Sphingosine-1-phosphate signaling modulates terminal erythroid differentiation through the regulation of mitophagy

Exp Hematol. 2019 Apr:72:47-59.e1. doi: 10.1016/j.exphem.2019.01.004. Epub 2019 Jan 16.

Abstract

Erythropoiesis is a highly coordinated stepwise process involving the progressive clearance of mitochondria via mitophagy. Based on the expression of several macroautophagy and mitophagy specific genes, we identified a sequential change in the transcriptional pattern during terminal erythroid differentiation. Because erythroid cells are a major source of serum sphingosine-1-phosphate, we analyzed the role of sphingolipid signaling in erythropoiesis and demonstrate that sphingosine kinase activity promotes terminal erythroid differentiation by regulating the expression of key mitophagy genes Pink1 and Bnip3l/Nix. Sphingosine kinase 1 (Sphk1) inhibition also disrupted Pink1-p62 mediated mitochondria clearance in late erythroblasts. Notably, we show that supplementing sphingosine-1-phosphate in vitro can promote erythroid differentiation. Our study clarifies the role of sphingolipid signaling in regulating mitophagy during terminal erythroid differentiation and highlights the potential utility of modulating sphingolipid signaling to facilitate the large-scale production of transfusable red blood cells.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Differentiation / physiology*
  • Erythropoiesis / physiology*
  • Lysophospholipids / genetics
  • Lysophospholipids / metabolism*
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism
  • Mice
  • Mice, Transgenic
  • Mitophagy / physiology*
  • Phosphotransferases (Alcohol Group Acceptor) / genetics
  • Phosphotransferases (Alcohol Group Acceptor) / metabolism
  • Protein Kinases / genetics
  • Protein Kinases / metabolism
  • Proto-Oncogene Proteins / genetics
  • Proto-Oncogene Proteins / metabolism
  • Signal Transduction / physiology*
  • Sphingosine / analogs & derivatives*
  • Sphingosine / genetics
  • Sphingosine / metabolism
  • Tumor Suppressor Proteins / genetics
  • Tumor Suppressor Proteins / metabolism

Substances

  • BNIP3 protein, human
  • BNIP3L protein, human
  • Lysophospholipids
  • Membrane Proteins
  • Proto-Oncogene Proteins
  • Tumor Suppressor Proteins
  • sphingosine 1-phosphate
  • Protein Kinases
  • Phosphotransferases (Alcohol Group Acceptor)
  • sphingosine kinase
  • PTEN-induced putative kinase
  • Sphingosine