Notch hyper-activation drives trans-differentiation of hESC-derived endothelium

Stem Cell Res. 2016 Sep;17(2):391-400. doi: 10.1016/j.scr.2016.09.005. Epub 2016 Sep 13.

Abstract

During development, endothelial cells (EC) display tissue-specific attributes that are unique to each vascular bed, as well as generic signaling mechanisms that are broadly applied to create a patent circulatory system. We have previously utilized human embryonic stem cells (hESC) to generate tissue-specific EC sub-types (Rafii et al., 2013) and identify pathways that govern growth and trans-differentiation potential of hESC-derived ECs (James et al., 2010). Here, we elucidate a novel Notch-dependent mechanism that induces endothelial to mesenchymal transition (EndMT) in confluent monolayer cultures of hESC-derived ECs. We demonstrate density-dependent induction of EndMT that can be rescued by the Notch signaling inhibitor DAPT and identify a positive feedback signaling mechanism in hESC-ECs whereby trans-activation of Notch by DLL4 ligand induces elevated expression and surface presentation of DLL4. Increased Notch activation in confluent hESC-EC monolayer cultures induces areas of EndMT containing transitional cells that are marked by increased Jagged1 expression and reduced Notch signal integration. Jagged1 loss of function in monolayer hESC-ECs induces accelerated feedback stimulation of Notch signaling, increased expression of cell-autonomous, cis-inhibitory DLL4, and EndMT. These data elucidate a novel interplay of Notch ligands in modulating pathway activation during both expansion and EndMT of hESC-derived ECs.

MeSH terms

  • Benzamides / pharmacology
  • Cell Transdifferentiation
  • Cells, Cultured
  • Diamines / pharmacology
  • Dioxoles / pharmacology
  • Endothelial Cells / cytology
  • Endothelial Cells / metabolism*
  • Human Embryonic Stem Cells / cytology*
  • Human Embryonic Stem Cells / metabolism
  • Humans
  • Intracellular Signaling Peptides and Proteins / antagonists & inhibitors
  • Intracellular Signaling Peptides and Proteins / chemistry
  • Intracellular Signaling Peptides and Proteins / metabolism
  • Jagged-1 Protein / antagonists & inhibitors
  • Jagged-1 Protein / genetics
  • Jagged-1 Protein / metabolism
  • Membrane Proteins / antagonists & inhibitors
  • Membrane Proteins / chemistry
  • Membrane Proteins / metabolism
  • Microscopy, Fluorescence
  • RNA Interference
  • RNA, Small Interfering / metabolism
  • Receptors, Notch / antagonists & inhibitors
  • Receptors, Notch / genetics
  • Receptors, Notch / metabolism*
  • Signal Transduction / drug effects
  • Thiazoles / pharmacology
  • Transcriptional Activation

Substances

  • 24-diamino-5-phenylthiazole
  • 4-(5-benzo(1,3)dioxol-5-yl-4-pyridin-2-yl-1H-imidazol-2-yl)benzamide
  • Benzamides
  • Diamines
  • Dioxoles
  • Intracellular Signaling Peptides and Proteins
  • Jagged-1 Protein
  • Membrane Proteins
  • RNA, Small Interfering
  • Receptors, Notch
  • Thiazoles
  • delta protein