Substrate-dependent proton antiport in neurotransmitter:sodium symporters

Nat Chem Biol. 2010 Feb;6(2):109-16. doi: 10.1038/nchembio.284. Epub 2009 Dec 27.

Abstract

Neurotransmitter-sodium symporters (NSS), targets for psychostimulants and therapeutic drugs, have a critical role in neurotransmission. Whereas eukaryotic NSS show chloride-dependent transport, bacterial NSS feature Cl(-)-independent substrate transport. Recently we showed that mutation of an acidic residue near one of the sodium ion-binding sites in LeuT of Aquifex aeolicus or Tyt1 of Fusobacterium nucleatum renders substrate binding and/or transport Cl(-) dependent. We reasoned that the negative charge--provided either by Cl(-) or by the transporter itself--is required for substrate translocation. Here we show that Tyt1 reconstituted in proteoliposomes is strictly dependent on the Na(+) gradient and is stimulated by an inside negative membrane potential and by an inversely oriented proton gradient. Notably, Na(+)/substrate symport elicited H(+) efflux, indicative of Na(+)/substrate symport-coupled H(+) antiport. Mutations that render the transport phenotype Cl(-) dependent essentially abolish the pH dependence. We propose unifying features of charge balance by all NSS members with similar mechanistic features but different molecular solutions.

Publication types

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

MeSH terms

  • Antiporters / chemistry
  • Antiporters / metabolism*
  • Bacillus / chemistry
  • Bacillus / metabolism*
  • Binding Sites
  • Fusobacterium nucleatum / chemistry
  • Fusobacterium nucleatum / metabolism*
  • Hydrogen-Ion Concentration
  • Membrane Potentials
  • Models, Molecular
  • Plasma Membrane Neurotransmitter Transport Proteins / chemistry
  • Plasma Membrane Neurotransmitter Transport Proteins / metabolism*
  • Protein Structure, Quaternary
  • Substrate Specificity

Substances

  • Antiporters
  • Plasma Membrane Neurotransmitter Transport Proteins