Molecular determinants for selective recognition of antidepressants in the human serotonin and norepinephrine transporters

Proc Natl Acad Sci U S A. 2011 Jul 19;108(29):12137-42. doi: 10.1073/pnas.1103060108. Epub 2011 Jul 5.

Abstract

Inhibitors of the serotonin transporter (SERT) and norepinephrine transporter (NET) are widely used in the treatment of major depressive disorder. Although SERT/NET selectivity is a key determinant for the therapeutic properties of these drugs, the molecular determinants defining SERT/NET selectivity are poorly understood. In this study, the structural basis for selectivity of the SERT selective inhibitor citalopram and the structurally closely related NET selective inhibitor talopram is delineated. A systematic structure-activity relationship study allowed identification of the substituents that control activity and selectivity toward SERT and NET and revealed a common pattern showing that SERT and NET have opposite preference for the stereochemical configuration of these inhibitors. Mutational analysis of nonconserved SERT/NET residues within the central substrate binding site was performed to determine the molecular basis for inhibitor selectivity. Changing only five residues in NET to the complementary residues in SERT transferred a SERT-like affinity profile for R- and S-citalopram into NET, showing that the selectivity of these compounds is determined by amino acid differences in the central binding site of the transporters. In contrast, the activity of R- and S-talopram was largely unaffected by any mutations within the central substrate binding site of SERT and NET and in the outer vestibule of NET, suggesting that citalopram and talopram bind to distinct sites on SERT and NET. Together, these findings provide important insight into the molecular basis for SERT/NET selectivity of antidepressants, which can be used to guide rational development of unique transporter inhibitors with fine-tuned transporter selectivity.

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Antidepressive Agents / metabolism*
  • Base Sequence
  • Benzofurans / metabolism
  • Binding Sites / genetics
  • COS Cells
  • Chlorocebus aethiops
  • Citalopram / metabolism
  • Crystallization
  • DNA Mutational Analysis
  • Genetic Vectors / genetics
  • Humans
  • Models, Molecular*
  • Molecular Sequence Data
  • Norepinephrine Plasma Membrane Transport Proteins / antagonists & inhibitors
  • Norepinephrine Plasma Membrane Transport Proteins / chemistry
  • Norepinephrine Plasma Membrane Transport Proteins / genetics*
  • Norepinephrine Plasma Membrane Transport Proteins / metabolism*
  • Propylamines / metabolism
  • Radioligand Assay
  • Selective Serotonin Reuptake Inhibitors / metabolism*
  • Serotonin Plasma Membrane Transport Proteins / chemistry
  • Serotonin Plasma Membrane Transport Proteins / genetics*
  • Serotonin Plasma Membrane Transport Proteins / metabolism*
  • Structure-Activity Relationship

Substances

  • Antidepressive Agents
  • Benzofurans
  • Norepinephrine Plasma Membrane Transport Proteins
  • Propylamines
  • SLC6A2 protein, human
  • Serotonin Plasma Membrane Transport Proteins
  • Serotonin Uptake Inhibitors
  • Citalopram
  • talopram