Dynamics of intracellular neonatal Fc receptor-ligand interactions in primary macrophages using biophysical fluorescence techniques

Mol Biol Cell. 2022 Jan 1;33(1):ar6. doi: 10.1091/mbc.E21-02-0061. Epub 2021 Nov 3.

Abstract

The neonatal Fc receptor (FcRn) is responsible for the recycling of endocytosed albumin and IgG, and contributes to their long plasma half-life. We recently identified an FcRn-dependent recycling pathway from macropinosomes in macrophages; however, little is known about the dynamics of intracellular FcRn-ligand interactions to promote recycling. Here we demonstrate a multiplexed biophysical fluorescent microscopy approach to resolve the spatiotemporal dynamics of albumin-FcRn interactions in living bone marrow-derived macrophages (BMDMs). We used the phasor approach to fluorescence lifetime imaging microscopy (FLIM) of Förster resonance energy transfer (FRET) to detect the interaction of a FcRn-mCherry fusion protein with endocytosed Alexa Fluor 488-labeled human serum albumin (HSA-AF488) in BMDMs, and raster image correlation spectroscopy (RICS) analysis of single fluorescent-labeled albumin molecules to monitor the diffusion kinetics of internalized albumin. Our data identified a major fraction of immobile HSA-AF488 molecules in endosomal structures of human FcRn-positive mouse macrophages and an increase in FLIM-FRET following endocytosis, including detection of FRET in tubular-like structures. A nonbinding mutant of albumin showed minimum FLIM-FRET and high mobility. These data reveal the kinetics of FcRn-ligand binding within endosomal structures for recruitment into transport carriers for recycling. These approaches have wide applicability for analyses of intracellular ligand-receptor interactions.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Albumins / metabolism
  • Animals
  • Endocytosis / physiology
  • Endosomes / metabolism
  • Female
  • Fluorescence
  • Fluorescence Resonance Energy Transfer / methods
  • Half-Life
  • HeLa Cells
  • Histocompatibility Antigens Class I / metabolism*
  • Histocompatibility Antigens Class I / physiology
  • Humans
  • Kinetics
  • Ligands
  • Macrophages / metabolism*
  • Male
  • Mice
  • Mice, Knockout
  • Mice, Transgenic
  • Microscopy, Fluorescence / methods
  • Protein Binding
  • Receptors, Fc / metabolism*
  • Receptors, Fc / physiology

Substances

  • Albumins
  • Histocompatibility Antigens Class I
  • Ligands
  • Receptors, Fc
  • Fc receptor, neonatal