PCYT1A Regulates Phosphatidylcholine Homeostasis from the Inner Nuclear Membrane in Response to Membrane Stored Curvature Elastic Stress

Dev Cell. 2018 May 21;45(4):481-495.e8. doi: 10.1016/j.devcel.2018.04.012. Epub 2018 May 10.

Abstract

Cell and organelle membranes consist of a complex mixture of phospholipids (PLs) that determine their size, shape, and function. Phosphatidylcholine (PC) is the most abundant phospholipid in eukaryotic membranes, yet how cells sense and regulate its levels in vivo remains unclear. Here we show that PCYT1A, the rate-limiting enzyme of PC synthesis, is intranuclear and re-locates to the nuclear membrane in response to the need for membrane PL synthesis in yeast, fly, and mammalian cells. By aligning imaging with lipidomic analysis and data-driven modeling, we demonstrate that yeast PCYT1A membrane association correlates with membrane stored curvature elastic stress estimates. Furthermore, this process occurs inside the nucleus, although nuclear localization signal mutants can compensate for the loss of endogenous PCYT1A in yeast and in fly photoreceptors. These data suggest an ancient mechanism by which nucleoplasmic PCYT1A senses surface PL packing defects on the inner nuclear membrane to control PC homeostasis.

Keywords: CCT; Kennedy pathway; PCYT1A; lipidomics; phosphatidylcholine; stored curvature elastic stress.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Membrane / chemistry*
  • Cell Membrane / metabolism
  • Cell Nucleus / chemistry*
  • Cell Nucleus / metabolism
  • Choline-Phosphate Cytidylyltransferase / genetics
  • Choline-Phosphate Cytidylyltransferase / metabolism*
  • Drosophila melanogaster / genetics
  • Drosophila melanogaster / growth & development
  • Drosophila melanogaster / metabolism
  • Elasticity*
  • Homeostasis
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Models, Biological
  • Nuclear Envelope / chemistry*
  • Nuclear Envelope / genetics
  • Nuclear Envelope / metabolism
  • Phosphatidylcholines / metabolism*
  • Saccharomyces cerevisiae / genetics
  • Saccharomyces cerevisiae / growth & development
  • Saccharomyces cerevisiae / metabolism
  • Stress, Physiological*

Substances

  • Phosphatidylcholines
  • Choline-Phosphate Cytidylyltransferase
  • Pcyt1a protein, mouse