Multi-site Neurogenin3 Phosphorylation Controls Pancreatic Endocrine Differentiation

Dev Cell. 2017 May 8;41(3):274-286.e5. doi: 10.1016/j.devcel.2017.04.004. Epub 2017 Apr 27.

Abstract

The proneural transcription factor Neurogenin3 (Ngn3) plays a critical role in pancreatic endocrine cell differentiation, although regulation of Ngn3 protein is largely unexplored. Here we demonstrate that Ngn3 protein undergoes cyclin-dependent kinase (Cdk)-mediated phosphorylation on multiple serine-proline sites. Replacing wild-type protein with a phosphomutant form of Ngn3 increases α cell generation, the earliest endocrine cell type to be formed in the developing pancreas. Moreover, un(der)phosphorylated Ngn3 maintains insulin expression in adult β cells in the presence of elevated c-Myc and enhances endocrine specification during ductal reprogramming. Mechanistically, preventing multi-site phosphorylation enhances both Ngn3 stability and DNA binding, promoting the increased expression of target genes that drive differentiation. Therefore, multi-site phosphorylation of Ngn3 controls its ability to promote pancreatic endocrine differentiation and to maintain β cell function in the presence of pro-proliferation cues and could be manipulated to promote and maintain endocrine differentiation in vitro and in vivo.

Keywords: diabetes; endocrine differentiation; insulinoma; neurogenin3; pancreatic development; pancreatic organoids; proneural bHLH transcription factors; β cells.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Basic Helix-Loop-Helix Transcription Factors / metabolism*
  • Cell Differentiation / physiology*
  • Cyclin-Dependent Kinases / metabolism
  • Homeodomain Proteins / metabolism
  • Humans
  • Insulin-Secreting Cells / metabolism*
  • Islets of Langerhans / cytology*
  • Mice
  • Nerve Tissue Proteins / metabolism*
  • Pancreas / metabolism
  • Phosphorylation
  • Signal Transduction / physiology

Substances

  • Basic Helix-Loop-Helix Transcription Factors
  • Homeodomain Proteins
  • NEUROG3 protein, human
  • Nerve Tissue Proteins
  • Neurog3 protein, mouse
  • Cyclin-Dependent Kinases