Deciphering the Dynamic Transcriptional and Post-transcriptional Networks of Macrophages in the Healthy Heart and after Myocardial Injury

Cell Rep. 2018 Apr 10;23(2):622-636. doi: 10.1016/j.celrep.2018.03.029.

Abstract

Macrophage plasticity has been studied in vitro, but transcriptional regulation upon injury is poorly understood. We generated a valuable dataset that captures transcriptional changes in the healthy heart and after myocardial injury, revealing a dynamic transcriptional landscape of macrophage activation. Partial deconvolution suggested that post-injury macrophages exhibit overlapping activation of pro-inflammatory and anti-inflammatory programs rather than aligning to canonical M1/M2 programs. Furthermore, simulated dynamics and experimental validation of a regulatory core of the underlying gene-regulatory network revealed a negative-feedback loop that limits initial inflammation via hypoxia-mediated upregulation of Il10. Our results also highlight the prominence of post-transcriptional regulation (miRNAs, mRNA decay, and lincRNAs) in attenuating the myocardial injury-induced inflammatory response. We also identified a cardiac-macrophage-specific gene signature (e.g., Egfr and Lifr) and time-specific markers for macrophage populations (e.g., Lyve1, Cd40, and Mrc1). Altogether, these data provide a core resource for deciphering the transcriptional network in cardiac macrophages in vivo.

Keywords: Boolean dynamical model; IL-10; heart; lincRNAs; miRnome; myocardial injury; partial deconvolution; transcriptome analysis.

MeSH terms

  • 3' Untranslated Regions
  • AU Rich Elements / genetics
  • Animals
  • CX3C Chemokine Receptor 1 / genetics
  • Gene Expression Regulation
  • Gene Regulatory Networks*
  • Heart Injuries / metabolism*
  • Heart Injuries / pathology
  • Macrophages / cytology
  • Macrophages / immunology
  • Macrophages / metabolism*
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Myocardium / metabolism*
  • Principal Component Analysis
  • RNA, Long Noncoding / metabolism
  • RNA, Messenger / metabolism
  • RNA-Binding Proteins / genetics
  • RNA-Binding Proteins / metabolism
  • Transcriptome*

Substances

  • 3' Untranslated Regions
  • CX3C Chemokine Receptor 1
  • Cx3cr1 protein, mouse
  • RNA, Long Noncoding
  • RNA, Messenger
  • RNA-Binding Proteins