Nanoscale Landscape of Phosphoinositides Revealed by Specific Pleckstrin Homology (PH) Domains Using Single-molecule Superresolution Imaging in the Plasma Membrane

J Biol Chem. 2015 Nov 6;290(45):26978-26993. doi: 10.1074/jbc.M115.663013. Epub 2015 Sep 22.

Abstract

Both phosphatidylinositol 4-phosphate (PI4P) and phosphatidylinositol 4,5-bisphosphate (PI(4,5)P2) are independent plasma membrane (PM) determinant lipids that are essential for multiple cellular functions. However, their nanoscale spatial organization in the PM remains elusive. Using single-molecule superresolution microscopy and new photoactivatable fluorescence probes on the basis of pleckstrin homology domains that specifically recognize phosphatidylinositides in insulin-secreting INS-1 cells, we report that the PI(4,5)P2 probes exhibited a remarkably uniform distribution in the major regions of the PM, with some sparse PI(4,5)P2-enriched membrane patches/domains of diverse sizes (383 ± 14 nm on average). Quantitative analysis revealed a modest concentration gradient that was much less steep than previously thought, and no densely packed PI(4,5)P2 nanodomains were observed. Live-cell superresolution imaging further demonstrated the dynamic structural changes of those domains in the flat PM and membrane protrusions. PI4P and phosphatidylinositol (3,4,5)-trisphosphate (PI(3,4,5)P3) showed similar spatial distributions as PI(4,5)P2. These data reveal the nanoscale landscape of key inositol phospholipids in the native PM and imply a framework for local cellular signaling and lipid-protein interactions at a nanometer scale.

Keywords: SNARE proteins; inositol phospholipid; membrane lipid; metabolism; phosphatidylinositol; superresolution microscopy; β cell (B cell).

Publication types

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

MeSH terms

  • Animals
  • COS Cells
  • Cell Line
  • Cell Membrane / metabolism
  • Cell Membrane / ultrastructure
  • Chlorocebus aethiops
  • Insulin-Secreting Cells / metabolism
  • Insulin-Secreting Cells / ultrastructure
  • Luminescent Proteins / metabolism
  • Membrane Proteins / chemistry*
  • Membrane Proteins / metabolism*
  • Microtubules / metabolism
  • Nanotechnology
  • Phosphatidylinositol 4,5-Diphosphate / metabolism
  • Phosphatidylinositol Phosphates / metabolism
  • Phosphatidylinositols / metabolism*
  • Protein Structure, Tertiary
  • Rats
  • Signal Transduction
  • Syntaxin 1 / metabolism

Substances

  • Luminescent Proteins
  • Membrane Proteins
  • Phosphatidylinositol 4,5-Diphosphate
  • Phosphatidylinositol Phosphates
  • Phosphatidylinositols
  • Stx1a protein, rat
  • Syntaxin 1
  • phosphatidylinositol 3,4,5-triphosphate
  • phosphatidylinositol 4-phosphate