5-HT(2B) antagonism arrests non-canonical TGF-β1-induced valvular myofibroblast differentiation

J Mol Cell Cardiol. 2012 Nov;53(5):707-14. doi: 10.1016/j.yjmcc.2012.08.012. Epub 2012 Aug 23.

Abstract

Transforming growth factor-β1 (TGF-β1) induces myofibroblast activation of quiescent aortic valve interstitial cells (AVICs), a differentiation process implicated in calcific aortic valve disease (CAVD). The ubiquity of TGF-β1 signaling makes it difficult to target in a tissue specific manner; however, the serotonin 2B receptor (5-HT(2B)) is highly localized to cardiopulmonary tissues and agonism of this receptor displays pro-fibrotic effects in a TGF-β1-dependent manner. Therefore, we hypothesized that antagonism of 5-HT(2B) opposes TGF-β1-induced pathologic differentiation of AVICs and may offer a druggable target to prevent CAVD. To test this hypothesis, we assessed the interaction of 5-HT(2B) antagonism with canonical and non-canonical TGF-β1 pathways to inhibit TGF-β1-induced activation of isolated porcine AVICs in vitro. Here we show that AVIC activation and subsequent calcific nodule formation is completely mitigated by 5-HT(2B) antagonism. Interestingly, 5-HT(2B) antagonism does not inhibit canonical TGF-β1 signaling as identified by Smad3 phosphorylation and activation of a partial plasminogen activator inhibitor-1 promoter (PAI-1, a transcriptional target of Smad3), but prevents non-canonical p38 MAPK phosphorylation. It was initially suspected that 5-HT(2B) antagonism prevents Src tyrosine kinase phosphorylation; however, we found that this is not the case and time-lapse microscopy indicates that 5-HT(2B) antagonism prevents non-canonical TGF-β1 signaling by physically arresting Src tyrosine kinase. This study demonstrates the necessity of non-canonical TGF-β1 signaling in leading to pathologic AVIC differentiation. Moreover, we believe that the results of this study suggest 5-HT(2B) antagonism as a novel therapeutic approach for CAVD that merits further investigation.

Publication types

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

MeSH terms

  • Actins / genetics
  • Actins / metabolism
  • Animals
  • Aortic Diseases / pathology
  • Aortic Valve / pathology
  • Calcinosis / pathology
  • Cell Differentiation / drug effects*
  • Cells, Cultured
  • Gene Expression
  • Indoles / pharmacology*
  • Microfilament Proteins / genetics
  • Microfilament Proteins / metabolism
  • Muscle Proteins / genetics
  • Muscle Proteins / metabolism
  • Myofibroblasts / physiology*
  • Phosphorylation
  • Plasminogen Activator Inhibitor 1 / genetics
  • Plasminogen Activator Inhibitor 1 / metabolism
  • Promoter Regions, Genetic
  • Protein Processing, Post-Translational
  • Protein Transport
  • Pyridines / pharmacology*
  • Receptor, Serotonin, 5-HT2B / metabolism*
  • Serotonin 5-HT2 Receptor Antagonists / pharmacology*
  • Signal Transduction
  • Smad3 Protein / metabolism
  • Sus scrofa
  • Transcriptional Activation
  • Transforming Growth Factor beta1 / physiology*
  • Urea / analogs & derivatives*
  • Urea / pharmacology
  • p38 Mitogen-Activated Protein Kinases / metabolism
  • src-Family Kinases / metabolism
  • src-Family Kinases / physiology

Substances

  • Actins
  • Indoles
  • Microfilament Proteins
  • Muscle Proteins
  • N-(1-methyl-5-indolyl)-N'-(3-methyl-5-isothiazolyl)urea
  • Plasminogen Activator Inhibitor 1
  • Pyridines
  • Receptor, Serotonin, 5-HT2B
  • Serotonin 5-HT2 Receptor Antagonists
  • Smad3 Protein
  • Transforming Growth Factor beta1
  • transgelin
  • SB 228357
  • Urea
  • src-Family Kinases
  • p38 Mitogen-Activated Protein Kinases