Chemical Enhancement of In Vitro and In Vivo Direct Cardiac Reprogramming

Circulation. 2017 Mar 7;135(10):978-995. doi: 10.1161/CIRCULATIONAHA.116.024692. Epub 2016 Nov 10.

Abstract

Background: Reprogramming of cardiac fibroblasts into induced cardiomyocyte-like cells in situ represents a promising strategy for cardiac regeneration. A combination of 3 cardiac transcription factors, Gata4, Mef2c, and Tbx5 (GMT), can convert fibroblasts into induced cardiomyocyte-like cells, albeit with low efficiency in vitro.

Methods: We screened 5500 compounds in primary cardiac fibroblasts to identify the pathways that can be modulated to enhance cardiomyocyte reprogramming.

Results: We found that a combination of the transforming growth factor-β inhibitor SB431542 and the WNT inhibitor XAV939 increased reprogramming efficiency 8-fold when added to GMT-overexpressing cardiac fibroblasts. The small molecules also enhanced the speed and quality of cell conversion; we observed beating cells as early as 1 week after reprogramming compared with 6 to 8 weeks with GMT alone. In vivo, mice exposed to GMT, SB431542, and XAV939 for 2 weeks after myocardial infarction showed significantly improved reprogramming and cardiac function compared with those exposed to only GMT. Human cardiac reprogramming was similarly enhanced on transforming growth factor-β and WNT inhibition and was achieved most efficiently with GMT plus myocardin.

Conclusions: Transforming growth factor-β and WNT inhibitors jointly enhance GMT-induced direct cardiac reprogramming from cardiac fibroblasts in vitro and in vivo and provide a more robust platform for cardiac regeneration.

Keywords: cell differentiation; heart; regeneration; transcription factors.

MeSH terms

  • Animals
  • Benzamides / pharmacology*
  • Benzamides / therapeutic use
  • Cells, Cultured
  • Cellular Reprogramming / drug effects*
  • Dioxoles / pharmacology*
  • Dioxoles / therapeutic use
  • Fibroblasts / cytology
  • Fibroblasts / drug effects
  • Fibroblasts / metabolism
  • GATA4 Transcription Factor / genetics
  • GATA4 Transcription Factor / metabolism
  • Heart / diagnostic imaging
  • Heterocyclic Compounds, 3-Ring / pharmacology*
  • Heterocyclic Compounds, 3-Ring / therapeutic use
  • Humans
  • MEF2 Transcription Factors / genetics
  • MEF2 Transcription Factors / metabolism
  • Magnetic Resonance Imaging
  • Mice
  • Myocardial Infarction / drug therapy
  • Myocardium / pathology
  • Myocytes, Cardiac / cytology
  • Myocytes, Cardiac / metabolism
  • T-Box Domain Proteins / genetics
  • T-Box Domain Proteins / metabolism
  • Transcription Factors / genetics
  • Transcription Factors / metabolism*
  • Transforming Growth Factor beta / antagonists & inhibitors
  • Transforming Growth Factor beta / metabolism
  • Wnt Proteins / antagonists & inhibitors
  • Wnt Proteins / metabolism

Substances

  • 4-(5-benzo(1,3)dioxol-5-yl-4-pyridin-2-yl-1H-imidazol-2-yl)benzamide
  • Benzamides
  • Dioxoles
  • GATA4 Transcription Factor
  • Gata4 protein, mouse
  • Heterocyclic Compounds, 3-Ring
  • MEF2 Transcription Factors
  • T-Box Domain Proteins
  • T-box transcription factor 5
  • Transcription Factors
  • Transforming Growth Factor beta
  • Wnt Proteins
  • XAV939