Pancreatic Cell Fate Determination Relies on Notch Ligand Trafficking by NFIA

Cell Rep. 2018 Dec 26;25(13):3811-3827.e7. doi: 10.1016/j.celrep.2018.11.078.

Abstract

Notch is activated globally in pancreatic progenitors; however, for progenitors to differentiate into endocrine cells, they must escape Notch activation to express Neurogenin-3. Here, we find that the transcription factor nuclear factor I/A (NFIA) promotes endocrine development by regulating Notch ligand Dll1 trafficking. Pancreatic deletion of NFIA leads to cell fate defects, with increased duct and decreased endocrine formation, while ectopic expression promotes endocrine formation in mice and human pancreatic progenitors. NFIA-deficient mice exhibit dysregulation of trafficking-related genes including increased expression of Mib1, which acts to target Dll1 for endocytosis. We find that NFIA binds to the Mib1 promoter, with loss of NFIA leading to an increase in Dll1 internalization and enhanced Notch activation with rescue of the cell fate defects after Mib1 knockdown. This study reveals NFIA as a pro-endocrine factor in the pancreas, acting to repress Mib1, inhibit Dll1 endocytosis and thus promote escape from Notch activation.

Keywords: Mib1; NFIA; Notch signaling; cell fate; development; endocrine cell; endocytosis; pancreas.

Publication types

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

MeSH terms

  • Animals
  • Calcium-Binding Proteins
  • Cell Lineage*
  • Endocytosis
  • Gene Expression Regulation
  • Human Embryonic Stem Cells / cytology
  • Human Embryonic Stem Cells / metabolism
  • Humans
  • Intercellular Signaling Peptides and Proteins / metabolism*
  • Ligands
  • Male
  • Membrane Proteins / metabolism*
  • Mice, Knockout
  • NFI Transcription Factors / metabolism*
  • Pancreas / cytology*
  • Pancreas / metabolism
  • Pancreas / ultrastructure
  • Protein Transport
  • Receptors, Notch / metabolism*
  • Ubiquitin-Protein Ligases / metabolism

Substances

  • Calcium-Binding Proteins
  • DLK1 protein, human
  • Dlk1 protein, mouse
  • Intercellular Signaling Peptides and Proteins
  • Ligands
  • Membrane Proteins
  • NFI Transcription Factors
  • Receptors, Notch
  • MIB1 protein, mouse
  • Ubiquitin-Protein Ligases