Alk1 controls arterial endothelial cell migration in lumenized vessels

Development. 2016 Jul 15;143(14):2593-602. doi: 10.1242/dev.135392. Epub 2016 Jun 10.

Abstract

Heterozygous loss of the arterial-specific TGFβ type I receptor, activin receptor-like kinase 1 (ALK1; ACVRL1), causes hereditary hemorrhagic telangiectasia (HHT). HHT is characterized by development of fragile, direct connections between arteries and veins, or arteriovenous malformations (AVMs). However, how decreased ALK1 signaling leads to AVMs is unknown. To understand the cellular mis-steps that cause AVMs, we assessed endothelial cell behavior in alk1-deficient zebrafish embryos, which develop cranial AVMs. Our data demonstrate that alk1 loss has no effect on arterial endothelial cell proliferation but alters arterial endothelial cell migration within lumenized vessels. In wild-type embryos, alk1-positive cranial arterial endothelial cells generally migrate towards the heart, against the direction of blood flow, with some cells incorporating into endocardium. In alk1-deficient embryos, migration against flow is dampened and migration in the direction of flow is enhanced. Altered migration results in decreased endothelial cell number in arterial segments proximal to the heart and increased endothelial cell number in arterial segments distal to the heart. We speculate that the consequent increase in distal arterial caliber and hemodynamic load precipitates the flow-dependent development of downstream AVMs.

Keywords: Alk1/Acvrl1; Angiogenesis; Arteriovenous malformation; Endocardium; Hereditary hemorrhagic telangiectasia; Zebrafish.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Activin Receptors / deficiency
  • Activin Receptors / metabolism*
  • Animals
  • Apoptosis
  • Arteries / cytology*
  • Arteries / metabolism
  • Brain / blood supply
  • Cell Count
  • Cell Movement*
  • Cell Proliferation
  • Coronary Circulation / physiology
  • Embryo, Mammalian / metabolism
  • Endocardium / metabolism
  • Endothelial Cells / cytology*
  • Endothelial Cells / metabolism*
  • Heart / physiology
  • Zebrafish / metabolism*
  • Zebrafish Proteins / deficiency
  • Zebrafish Proteins / metabolism*

Substances

  • Zebrafish Proteins
  • Acvrl1 protein, zebrafish
  • Activin Receptors