The potassium channel Kcne3 is a VEGFA-inducible gene selectively expressed by vascular endothelial tip cells

Angiogenesis. 2020 May;23(2):179-192. doi: 10.1007/s10456-019-09696-8. Epub 2019 Nov 21.

Abstract

Angiogenesis is largely driven by motile endothelial tip-cells capable of invading avascular tissue domains and enabling new vessel formation. Highly responsive to Vascular Endothelial Growth-Factor-A (VEGFA), endothelial tip-cells also suppress angiogenic sprouting in adjacent stalk cells, and thus have been a primary therapeutic focus in addressing neovascular pathologies. Surprisingly, however, there remains a paucity of specific endothelial tip-cell markers. Here, we employ transcriptional profiling and a lacZ reporter allele to identify Kcne3 as an early and selective endothelial tip-cell marker in multiple angiogenic contexts. In development, Kcne3 expression initiates during early phases of angiogenesis (E9) and remains specific to endothelial tip-cells, often adjacent to regions expressing VEGFA. Consistently, Kcne3 activation is highly responsive to exogenous VEGFA but maintains tip-cell specificity throughout normal retinal angiogenesis. We also demonstrate endothelial tip-cell selectivity of Kcne3 in several injury and tumor models. Together, our data show that Kcne3 is a unique marker of sprouting angiogenic tip-cells and offers new opportunities for investigating and targeting this cell type.

Keywords: Endothelial tip-cell; Kcne3; Retinal angiogenesis; VEGFA.

MeSH terms

  • Animals
  • Animals, Newborn
  • Cell Differentiation / genetics
  • Cells, Cultured
  • Diabetic Retinopathy / genetics
  • Diabetic Retinopathy / pathology
  • Embryo, Mammalian
  • Endothelial Cells / pathology
  • Endothelial Cells / physiology*
  • Female
  • Gene Expression Regulation, Developmental / drug effects
  • Mice
  • Mice, 129 Strain
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Morphogenesis / genetics
  • Neovascularization, Pathologic / genetics*
  • Neovascularization, Pathologic / metabolism
  • Neovascularization, Physiologic / genetics*
  • Potassium Channels, Voltage-Gated / genetics*
  • Pregnancy
  • Retina / metabolism
  • Retina / pathology
  • Retinal Vessels / metabolism
  • Retinal Vessels / pathology
  • Vascular Endothelial Growth Factor A / physiology*

Substances

  • Kcne3 protein, mouse
  • Potassium Channels, Voltage-Gated
  • Vascular Endothelial Growth Factor A
  • vascular endothelial growth factor A, mouse