In vitro expansion of single Lgr5+ liver stem cells induced by Wnt-driven regeneration

Nature. 2013 Feb 14;494(7436):247-50. doi: 10.1038/nature11826. Epub 2013 Jan 27.

Abstract

The Wnt target gene Lgr5 (leucine-rich-repeat-containing G-protein-coupled receptor 5) marks actively dividing stem cells in Wnt-driven, self-renewing tissues such as small intestine and colon, stomach and hair follicles. A three-dimensional culture system allows long-term clonal expansion of single Lgr5(+) stem cells into transplantable organoids (budding cysts) that retain many characteristics of the original epithelial architecture. A crucial component of the culture medium is the Wnt agonist RSPO1, the recently discovered ligand of LGR5. Here we show that Lgr5-lacZ is not expressed in healthy adult liver, however, small Lgr5-LacZ(+) cells appear near bile ducts upon damage, coinciding with robust activation of Wnt signalling. As shown by mouse lineage tracing using a new Lgr5-IRES-creERT2 knock-in allele, damage-induced Lgr5(+) cells generate hepatocytes and bile ducts in vivo. Single Lgr5(+) cells from damaged mouse liver can be clonally expanded as organoids in Rspo1-based culture medium over several months. Such clonal organoids can be induced to differentiate in vitro and to generate functional hepatocytes upon transplantation into Fah(-/-) mice. These findings indicate that previous observations concerning Lgr5(+) stem cells in actively self-renewing tissues can also be extended to damage-induced stem cells in a tissue with a low rate of spontaneous proliferation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alleles
  • Animals
  • Bile Ducts / cytology
  • Bile Ducts / metabolism
  • Cell Lineage
  • Clone Cells / cytology
  • Clone Cells / metabolism
  • Culture Media / chemistry
  • Culture Media / metabolism
  • Disease Models, Animal
  • Female
  • Gene Knock-In Techniques
  • Hepatocytes / cytology*
  • Hepatocytes / metabolism*
  • Hepatocytes / pathology
  • Hydrolases / deficiency
  • Hydrolases / genetics
  • Liver / cytology
  • Liver / metabolism
  • Liver / pathology
  • Liver Diseases / metabolism
  • Liver Diseases / pathology
  • Male
  • Mice
  • Multipotent Stem Cells / cytology
  • Multipotent Stem Cells / metabolism
  • Organoids / cytology
  • Organoids / transplantation
  • Receptors, G-Protein-Coupled / agonists
  • Receptors, G-Protein-Coupled / deficiency
  • Receptors, G-Protein-Coupled / genetics
  • Receptors, G-Protein-Coupled / metabolism*
  • Regeneration*
  • Stem Cells / cytology*
  • Stem Cells / metabolism*
  • Thrombospondins / deficiency
  • Thrombospondins / genetics
  • Thrombospondins / metabolism
  • Tyrosinemias / metabolism
  • Tyrosinemias / pathology
  • Wnt Signaling Pathway*

Substances

  • Culture Media
  • Lgr5 protein, mouse
  • RSPO1 protein, mouse
  • Receptors, G-Protein-Coupled
  • Thrombospondins
  • Hydrolases
  • fumarylacetoacetase

Associated data

  • GEO/GSE32210