Hes3 is expressed in the adult pancreatic islet and regulates gene expression, cell growth, and insulin release

J Biol Chem. 2014 Dec 19;289(51):35503-16. doi: 10.1074/jbc.M114.590687. Epub 2014 Nov 4.

Abstract

The transcription factor Hes3 is a component of a signaling pathway that supports the growth of neural stem cells with profound consequences in neurodegenerative disease models. Here we explored whether Hes3 also regulates pancreatic islet cells. We showed that Hes3 is expressed in human and rodent pancreatic islets. In mouse islets it co-localizes with alpha and beta cell markers. We employed the mouse insulinoma cell line MIN6 to perform in vitro characterization and functional studies in conditions known to modulate Hes3 based upon our previous work using neural stem cell cultures. In these conditions, cells showed elevated Hes3 expression and nuclear localization, grew efficiently, and showed higher evoked insulin release responses, compared with serum-containing conditions. They also exhibited higher expression of the transcription factor Pdx1 and insulin. Furthermore, they were responsive to pharmacological treatments with the GLP-1 analog Exendin-4, which increased nuclear Hes3 localization. We employed a transfection approach to address specific functions of Hes3. Hes3 RNA interference opposed cell growth and affected gene expression as revealed by DNA microarrays. Western blotting and PCR approaches specifically showed that Hes3 RNA interference opposes the expression of Pdx1 and insulin. Hes3 overexpression (using a Hes3-GFP fusion construct) confirmed a role of Hes3 in regulating Pdx1 expression. Hes3 RNA interference reduced evoked insulin release. Mice lacking Hes3 exhibited increased islet damage by streptozotocin. These data suggest roles of Hes3 in pancreatic islet function.

Keywords: Beta Cell (B-cell); Cell Culture; Islet; Neural Stem Cell (NSC); Neurodegenerative Disease; Neuroprogenitor Cell; Notch Pathway; Pancreas; Parkinson Disease; Signal Transduction.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Animals
  • Basic Helix-Loop-Helix Transcription Factors / genetics
  • Basic Helix-Loop-Helix Transcription Factors / metabolism
  • Blotting, Western
  • Cell Line, Tumor
  • Cell Nucleus / drug effects
  • Cell Nucleus / metabolism
  • Cell Proliferation*
  • DNA-Binding Proteins / genetics*
  • DNA-Binding Proteins / metabolism
  • Diabetes Mellitus, Experimental / genetics
  • Diabetes Mellitus, Experimental / metabolism
  • Diabetes Mellitus, Experimental / pathology
  • Exenatide
  • Gene Expression Profiling
  • Gene Expression*
  • Homeodomain Proteins / genetics
  • Homeodomain Proteins / metabolism
  • Humans
  • Hypoglycemic Agents / pharmacology
  • Insulin / genetics
  • Insulin / metabolism*
  • Insulin Secretion
  • Insulinoma / genetics
  • Insulinoma / metabolism
  • Insulinoma / pathology
  • Islets of Langerhans / cytology
  • Islets of Langerhans / drug effects
  • Islets of Langerhans / metabolism*
  • Mice, Inbred C57BL
  • Mice, Mutant Strains
  • Mice, Obese
  • Microscopy, Confocal
  • Nerve Tissue Proteins / genetics
  • Nerve Tissue Proteins / metabolism
  • Pancreatic Neoplasms / genetics
  • Pancreatic Neoplasms / metabolism
  • Pancreatic Neoplasms / pathology
  • Peptides / pharmacology
  • RNA Interference
  • Repressor Proteins
  • Reverse Transcriptase Polymerase Chain Reaction
  • Trans-Activators / genetics
  • Trans-Activators / metabolism
  • Transcription Factors / genetics*
  • Transcription Factors / metabolism
  • Venoms / pharmacology

Substances

  • Basic Helix-Loop-Helix Transcription Factors
  • DNA-Binding Proteins
  • HES3 protein, human
  • Hes3 protein, mouse
  • Homeodomain Proteins
  • Hypoglycemic Agents
  • Insulin
  • Nerve Tissue Proteins
  • Peptides
  • Repressor Proteins
  • Trans-Activators
  • Transcription Factors
  • Venoms
  • pancreatic and duodenal homeobox 1 protein
  • Exenatide