Specification of fetal liver endothelial progenitors to functional zonated adult sinusoids requires c-Maf induction

Cell Stem Cell. 2022 Apr 7;29(4):593-609.e7. doi: 10.1016/j.stem.2022.03.002. Epub 2022 Mar 31.

Abstract

The liver vascular network is patterned by sinusoidal and hepatocyte co-zonation. How intra-liver vessels acquire their hierarchical specialized functions is unknown. We study heterogeneity of hepatic vascular cells during mouse development through functional and single-cell RNA-sequencing. The acquisition of sinusoidal endothelial cell identity is initiated during early development and completed postnatally, originating from a pool of undifferentiated vascular progenitors at E12. The peri-natal induction of the transcription factor c-Maf is a critical switch for the sinusoidal identity determination. Endothelium-restricted deletion of c-Maf disrupts liver sinusoidal development, aberrantly expands postnatal liver hematopoiesis, promotes excessive postnatal sinusoidal proliferation, and aggravates liver pro-fibrotic sensitivity to chemical insult. Enforced c-Maf overexpression in generic human endothelial cells switches on a liver sinusoidal transcriptional program that maintains hepatocyte function. c-Maf represents an inducible intra-organotypic and niche-responsive molecular determinant of hepatic sinusoidal cell identity and lays the foundation for the strategies for vasculature-driven liver repair.

Keywords: c-Maf; development; endothelial cell reprogramming; endothelial cell specification; fibrosis; hepatic angiocrine factors; liver sinusoidal endothelial cells; postnatal maturation; single-cell RNAseq; single-cell molecular profiling; vascular heterogeneity.

Publication types

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

MeSH terms

  • Animals
  • Capillaries*
  • Endothelial Cells*
  • Endothelium
  • Liver / pathology
  • Liver Cirrhosis / pathology
  • Liver Regeneration
  • Mice
  • Proto-Oncogene Proteins c-maf

Substances

  • Maf protein, mouse
  • Proto-Oncogene Proteins c-maf