AKAP12 deficiency impairs VEGF-induced endothelial cell migration and sprouting

Acta Physiol (Oxf). 2020 Jan;228(1):e13325. doi: 10.1111/apha.13325. Epub 2019 Jun 21.

Abstract

Aim: Protein kinase (PK) A anchoring protein (AKAP) 12 is a scaffolding protein that anchors PKA to compartmentalize cyclic AMP signalling. This study assessed the consequences of the downregulation or deletion of AKAP12 on endothelial cell migration and angiogenesis.

Methods: The consequences of siRNA-mediated downregulation AKAP12 were studied in primary cultures of human endothelial cells as well as in endothelial cells and retinas from wild-type versus AKAP12-/- mice. Molecular interactions were investigated using a combination of immunoprecipitation and mass spectrometry.

Results: AKAP12 was expressed at low levels in confluent endothelial cells but its expression was increased in actively migrating cells, where it localized to lamellipodia. In the postnatal retina, AKAP12 was expressed by actively migrating tip cells at the angiogenic front, and its deletion resulted in defective extension of the vascular plexus. In migrating endothelial cells, AKAP12 was co-localized with the PKA type II-α regulatory subunit as well as multiple key regulators of actin dynamics and actin filament-based movement; including components of the Arp2/3 complex and the vasodilator-stimulated phosphoprotein (VASP). Fitting with the evidence of a physical VASP/AKAP12/PKA complex, it was possible to demonstrate that the VEGF-stimulated and PKA-dependent phosphorylation of VASP was dependent on AKAP12. Indeed, AKAP12 colocalized with phospho-Ser157 VASP at the leading edge of migrating endothelial cells.

Conclusion: The results suggest that compartmentalized AKAP12/PKA signalling mediates VASP phosphorylation at the leading edge of migrating endothelial cells to translate angiogenic stimuli into altered actin dynamics and cell movement.

Keywords: angiogenesis; protein kinase A; protein kinase A anchoring protein 12; retina; vasodilator-stimulated phosphoprotein.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • A Kinase Anchor Proteins / genetics
  • A Kinase Anchor Proteins / metabolism*
  • Animals
  • Cell Adhesion Molecules / genetics
  • Cell Adhesion Molecules / metabolism
  • Cell Cycle Proteins / genetics
  • Cell Cycle Proteins / metabolism*
  • Cell Movement / drug effects
  • Cell Movement / physiology
  • Cyclic AMP-Dependent Protein Kinases / genetics
  • Cyclic AMP-Dependent Protein Kinases / metabolism
  • Endothelial Cells / drug effects*
  • Endothelial Cells / physiology
  • Gene Expression Regulation / drug effects
  • Gene Expression Regulation / physiology
  • Mice
  • Mice, Knockout
  • Microfilament Proteins / genetics
  • Microfilament Proteins / metabolism
  • Phosphoproteins / genetics
  • Phosphoproteins / metabolism
  • Phosphorylation
  • Vascular Endothelial Growth Factor A / administration & dosage
  • Vascular Endothelial Growth Factor A / pharmacology*

Substances

  • A Kinase Anchor Proteins
  • Akap12 protein, mouse
  • Cell Adhesion Molecules
  • Cell Cycle Proteins
  • Microfilament Proteins
  • Phosphoproteins
  • Vascular Endothelial Growth Factor A
  • vasodilator-stimulated phosphoprotein
  • Cyclic AMP-Dependent Protein Kinases