Allosteric gate modulation confers K+ coupling in glutamate transporters

EMBO J. 2019 Oct 1;38(19):e101468. doi: 10.15252/embj.2019101468. Epub 2019 Sep 10.

Abstract

Excitatory amino acid transporters (EAATs) mediate glial and neuronal glutamate uptake to terminate synaptic transmission and to ensure low resting glutamate concentrations. Effective glutamate uptake is achieved by cotransport with 3 Na+ and 1 H+ , in exchange with 1 K+ . The underlying principles of this complex transport stoichiometry remain poorly understood. We use molecular dynamics simulations and electrophysiological experiments to elucidate how mammalian EAATs harness K+ gradients, unlike their K+ -independent prokaryotic homologues. Glutamate transport is achieved via elevator-like translocation of the transport domain. In EAATs, glutamate-free re-translocation is prevented by an external gate remaining open until K+ binding closes and locks the gate. Prokaryotic GltPh contains the same K+ -binding site, but the gate can close without K+ . Our study provides a comprehensive description of K+ -dependent glutamate transport and reveals a hitherto unknown allosteric coupling mechanism that permits adaptions of the transport stoichiometry without affecting ion or substrate binding.

Keywords: K+ binding; allosteric coupling; excitatory amino acid transporters; secondary active transport; transport stoichiometry.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Allosteric Regulation
  • Biological Transport
  • Glutamate Plasma Membrane Transport Proteins / chemistry*
  • Glutamate Plasma Membrane Transport Proteins / metabolism*
  • HEK293 Cells
  • Humans
  • Models, Molecular
  • Molecular Dynamics Simulation
  • Potassium / metabolism*
  • Protein Conformation
  • Synaptic Transmission

Substances

  • Glutamate Plasma Membrane Transport Proteins
  • Potassium