Foxf1-mediated co-regulation of miR-495 and let-7c modulates epicardial cell migration and myocardial specification

Cell Mol Life Sci. 2025 Jun 25;82(1):254. doi: 10.1007/s00018-025-05735-4.

Abstract

Background: The heart is the first functional organ to develop in the vertebrate embryos. In mice, the primitive tubular heart begins beating at embryonic day (E) 8.0-E.8.5 and undergoes rightward looping to form the atrial and ventricular chambers. The proepicardium, a transient cell cluster at the sinus venous-lateral plate mesenchyme junction migrates onto the heart and gives rise to the embryonic epicardium, a squamous epithelium that plays a key role in cardiac development. Despite advances in understanding epicardial lineage contributions, the molecular mechanisms governing these processes remain poorly understood.

Methods: To characterize the transcriptional and post-transcriptional regulation of epicardial development, we performed RNA sequencing at two critical timepoints, proepicardium formation and embryonic epicardium establishment. We analysed differentially expressed coding and non-coding RNAs, focusing on microRNAs and their potential regulatory interactions.

Results: We identified a complex network involving differentially expressed mRNAs, microRNAs and lncRNAs between proepicardium and embryonic epicardium. Notably, with miR-495 and let-7c emerged as key regulators of epicardial cell migration, an essential process for proper epicardium formation and epicardial-derived cell migration. Our findings also reveal that these microRNAs not only regulate target gene expression but also modulate other microRNAs, suggesting a novel regulatory mechanism in epicardial development. Additionally, Foxf1 inhibition modulates let-7c, promoting the expression of key cardiogenic lineage markers in epicardial cells.

Conclusion: Our study highlights the role of Foxf1 in regulating miR-495 and let-7c, which in turn modulate epicardial cell migration and myocardial specification. These finding provide new insights into the intricate interplay between transcription factors and microRNAs in governing cardiogenesis.

Keywords: Cell lineage specification; Cell migration; Epicardial cells; MicroRNAs; Transcription factors.

MeSH terms

  • Animals
  • Cell Movement* / genetics
  • Forkhead Transcription Factors* / genetics
  • Forkhead Transcription Factors* / metabolism
  • Gene Expression Regulation, Developmental
  • Mice
  • MicroRNAs* / genetics
  • MicroRNAs* / metabolism
  • Myocardium* / cytology
  • Myocardium* / metabolism
  • Pericardium* / cytology
  • Pericardium* / embryology
  • Pericardium* / metabolism
  • RNA, Long Noncoding / genetics
  • RNA, Long Noncoding / metabolism

Substances

  • MicroRNAs
  • Forkhead Transcription Factors
  • Foxf1 protein, mouse
  • mirnlet7 microRNA, mouse
  • RNA, Long Noncoding