Modelling human hepato-biliary-pancreatic organogenesis from the foregut-midgut boundary

Nature. 2019 Oct;574(7776):112-116. doi: 10.1038/s41586-019-1598-0. Epub 2019 Sep 25.

Abstract

Organogenesis is a complex and interconnected process that is orchestrated by multiple boundary tissue interactions1-7. However, it remains unclear how individual, neighbouring components coordinate to establish an integral multi-organ structure. Here we report the continuous patterning and dynamic morphogenesis of hepatic, biliary and pancreatic structures, invaginating from a three-dimensional culture of human pluripotent stem cells. The boundary interactions between anterior and posterior gut spheroids differentiated from human pluripotent stem cells enables retinoic acid-dependent emergence of hepato-biliary-pancreatic organ domains specified at the foregut-midgut boundary organoids in the absence of extrinsic factors. Whereas transplant-derived tissues are dominated by midgut derivatives, long-term-cultured microdissected hepato-biliary-pancreatic organoids develop into segregated multi-organ anlages, which then recapitulate early morphogenetic events including the invagination and branching of three different and interconnected organ structures, reminiscent of tissues derived from mouse explanted foregut-midgut culture. Mis-segregation of multi-organ domains caused by a genetic mutation in HES1 abolishes the biliary specification potential in culture, as seen in vivo8,9. In sum, we demonstrate that the experimental multi-organ integrated model can be established by the juxtapositioning of foregut and midgut tissues, and potentially serves as a tractable, manipulatable and easily accessible model for the study of complex human endoderm organogenesis.

Publication types

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

MeSH terms

  • Animals
  • Biliary Tract / cytology
  • Biliary Tract / embryology*
  • Biomarkers / analysis
  • Biomarkers / metabolism
  • Body Patterning
  • Endoderm / cytology
  • Endoderm / embryology
  • Humans
  • Induced Pluripotent Stem Cells / cytology
  • Induced Pluripotent Stem Cells / metabolism
  • Intestines / cytology
  • Intestines / embryology*
  • Liver / cytology
  • Liver / embryology*
  • Male
  • Mice
  • Models, Biological*
  • Morphogenesis*
  • Organoids / cytology
  • Organoids / embryology
  • Pancreas / cytology
  • Pancreas / embryology*
  • Spheroids, Cellular / cytology
  • Spheroids, Cellular / metabolism
  • Spheroids, Cellular / transplantation
  • Transcription Factor HES-1 / analysis
  • Transcription Factor HES-1 / metabolism

Substances

  • Biomarkers
  • Transcription Factor HES-1
  • HES1 protein, human