Paracrine signals regulate human liver organoid maturation from induced pluripotent stem cells

Development. 2017 Mar 15;144(6):1056-1064. doi: 10.1242/dev.142794.

Abstract

A self-organizing organoid model provides a new approach to study the mechanism of human liver organogenesis. Previous animal models documented that simultaneous paracrine signaling and cell-to-cell surface contact regulate hepatocyte differentiation. To dissect the relative contributions of the paracrine effects, we first established a liver organoid using human induced pluripotent stem cells (iPSCs), mesenchymal stem cells (MSCs) and human umbilical vein endothelial cells (HUVECs) as previously reported. Time-lapse imaging showed that hepatic-specified endoderm iPSCs (HE-iPSCs) self-assembled into three-dimensional organoids, resulting in hepatic gene induction. Progressive differentiation was demonstrated by hepatic protein production after in vivo organoid transplantation. To assess the paracrine contributions, we employed a Transwell system in which HE-iPSCs were separately co-cultured with MSCs and/or HUVECs. Although the three-dimensional structure did not form, their soluble factors induced a hepatocyte-like phenotype in HE-iPSCs, resulting in the expression of bile salt export pump. In conclusion, the mesoderm-derived paracrine signals promote hepatocyte maturation in liver organoids, but organoid self-organization requires cell-to-cell surface contact. Our in vitro model demonstrates a novel approach to identify developmental paracrine signals regulating the differentiation of human hepatocytes.

Keywords: ABCB11; Hepatocyte differentiation; Liver development; Regeneration; Tissue engineering.

MeSH terms

  • Animals
  • Bile Acids and Salts / metabolism
  • Biological Transport
  • Biomarkers / metabolism
  • Cell Differentiation*
  • Cell Polarity
  • Coculture Techniques
  • Gene Expression Regulation
  • Hepatocytes / cytology
  • Hepatocytes / ultrastructure
  • Human Umbilical Vein Endothelial Cells / cytology
  • Human Umbilical Vein Endothelial Cells / metabolism
  • Humans
  • Induced Pluripotent Stem Cells / cytology*
  • Induced Pluripotent Stem Cells / metabolism
  • Liver / cytology*
  • Mesenchymal Stem Cells / cytology
  • Mesenchymal Stem Cells / metabolism
  • Mice
  • Morphogenesis / genetics
  • Organ Specificity / genetics
  • Organoids / cytology*
  • Organoids / metabolism
  • Paracrine Communication*
  • Proteins / analysis

Substances

  • Bile Acids and Salts
  • Biomarkers
  • Proteins