Sphingosine kinase 1 is critically involved in nitric oxide-mediated human endothelial cell migration and tube formation

Br J Pharmacol. 2010 Aug;160(7):1641-51. doi: 10.1111/j.1476-5381.2010.00818.x.

Abstract

Background and purpose: Sphingosine kinases (SKs) convert sphingosine to sphingosine 1-phosphate (S1P), which is a bioactive lipid that regulates a variety of cellular processes including proliferation, differentiation and migration.

Experimental approach: We used the human endothelial cell line EA.hy926 to investigate the effect of nitric oxide (NO) donors on SK-1 expression, and on cell migration and tube formation.

Key results: We showed that exposure of EA.hy926 cells to Deta-NO (125-1000 microM) resulted in a time- and concentration-dependent up-regulation of SK-1 mRNA and protein expression, and activity with a first significant effect at 250 microM of Deta-NO. The increased SK-1 mRNA expression resulted from an enhanced SK-1 promoter activity. A similar effect was also seen with various other NO donors. In mechanistic terms, the NO-triggered effect occurred independently of cGMP, but involved the classical mitogen-activated protein kinase cascade because the MEK inhibitor U0126 abolished the NO-induced SK-1 expression. The effect of NO was also markedly reduced by the thiol-reducing agent N-acetylcysteine, suggesting a redox-dependent mechanism. Functionally, Deta-NO triggered an increase in the migration of endothelial cells in an adapted Boyden chamber assay, and also increased endothelial tube formation in a Matrigel assay. These responses were both abolished in cells depleted of SK-1.

Conclusions and implications: These data show that NO donors up-regulate specifically SK-1 expression and activity in human endothelial cells, and SK-1 in turn critically contributes to the migratory capability and tube formation of endothelial cells. Thus, SK-1 may be considered an attractive novel target to interfere with pathological processes involving angiogenesis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Blotting, Western
  • Cell Culture Techniques
  • Cell Line
  • Cell Movement / drug effects*
  • Cyclic GMP / metabolism
  • Dose-Response Relationship, Drug
  • Endothelial Cells / cytology
  • Endothelial Cells / drug effects*
  • Endothelial Cells / enzymology
  • Endothelial Cells / metabolism
  • Humans
  • Luciferases, Firefly / genetics
  • Neovascularization, Physiologic / drug effects*
  • Nitric Oxide / metabolism
  • Nitric Oxide / physiology*
  • Nitric Oxide Donors / pharmacology
  • Phosphotransferases (Alcohol Group Acceptor) / biosynthesis
  • Phosphotransferases (Alcohol Group Acceptor) / genetics
  • Phosphotransferases (Alcohol Group Acceptor) / physiology*
  • RNA, Small Interfering / genetics
  • Reverse Transcriptase Polymerase Chain Reaction
  • Time Factors
  • Transfection
  • Triazenes / pharmacology
  • Up-Regulation

Substances

  • 1-hydroxy-2-oxo-3,3-bis(2-aminoethyl)-1-triazene
  • Nitric Oxide Donors
  • RNA, Small Interfering
  • Triazenes
  • Nitric Oxide
  • Luciferases, Firefly
  • Phosphotransferases (Alcohol Group Acceptor)
  • sphingosine kinase
  • Cyclic GMP