Insulin-Like Growth Factor 1 Receptor-Dependent Pathway Drives Epicardial Adipose Tissue Formation After Myocardial Injury

Circulation. 2017 Jan 3;135(1):59-72. doi: 10.1161/CIRCULATIONAHA.116.022064. Epub 2016 Nov 1.

Abstract

Background: Epicardial adipose tissue volume and coronary artery disease are strongly associated, even after accounting for overall body mass. Despite its pathophysiological significance, the origin and paracrine signaling pathways that regulate epicardial adipose tissue's formation and expansion are unclear.

Methods: We used a novel modified mRNA-based screening approach to probe the effect of individual paracrine factors on epicardial progenitors in the adult heart.

Results: Using 2 independent lineage-tracing strategies in murine models, we show that cells originating from the Wt1+ mesothelial lineage, which includes epicardial cells, differentiate into epicardial adipose tissue after myocardial infarction. This differentiation process required Wt1 expression in this lineage and was stimulated by insulin-like growth factor 1 receptor (IGF1R) activation. IGF1R inhibition within this lineage significantly reduced its adipogenic differentiation in the context of exogenous, IGF1-modified mRNA stimulation. Moreover, IGF1R inhibition significantly reduced Wt1 lineage cell differentiation into adipocytes after myocardial infarction.

Conclusions: Our results establish IGF1R signaling as a key pathway that governs epicardial adipose tissue formation in the context of myocardial injury by redirecting the fate of Wt1+ lineage cells. Our study also demonstrates the power of modified mRNA -based paracrine factor library screening to dissect signaling pathways that govern progenitor cell activity in homeostasis and disease.

Keywords: Wt1; epicardial adipose tissue; epicardium; insulin-like growth factor-1; myocardial infarction.

MeSH terms

  • Adipocytes / cytology
  • Adipocytes / metabolism*
  • Animals
  • Cell Differentiation
  • Cell Lineage
  • Cells, Cultured
  • Disease Models, Animal
  • Gene Expression Profiling
  • Humans
  • Insulin-Like Growth Factor I / metabolism
  • Mesenchymal Stem Cells / cytology*
  • Mesenchymal Stem Cells / metabolism
  • Mice
  • Myocardial Infarction / metabolism
  • Myocardial Infarction / pathology*
  • Paracrine Communication
  • Pericardium / cytology*
  • Real-Time Polymerase Chain Reaction
  • Receptor, IGF Type 1 / genetics
  • Receptor, IGF Type 1 / metabolism*
  • Repressor Proteins / metabolism
  • Signal Transduction
  • WT1 Proteins

Substances

  • Repressor Proteins
  • WT1 Proteins
  • WT1 protein, mouse
  • Insulin-Like Growth Factor I
  • Receptor, IGF Type 1