The organization of leukotriene biosynthesis on the nuclear envelope revealed by single molecule localization microscopy and computational analyses

PLoS One. 2019 Feb 8;14(2):e0211943. doi: 10.1371/journal.pone.0211943. eCollection 2019.

Abstract

The initial steps in the synthesis of leukotrienes are the translocation of 5-lipoxygenase (5-LO) to the nuclear envelope and its subsequent association with its scaffold protein 5-lipoxygenase-activating protein (FLAP). A major gap in our understanding of this process is the knowledge of how the organization of 5-LO and FLAP on the nuclear envelope regulates leukotriene synthesis. We combined single molecule localization microscopy with Clus-DoC cluster analysis, and also a novel unbiased cluster analysis to analyze changes in the relationships between 5-LO and FLAP in response to activation of RBL-2H3 cells to generate leukotriene C4. We identified the time-dependent reorganization of both 5-LO and FLAP into higher-order assemblies or clusters in response to cell activation via the IgE receptor. Clus-DoC analysis identified a subset of these clusters with a high degree of interaction between 5-LO and FLAP that specifically correlates with the time course of LTC4 synthesis, strongly suggesting their role in the initiation of leukotriene biosynthesis.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • 5-Lipoxygenase-Activating Proteins / chemistry
  • 5-Lipoxygenase-Activating Proteins / genetics
  • 5-Lipoxygenase-Activating Proteins / metabolism*
  • Animals
  • Arachidonate 5-Lipoxygenase / chemistry
  • Arachidonate 5-Lipoxygenase / genetics
  • Arachidonate 5-Lipoxygenase / metabolism*
  • Basophils / cytology
  • Basophils / drug effects
  • Basophils / metabolism*
  • Cell Line, Tumor
  • Cluster Analysis
  • Gene Expression Regulation
  • Immunoglobulin E / genetics
  • Immunoglobulin E / metabolism
  • Immunoglobulin E / pharmacology
  • Leukotriene C4 / biosynthesis*
  • Nuclear Envelope / drug effects
  • Nuclear Envelope / genetics
  • Nuclear Envelope / metabolism*
  • Nuclear Envelope / ultrastructure
  • Protein Binding
  • Rats
  • Receptors, IgE / genetics
  • Receptors, IgE / metabolism
  • Signal Transduction
  • Single Molecule Imaging

Substances

  • 5-Lipoxygenase-Activating Proteins
  • Alox5ap protein, rat
  • FCER1A protein, rat
  • Receptors, IgE
  • Leukotriene C4
  • Immunoglobulin E
  • Arachidonate 5-Lipoxygenase