WNK1 protein kinase regulates embryonic cardiovascular development through the OSR1 signaling cascade

J Biol Chem. 2013 Mar 22;288(12):8566-8574. doi: 10.1074/jbc.M113.451575. Epub 2013 Feb 5.

Abstract

WNK1 is a widely expressed serine/threonine protein kinase that regulates multiple cellular and organ functions via diverse mechanisms. We previously reported that endothelial-specific deletion of Wnk1 in mice results in embryonic lethality, with angiogenesis and cardiac defects beginning at embryonic day ∼10.5. Here, we further investigated the signaling mechanism by which WNK1 regulates embryonic cardiovascular development. We found that mice with a global deletion of Osr1, which encodes oxidative stress-responsive kinase-1, a protein kinase activated by WNK1, died in utero beginning at embryonic day ∼11. The defects in Osr1-null yolk sacs and embryos were virtually identical to those observed in Wnk1-knock-out mice: no mature large vessels in yolk sacs, defective angiogenesis in the brain and intersomitic vessels, and smaller chambers and reduced myocardial trabeculation in mutant hearts. Endothelial-specific deletion of Osr1 generated by crossing Osr1(flox/flox) mice with Tie2-Cre mice phenocopied defects caused by global Osr1 deletion. To investigate whether OSR1 acts downstream of WNK1 in embryonic angiogenesis, we generated a mouse line that carries a catalytically and constitutively active human OSR1 transgene in the ROSA26 locus under the control of a cassette of floxed transcription stop codons. We found that endothelial-specific expression of the constitutively active mutant OSR1, generated by Tie2-Cre-mediated excision of floxed stop codons in the mutated ROSA26 locus, rescued angiogenesis and cardiac defects in global Wnk1-null embryos. These results indicate that WNK1 activation of the OSR1 signaling cascade is an essential pathway that regulates angiogenesis and cardiac formation during mouse embryo development.

Publication types

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

MeSH terms

  • Alleles
  • Animals
  • Cardiovascular Abnormalities / embryology
  • Cardiovascular Abnormalities / genetics
  • Cardiovascular System / embryology
  • Cardiovascular System / enzymology
  • Cardiovascular System / pathology
  • Embryo, Mammalian / blood supply
  • Embryo, Mammalian / metabolism
  • Embryo, Mammalian / pathology
  • Female
  • Gene Expression Regulation
  • Genes, Lethal
  • Heart / embryology*
  • Humans
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Minor Histocompatibility Antigens
  • Neovascularization, Physiologic
  • Platelet Endothelial Cell Adhesion Molecule-1 / metabolism
  • Protein Serine-Threonine Kinases / biosynthesis
  • Protein Serine-Threonine Kinases / genetics
  • Protein Serine-Threonine Kinases / metabolism*
  • Protein Serine-Threonine Kinases / physiology*
  • Signal Transduction
  • WNK Lysine-Deficient Protein Kinase 1

Substances

  • Minor Histocompatibility Antigens
  • Platelet Endothelial Cell Adhesion Molecule-1
  • OXSR1 protein, human
  • OXSR1 protein, mouse
  • Protein Serine-Threonine Kinases
  • WNK Lysine-Deficient Protein Kinase 1
  • Wnk1 protein, mouse