Regulation of vasculogenesis and angiogenesis by EphB/ephrin-B2 signaling between endothelial cells and surrounding mesenchymal cells

Blood. 2002 Aug 15;100(4):1326-33.

Abstract

Although the cellular and molecular mechanisms governing angiogenesis are only beginning to be understood, signaling through endothelial-restricted receptors, particularly receptor tyrosine kinases, has been shown to play a pivotal role in these events. Recent reports show that EphB receptor tyrosine kinases and their transmembrane-type ephrin-B2 ligands play essential roles in the embryonic vasculature. These studies suggest that cell-to-cell repellent effects due to bidirectional EphB/ephrin-B2 signaling may be crucial for vascular development, similar to the mechanism described for neuronal development. To test this hypothesis, we disrupted the precise expression pattern of EphB/ephrin-B2 in vivo by generating transgenic (CAGp-ephrin-B2 Tg) mice that express ephrin-B2 under the control of a ubiquitous and constitutive promoter, CMV enhancer-beta-actin promoter-beta-globin splicing acceptor (CAG). These mice displayed an abnormal segmental arrangement of intersomitic vessels, while such anomalies were not observed in Tie-2p-ephrin-B2 Tg mice in which ephrin-B2 was overexpressed in only vascular endothelial cells (ECs). This finding suggests that non-ECs expressing ephrin-B2 alter the migration of ECs expressing EphB receptors into the intersomitic region where ephrin-B2 expression is normally absent. CAGp-ephrin-B2 Tg mice show sudden death at neonatal stages from aortic dissecting aneurysms due to defective recruitment of vascular smooth muscle cells to the ascending aorta. EphB/ephrin-B2 signaling between endothelial cells and surrounding mesenchymal cells plays an essential role in vasculogenesis, angiogenesis, and vessel maturation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Actins / genetics
  • Animals
  • Animals, Newborn
  • Aortic Aneurysm / genetics
  • Aortic Dissection / genetics
  • Blood Vessels / embryology*
  • Capillaries / metabolism
  • Cell Line
  • Cytomegalovirus / genetics
  • Endothelium, Vascular / metabolism*
  • Enhancer Elements, Genetic
  • Ephrin-B2
  • Gene Expression
  • Globins / genetics
  • Membrane Proteins / genetics
  • Membrane Proteins / physiology*
  • Mesoderm / metabolism*
  • Mice
  • Mice, Transgenic
  • Muscle, Smooth, Vascular / metabolism
  • Neovascularization, Physiologic / physiology*
  • Promoter Regions, Genetic
  • RNA Splicing
  • Receptor Protein-Tyrosine Kinases / physiology
  • Receptors, Eph Family
  • Signal Transduction*

Substances

  • Actins
  • Ephrin-B2
  • Membrane Proteins
  • Globins
  • Receptor Protein-Tyrosine Kinases
  • Receptors, Eph Family