Identification of a second substrate-binding site in solute-sodium symporters

J Biol Chem. 2015 Jan 2;290(1):127-41. doi: 10.1074/jbc.M114.584383. Epub 2014 Nov 14.

Abstract

The structure of the sodium/galactose transporter (vSGLT), a solute-sodium symporter (SSS) from Vibrio parahaemolyticus, shares a common structural fold with LeuT of the neurotransmitter-sodium symporter family. Structural alignments between LeuT and vSGLT reveal that the crystallographically identified galactose-binding site in vSGLT is located in a more extracellular location relative to the central substrate-binding site (S1) in LeuT. Our computational analyses suggest the existence of an additional galactose-binding site in vSGLT that aligns to the S1 site of LeuT. Radiolabeled galactose saturation binding experiments indicate that, like LeuT, vSGLT can simultaneously bind two substrate molecules under equilibrium conditions. Mutating key residues in the individual substrate-binding sites reduced the molar substrate-to-protein binding stoichiometry to ~1. In addition, the related and more experimentally tractable SSS member PutP (the Na(+)/proline transporter) also exhibits a binding stoichiometry of 2. Targeting residues in the proposed sites with mutations results in the reduction of the binding stoichiometry and is accompanied by severely impaired translocation of proline. Our data suggest that substrate transport by SSS members requires both substrate-binding sites, thereby implying that SSSs and neurotransmitter-sodium symporters share common mechanistic elements in substrate transport.

Keywords: Amino Acid Transport; Computational Biology; Equilibrium Binding; Galactose; Membrane Transport; Molecular Dynamics; Scintillation Proximity Assay; Solute-Sodium Symporter; Structural Alignment; Transporter.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Amino Acid Sequence
  • Amino Acid Transport Systems, Neutral / chemistry*
  • Amino Acid Transport Systems, Neutral / metabolism
  • Binding Sites
  • Biological Transport
  • Escherichia coli / chemistry
  • Escherichia coli / metabolism
  • Escherichia coli Proteins / chemistry*
  • Escherichia coli Proteins / metabolism
  • Galactose / chemistry*
  • Galactose / metabolism
  • Kinetics
  • Molecular Docking Simulation
  • Molecular Dynamics Simulation
  • Molecular Sequence Data
  • Plasma Membrane Neurotransmitter Transport Proteins / chemistry*
  • Plasma Membrane Neurotransmitter Transport Proteins / metabolism
  • Protein Binding
  • Protein Folding
  • Protein Structure, Secondary
  • Protein Structure, Tertiary
  • Recombinant Proteins / chemistry
  • Recombinant Proteins / metabolism
  • Sequence Alignment
  • Sodium / chemistry*
  • Sodium / metabolism
  • Sodium-Glucose Transport Proteins / chemistry*
  • Sodium-Glucose Transport Proteins / metabolism
  • Structural Homology, Protein
  • Substrate Specificity
  • Symporters / chemistry*
  • Symporters / metabolism
  • Thermodynamics
  • Vibrio parahaemolyticus / chemistry
  • Vibrio parahaemolyticus / metabolism

Substances

  • Amino Acid Transport Systems, Neutral
  • Escherichia coli Proteins
  • Plasma Membrane Neurotransmitter Transport Proteins
  • Recombinant Proteins
  • Sodium-Glucose Transport Proteins
  • Symporters
  • PutP protein, E coli
  • Sodium
  • Galactose

Associated data

  • PDB/2A65
  • PDB/3DH4
  • PDB/3TT3