LincRNA-p21 regulates neointima formation, vascular smooth muscle cell proliferation, apoptosis, and atherosclerosis by enhancing p53 activity

Circulation. 2014 Oct 21;130(17):1452-1465. doi: 10.1161/CIRCULATIONAHA.114.011675. Epub 2014 Aug 25.

Abstract

Background: Long noncoding RNAs (lncRNAs) have recently been implicated in many biological processes and diseases. Atherosclerosis is a major risk factor for cardiovascular disease. However, the functional role of lncRNAs in atherosclerosis is largely unknown.

Methods and results: We identified lincRNA-p21 as a key regulator of cell proliferation and apoptosis during atherosclerosis. The expression of lincRNA-p21 was dramatically downregulated in atherosclerotic plaques of ApoE(-/-) mice, an animal model for atherosclerosis. Through loss- and gain-of-function approaches, we showed that lincRNA-p21 represses cell proliferation and induces apoptosis in vascular smooth muscle cells and mouse mononuclear macrophage cells in vitro. Moreover, we found that inhibition of lincRNA-p21 results in neointimal hyperplasia in vivo in a carotid artery injury model. Genome-wide analysis revealed that lincRNA-p21 inhibition dysregulated many p53 targets. Furthermore, lincRNA-p21, a transcriptional target of p53, feeds back to enhance p53 transcriptional activity, at least in part, via binding to mouse double minute 2 (MDM2), an E3 ubiquitin-protein ligase. The association of lincRNA-p21 and MDM2 releases MDM2 repression of p53, enabling p53 to interact with p300 and to bind to the promoters/enhancers of its target genes. Finally, we show that lincRNA-p21 expression is decreased in patients with coronary artery disease.

Conclusions: Our studies identify lincRNA-p21 as a novel regulator of cell proliferation and apoptosis and suggest that this lncRNA could serve as a therapeutic target to treat atherosclerosis and related cardiovascular disorders.

Keywords: MDM2 protein; RNA, long noncoding; apoptosis; atherosclerosis; cell proliferation; tumor suppressor protein p53.

Publication types

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

MeSH terms

  • Animals
  • Apoptosis / genetics*
  • Atherosclerosis / genetics
  • Atherosclerosis / metabolism
  • Atherosclerosis / pathology
  • Carotid Artery Diseases / genetics
  • Carotid Artery Diseases / metabolism
  • Carotid Artery Diseases / pathology
  • Cell Line
  • Cell Proliferation
  • Disease Models, Animal
  • Humans
  • Macrophages / cytology*
  • Macrophages / physiology
  • Mice
  • Mice, Inbred C57BL
  • Muscle, Smooth, Vascular / cytology*
  • Muscle, Smooth, Vascular / physiology
  • Neointima / genetics*
  • Neointima / pathology
  • Proto-Oncogene Proteins c-mdm2 / metabolism
  • RNA, Long Noncoding / genetics*
  • Tumor Suppressor Protein p53 / genetics
  • Tumor Suppressor Protein p53 / metabolism*

Substances

  • RNA, Long Noncoding
  • TP53 protein, human
  • Tumor Suppressor Protein p53
  • MDM2 protein, human
  • Mdm2 protein, mouse
  • Proto-Oncogene Proteins c-mdm2