A Lipid Transfer Protein Signaling Axis Exerts Dual Control of Cell-Cycle and Membrane Trafficking Systems

Dev Cell. 2018 Feb 5;44(3):378-391.e5. doi: 10.1016/j.devcel.2017.12.026. Epub 2018 Jan 27.

Abstract

Kes1/Osh4 is a member of the conserved, but functionally enigmatic, oxysterol binding protein-related protein (ORP) superfamily that inhibits phosphatidylinositol transfer protein (Sec14)-dependent membrane trafficking through the trans-Golgi (TGN)/endosomal network. We now report that Kes1, and select other ORPs, execute cell-cycle control activities as functionally non-redundant inhibitors of the G1/S transition when cells confront nutrient-poor environments and promote replicative aging. Kes1-dependent cell-cycle regulation requires the Greatwall/MASTL kinase ortholog Rim15, and is opposed by Sec14 activity in a mechanism independent of Kes1/Sec14 bulk membrane-trafficking functions. Moreover, the data identify Kes1 as a non-histone target for NuA4 through which this lysine acetyltransferase co-modulates membrane-trafficking and cell-cycle activities. We propose the Sec14/Kes1 lipid-exchange protein pair constitutes part of the mechanism for integrating TGN/endosomal lipid signaling with cell-cycle progression and hypothesize that ORPs define a family of stage-specific cell-cycle control factors that execute tumor-suppressor-like functions.

Keywords: ORPs; PITPs; aging; cell cycle; lipid exchange proteins; lipid signaling; lysine acetyltransferase; phosphoinositides.

Publication types

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

MeSH terms

  • Biological Transport
  • Cell Cycle / physiology*
  • Cell Membrane / metabolism*
  • Cell Movement
  • Endosomes
  • Golgi Apparatus / metabolism*
  • Histone Acetyltransferases / metabolism*
  • Lipids / analysis
  • Lipids / physiology*
  • Membrane Proteins / metabolism*
  • Phospholipid Transfer Proteins / metabolism*
  • Receptors, Steroid / metabolism*
  • Saccharomyces cerevisiae / growth & development
  • Saccharomyces cerevisiae / metabolism*
  • Saccharomyces cerevisiae Proteins / metabolism*
  • Signal Transduction

Substances

  • KES1 protein, S cerevisiae
  • Lipids
  • Membrane Proteins
  • Phospholipid Transfer Proteins
  • Receptors, Steroid
  • SEC14 protein, S cerevisiae
  • Saccharomyces cerevisiae Proteins
  • Histone Acetyltransferases
  • NuA4 protein, S cerevisiae