Membrane translocation of TRPC6 channels and endothelial migration are regulated by calmodulin and PI3 kinase activation

Proc Natl Acad Sci U S A. 2016 Feb 23;113(8):2110-5. doi: 10.1073/pnas.1600371113. Epub 2016 Feb 8.

Abstract

Lipid oxidation products, including lysophosphatidylcholine (lysoPC), activate canonical transient receptor potential 6 (TRPC6) channels leading to inhibition of endothelial cell (EC) migration in vitro and delayed EC healing of arterial injuries in vivo. The precise mechanism through which lysoPC activates TRPC6 channels is not known, but calmodulin (CaM) contributes to the regulation of TRPC channels. Using site-directed mutagenesis, cDNAs were generated in which Tyr(99) or Tyr(138) of CaM was replaced with Phe, generating mutant CaM, Phe(99)-CaM, or Phe(138)-CaM, respectively. In ECs transiently transfected with pcDNA3.1-myc-His-Phe(99)-CaM, but not in ECs transfected with pcDNA3.1-myc-His-Phe(138)-CaM, the lysoPC-induced TRPC6-CaM dissociation and TRPC6 externalization was disrupted. Also, the lysoPC-induced increase in intracellular calcium concentration was inhibited in ECs transiently transfected with pcDNA3.1-myc-His-Phe(99)-CaM. Blocking phosphorylation of CaM at Tyr(99) also reduced CaM association with the p85 subunit and subsequent activation of phosphatidylinositol 3-kinase (PI3K). This prevented the increase in phosphatidylinositol (3,4,5)-trisphosphate (PIP3) and the translocation of TRPC6 to the cell membrane and reduced the inhibition of EC migration by lysoPC. These findings suggest that lysoPC induces CaM phosphorylation at Tyr(99) by a Src family kinase and that phosphorylated CaM activates PI3K to produce PIP3, which promotes TRPC6 translocation to the cell membrane.

Keywords: PI3 kinase; TRPC6; calmodulin; endothelial.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, N.I.H., Intramural

MeSH terms

  • Animals
  • Calcium / metabolism
  • Calcium Signaling / physiology*
  • Calmodulin / genetics
  • Calmodulin / metabolism*
  • Cattle
  • Cell Membrane / genetics
  • Cell Membrane / metabolism*
  • Cell Movement / physiology*
  • Endothelial Cells / cytology
  • Endothelial Cells / metabolism*
  • Enzyme Activation / physiology
  • Humans
  • Lysophosphatidylcholines / genetics
  • Lysophosphatidylcholines / metabolism
  • Phosphatidylinositol 3-Kinases / genetics
  • Phosphatidylinositol 3-Kinases / metabolism*
  • Protein Transport / physiology
  • TRPC Cation Channels / genetics
  • TRPC Cation Channels / metabolism*
  • TRPC6 Cation Channel

Substances

  • Calmodulin
  • Lysophosphatidylcholines
  • TRPC Cation Channels
  • TRPC6 Cation Channel
  • TRPC6 protein, human
  • Phosphatidylinositol 3-Kinases
  • Calcium