Sphingosine-1-phosphate-induced Flk-1 transactivation stimulates mouse embryonic stem cell proliferation through S1P1/S1P3-dependent β-arrestin/c-Src pathways

Stem Cell Res. 2014 Jan;12(1):69-85. doi: 10.1016/j.scr.2013.08.013. Epub 2013 Sep 7.

Abstract

Although recent findings showed that the bioactive lipid metabolites can regulate the ES cell functions, the physiological relevance of interaction between sphingosine-1-phosphate (S1P) and Flk-1 and its related signaling molecules are not yet clear in ES cell proliferation. In the present study, S1P1-5 receptors were expressed in mouse ES cells and S1P increased S1P1-3 receptor expression level. S1P treatment stimulated the cellular proliferation in S1P1/3-dependent manner, located in lipid rafts. In response to S1P, β-arrestin was recruited to S1P1/3 receptor and c-Src was activated. S1P also increased the binding of S1P1/3 receptor with Flk-1. Similar to responses for VEGF, S1P increased Flk-1 phosphorylation, which was blocked by β-arrestin siRNA, and PP2, but not by VEGF-A164 antibody or VEGF siRNA. In addition, S1P induced VEGF expression and VEGFR2 kinase inhibitor (SU1498) blocked the S1P-induced cellular proliferation. However, VEGF-A164 antibody or VEGF siRNA partially blocked S1P-induced cellular proliferation, suggesting that both VEGF-dependent Flk-1 activation and VEGF-independent Flk-1 activation are involved in S1P-induced ES cell proliferation. S1P and VEGF-induced phosphorylation of ERK and JNK were blocked by pretreatment with SU1498. Moreover, inhibition of ERK and JNK blocked S1P-induced cellular proliferation. In conclusion, S1P-elicited transactivation of Flk-1 mediated by S1P1/3-dependent β-arrestin/c-Src pathways stimulated mouse ES cell proliferation.

Keywords: CDK; CLM; Cholesterol-loaded MβCD.; Cyclin dependent kinase; ERK; ESC; Embryonic stem cell; Extracellular signal-regulated kinases; Fetal Liver Kinase 1; Flk-1; JNK; Methyl-β-cyclodextrin; MβCD; RTK; Receptor tyrosine kinase; S1P; Sphingosine-1-phosphate; VEGF; Vascular endothelial growth factor; c-Jun N-terminal kinases.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antibodies / immunology
  • Arrestins / antagonists & inhibitors
  • Arrestins / genetics
  • Arrestins / metabolism*
  • CSK Tyrosine-Protein Kinase
  • Cell Line
  • Cell Proliferation
  • Embryonic Stem Cells / cytology*
  • Embryonic Stem Cells / metabolism
  • Extracellular Signal-Regulated MAP Kinases / antagonists & inhibitors
  • Extracellular Signal-Regulated MAP Kinases / metabolism
  • JNK Mitogen-Activated Protein Kinases / antagonists & inhibitors
  • JNK Mitogen-Activated Protein Kinases / metabolism
  • Lysophospholipids / genetics
  • Lysophospholipids / metabolism*
  • Mice
  • Phosphorylation
  • Protein Binding
  • RNA Interference
  • Receptors, Lysosphingolipid / genetics
  • Receptors, Lysosphingolipid / metabolism*
  • Sphingosine / analogs & derivatives*
  • Sphingosine / genetics
  • Sphingosine / metabolism
  • Sphingosine-1-Phosphate Receptors
  • Transcriptional Activation* / genetics
  • Vascular Endothelial Growth Factor A / antagonists & inhibitors
  • Vascular Endothelial Growth Factor A / immunology
  • Vascular Endothelial Growth Factor A / metabolism
  • Vascular Endothelial Growth Factor Receptor-2 / genetics
  • Vascular Endothelial Growth Factor Receptor-2 / metabolism*
  • beta-Arrestins
  • src-Family Kinases / metabolism*

Substances

  • Antibodies
  • Arrestins
  • Lysophospholipids
  • Receptors, Lysosphingolipid
  • S1pr3 protein, mouse
  • Sphingosine-1-Phosphate Receptors
  • Vascular Endothelial Growth Factor A
  • beta-Arrestins
  • sphingosine 1-phosphate
  • Vascular Endothelial Growth Factor Receptor-2
  • CSK Tyrosine-Protein Kinase
  • src-Family Kinases
  • Extracellular Signal-Regulated MAP Kinases
  • JNK Mitogen-Activated Protein Kinases
  • Sphingosine