322 is up-regulated after vascular injury. This is likely an adaptive response to counteract proliferation, although this mechanism is overwhelmed in pathological situations such as injury-induced restenosis.

Keywords: Calcium; MicroRNA; Proliferation; Restenosis; Vascular smooth muscle cells.

Publication types

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

MeSH terms

  • Animals
  • Apoptosis
  • Calcium / metabolism
  • Calcium-Binding Proteins / metabolism
  • Carotid Artery Injuries / genetics
  • Carotid Artery Injuries / metabolism*
  • Carotid Artery Injuries / pathology
  • Carotid Artery Injuries / prevention & control
  • Carotid Artery, External / metabolism
  • Carotid Artery, External / pathology
  • Cell Dedifferentiation
  • Cell Movement
  • Cell Proliferation
  • Cells, Cultured
  • Cyclin D1 / metabolism
  • Disease Models, Animal
  • Humans
  • Male
  • Membrane Glycoproteins / metabolism
  • MicroRNAs / metabolism*
  • Muscle, Smooth, Vascular / metabolism*
  • Muscle, Smooth, Vascular / pathology
  • Myocytes, Smooth Muscle / metabolism*
  • Myocytes, Smooth Muscle / pathology
  • Neointima*
  • Phenotype
  • Rats
  • Rats, Wistar
  • Signal Transduction
  • Stromal Interaction Molecule 1
  • Time Factors
  • Transfection
  • Up-Regulation

Substances

  • Calcium-Binding Proteins
  • Calu protein, rat
  • Ccnd1 protein, rat
  • MIRN322 microRNA, rat
  • MIRN424 microrna, human
  • Membrane Glycoproteins
  • MicroRNAs
  • Stim1 protein, rat
  • Stromal Interaction Molecule 1
  • Cyclin D1
  • Calcium