Elevated microRNA-155 promotes foam cell formation by targeting HBP1 in atherogenesis

Cardiovasc Res. 2014 Jul 1;103(1):100-10. doi: 10.1093/cvr/cvu070. Epub 2014 Mar 27.

Abstract

Aim: MicroRNAs (miRNAs) play key roles in inflammatory responses of macrophages. However, the function of miRNAs in macrophage-derived foam cell formation is unclear. Here, we investigated the role of miRNAs in macrophage-derived foam cell formation and atherosclerotic development.

Methods and results: Using quantitative reverse transcription-PCR (qRT-PCR), we found that the level of miR-155 expression was increased significantly in both plasma and macrophages from atherosclerosis (ApoE(-/-)) mice. We identified that oxidized low density lipoprotein (oxLDL) induced the expression and release of miR-155 in macrophages, and that miR-155 was required to mediate oxLDL-induced lipid uptake and reactive oxygen species (ROS) production of macrophages. Furthermore, ectopic overexpression and knockdown experiments identified that HMG box-transcription protein1 (HBP1) is a novel target of miR-155. Knockdown of HBP1 enhanced lipid uptake and ROS production in oxLDL-stimulated macrophages, and overexpression of HBP1 repressed these effects. Furthermore, bioinformatics analysis identified three YY1 binding sites in the promoter region of pri-miR-155 and verified YY1 binding directly to its promoter region. Detailed analysis showed that the YY1/HDAC2/4 complex negatively regulated the expression of miR-155 to suppress oxLDL-induced foam cell formation. Importantly, inhibition of miR-155 by a systemically delivered antagomiR-155 decreased clearly lipid-loading in macrophages and reduced atherosclerotic plaques in ApoE(-/-) mice. Moreover, we observed that the level of miR-155 expression was up-regulated in CD14(+) monocytes from patients with coronary heart disease.

Conclusion: Our findings reveal a new regulatory pathway of YY1/HDACs/miR-155/HBP1 in macrophage-derived foam cell formation during early atherogenesis and suggest that miR-155 is a potential therapeutic target for atherosclerosis.

Keywords: Atherogenesis; Foam cell formation; HBP1; MicroRNA; YY1.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Apolipoproteins E / deficiency
  • Apolipoproteins E / genetics
  • Atherosclerosis / etiology*
  • Atherosclerosis / metabolism
  • Atherosclerosis / pathology
  • Binding Sites / genetics
  • Case-Control Studies
  • Coronary Disease / genetics
  • Coronary Disease / metabolism
  • Foam Cells / metabolism*
  • Foam Cells / pathology*
  • Gene Knockdown Techniques
  • High Mobility Group Proteins / antagonists & inhibitors*
  • High Mobility Group Proteins / genetics
  • High Mobility Group Proteins / metabolism
  • Histone Deacetylase 2 / metabolism
  • Histone Deacetylases / metabolism
  • Humans
  • Lipoproteins, LDL / metabolism
  • Male
  • Mice
  • Mice, Knockout
  • MicroRNAs / genetics*
  • MicroRNAs / metabolism*
  • Monocytes / metabolism
  • Promoter Regions, Genetic
  • Reactive Oxygen Species / metabolism
  • Repressor Proteins / antagonists & inhibitors*
  • Repressor Proteins / genetics
  • Repressor Proteins / metabolism
  • YY1 Transcription Factor / metabolism

Substances

  • Apolipoproteins E
  • Hbp1 protein, mouse
  • High Mobility Group Proteins
  • Lipoproteins, LDL
  • MIRN155 microRNA, human
  • MicroRNAs
  • Mirn155 microRNA, mouse
  • Reactive Oxygen Species
  • Repressor Proteins
  • YY1 Transcription Factor
  • Yy1 protein, mouse
  • oxidized low density lipoprotein
  • Hdac2 protein, mouse
  • Hdac5 protein, mouse
  • Histone Deacetylase 2
  • Histone Deacetylases