Sphingolipid metabolic flow controls phosphoinositide turnover at the trans-Golgi network

EMBO J. 2017 Jun 14;36(12):1736-1754. doi: 10.15252/embj.201696048. Epub 2017 May 10.

Abstract

Sphingolipids are membrane lipids globally required for eukaryotic life. The sphingolipid content varies among endomembranes with pre- and post-Golgi compartments being poor and rich in sphingolipids, respectively. Due to this different sphingolipid content, pre- and post-Golgi membranes serve different cellular functions. The basis for maintaining distinct subcellular sphingolipid levels in the presence of membrane trafficking and metabolic fluxes is only partially understood. Here, we describe a homeostatic regulatory circuit that controls sphingolipid levels at the trans-Golgi network (TGN). Specifically, we show that sphingomyelin production at the TGN triggers a signalling pathway leading to PtdIns(4)P dephosphorylation. Since PtdIns(4)P is required for cholesterol and sphingolipid transport to the trans-Golgi network, PtdIns(4)P consumption interrupts this transport in response to excessive sphingomyelin production. Based on this evidence, we envisage a model where this homeostatic circuit maintains a constant lipid composition in the trans-Golgi network and post-Golgi compartments, thus counteracting fluctuations in the sphingolipid biosynthetic flow.

Keywords: PtdIns(4)P; ceramide; lipid territories; lipid‐transfer protein; membrane contact sites.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, N.I.H., Extramural

MeSH terms

  • HeLa Cells
  • Homeostasis
  • Humans
  • Models, Biological
  • Phosphatidylinositols / metabolism*
  • Sphingolipids / metabolism*
  • trans-Golgi Network / metabolism*

Substances

  • Phosphatidylinositols
  • Sphingolipids