Control of AMPA receptor activity by the extracellular loops of auxiliary proteins

Elife. 2017 Aug 30:6:e28680. doi: 10.7554/eLife.28680.

Abstract

At synapses throughout the mammalian brain, AMPA receptors form complexes with auxiliary proteins, including TARPs. However, how TARPs modulate AMPA receptor gating remains poorly understood. We built structural models of TARP-AMPA receptor complexes for TARPs γ2 and γ8, combining recent structural studies and de novo structure predictions. These models, combined with peptide binding assays, provide evidence for multiple interactions between GluA2 and variable extracellular loops of TARPs. Substitutions and deletions of these loops had surprisingly rich effects on the kinetics of glutamate-activated currents, without any effect on assembly. Critically, by altering the two interacting loops of γ2 and γ8, we could entirely remove all allosteric modulation of GluA2, without affecting formation of AMPA receptor-TARP complexes. Likewise, substitutions in the linker domains of GluA2 completely removed any effect of γ2 on receptor kinetics, indicating a dominant role for this previously overlooked site proximal to the AMPA receptor channel gate.

Keywords: biophysics; desensitization; glutamate; modulation; neuroscience; none; receptor kinetics; structural biology; superactivation.

MeSH terms

  • Allosteric Regulation
  • Amino Acid Substitution
  • Animals
  • Calcium Channels / chemistry*
  • Calcium Channels / genetics
  • Calcium Channels / metabolism*
  • DNA Mutational Analysis
  • Mice
  • Models, Biological
  • Models, Molecular
  • Protein Binding
  • Receptors, AMPA / chemistry*
  • Receptors, AMPA / metabolism*
  • Sequence Deletion

Substances

  • Cacng2 protein, mouse
  • Calcium Channels
  • Receptors, AMPA
  • TARP gamma-8 protein, mouse
  • glutamate receptor ionotropic, AMPA 2