MEF2C-MYOCD and Leiomodin1 Suppression by miRNA-214 Promotes Smooth Muscle Cell Phenotype Switching in Pulmonary Arterial Hypertension

PLoS One. 2016 May 4;11(5):e0153780. doi: 10.1371/journal.pone.0153780. eCollection 2016.

Abstract

Background: Vascular hyperproliferative disorders are characterized by excessive smooth muscle cell (SMC) proliferation leading to vessel remodeling and occlusion. In pulmonary arterial hypertension (PAH), SMC phenotype switching from a terminally differentiated contractile to synthetic state is gaining traction as our understanding of the disease progression improves. While maintenance of SMC contractile phenotype is reportedly orchestrated by a MEF2C-myocardin (MYOCD) interplay, little is known regarding molecular control at this nexus. Moreover, the burgeoning interest in microRNAs (miRs) provides the basis for exploring their modulation of MEF2C-MYOCD signaling, and in turn, a pro-proliferative, synthetic SMC phenotype. We hypothesized that suppression of SMC contractile phenotype in pulmonary hypertension is mediated by miR-214 via repression of the MEF2C-MYOCD-leiomodin1 (LMOD1) signaling axis.

Methods and results: In SMCs isolated from a PAH patient cohort and commercially obtained hPASMCs exposed to hypoxia, miR-214 expression was monitored by qRT-PCR. miR-214 was upregulated in PAH- vs. control subject hPASMCs as well as in commercially obtained hPASMCs exposed to hypoxia. These increases in miR-214 were paralleled by MEF2C, MYOCD and SMC contractile protein downregulation. Of these, LMOD1 and MEF2C were directly targeted by the miR. Mir-214 overexpression mimicked the PAH profile, downregulating MEF2C and LMOD1. AntagomiR-214 abrogated hypoxia-induced suppression of the contractile phenotype and its attendant proliferation. Anti-miR-214 also restored PAH-PASMCs to a contractile phenotype seen during vascular homeostasis.

Conclusions: Our findings illustrate a key role for miR-214 in modulation of MEF2C-MYOCD-LMOD1 signaling and suggest that an antagonist of miR-214 could mitigate SMC phenotype changes and proliferation in vascular hyperproliferative disorders including PAH.

Publication types

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

MeSH terms

  • Antagomirs / metabolism
  • Autoantigens / metabolism*
  • Cell Differentiation / physiology
  • Cell Line
  • Cell Proliferation / physiology
  • Cytoskeletal Proteins / metabolism*
  • Down-Regulation / physiology
  • Familial Primary Pulmonary Hypertension / metabolism
  • HEK293 Cells
  • Humans
  • Hypertension, Pulmonary / metabolism*
  • MEF2 Transcription Factors / metabolism
  • MicroRNAs / metabolism*
  • Muscle Contraction / physiology
  • Muscle, Smooth, Vascular / metabolism
  • Myocytes, Smooth Muscle / metabolism*
  • Nuclear Proteins / metabolism*
  • Phenotype
  • Pulmonary Artery / metabolism*
  • Trans-Activators / metabolism*
  • Up-Regulation / physiology

Substances

  • Antagomirs
  • Autoantigens
  • Cytoskeletal Proteins
  • LMOD1 protein, human
  • MEF2 Transcription Factors
  • MEF2C protein, human
  • MicroRNAs
  • Nuclear Proteins
  • Trans-Activators
  • myocardin