Sphinganine-1-phosphate attenuates both hepatic and renal injury induced by hepatic ischemia and reperfusion in mice

Shock. 2010 Jan;33(1):31-42. doi: 10.1097/SHK.0b013e3181c02c1f.

Abstract

Hepatic ischemia/reperfusion (I/R) injury is a major complication after liver transplantation, major hepatic resection, or prolonged portal vein occlusion. Furthermore, acute kidney injury is frequent after hepatic I/R and greatly increases postoperative complications. Sphinganine-1-phosphate is a sphingolipid with uncharacterized physiological effects. We serendipitously determined that plasma levels of sphinganine-1-phosphate fell significantly after liver I/R in mice. In this study, we hypothesized that repletion of plasma sphinganine-1-phosphate would protect against liver and kidney injuries after liver I/R. C57BL/6 mice were subjected to 60 min of partial hepatic I/R and treated with either vehicle or with sphinganine-1-phosphate (given immediately before and 2 h after reperfusion). Vehicle-treated mice subjected to liver I/R developed acute liver and kidney injuries with elevated plasma alanine aminotransferase and creatinine 5 and 24 h after liver I/R. However, liver and kidney injuries were significantly attenuated with sphinganine-1-phosphate treatment. Sphinganine-1-phosphate markedly inhibited liver and kidney necrosis and apoptosis 24 h after liver I/R. Moreover, sphinganine-1-phosphate attenuated neutrophil infiltration, reduced plasma IL-6 and TNF-alpha upregulation, and preserved liver and kidney vascular integrity while reducing liver and kidney F-actin degradation after liver I/R. Finally, sphinganine-1-phosphate-mediated hepatic and renal protection was blocked by VPC23019, an antagonist for sphingosine-1-phosphate type 1 receptor. Therefore, sphinganine-1-phosphate improves acute liver and kidney injuries after hepatic I/R via sphingosine-1-phosphate type 1 receptor-mediated inhibition of necrosis and apoptosis and by improving vascular integrity. Harnessing the mechanisms of cytoprotection with sphinganine-1-phosphate activation may lead to new therapies for perioperative hepatic I/R injury and subsequent remote organ injury.

Publication types

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

MeSH terms

  • Actins / metabolism
  • Animals
  • Apoptosis / drug effects
  • Dose-Response Relationship, Drug
  • Enzyme-Linked Immunosorbent Assay
  • Interleukin-6 / blood
  • Kidney / drug effects*
  • Kidney / metabolism
  • Kidney / pathology*
  • Liver / drug effects*
  • Liver / metabolism
  • Liver / pathology*
  • Lysophospholipids / blood
  • Lysophospholipids / therapeutic use*
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Neutrophil Infiltration / drug effects
  • Receptors, Lysosphingolipid / agonists
  • Receptors, Lysosphingolipid / blood
  • Reperfusion Injury / blood
  • Reperfusion Injury / drug therapy*
  • Reperfusion Injury / pathology
  • Sphingosine / analogs & derivatives*
  • Sphingosine / blood
  • Sphingosine / therapeutic use
  • Tumor Necrosis Factor-alpha / blood

Substances

  • Actins
  • Interleukin-6
  • Lysophospholipids
  • Receptors, Lysosphingolipid
  • Tumor Necrosis Factor-alpha
  • sphingosine 1-phosphate
  • Sphingosine