What Contributes to Serotonin-Norepinephrine Reuptake Inhibitors' Dual-Targeting Mechanism? The Key Role of Transmembrane Domain 6 in Human Serotonin and Norepinephrine Transporters Revealed by Molecular Dynamics Simulation

ACS Chem Neurosci. 2018 May 16;9(5):1128-1140. doi: 10.1021/acschemneuro.7b00490. Epub 2018 Jan 24.

Abstract

Dual inhibition of serotonin and norepinephrine transporters (hSERT and hNET) gives greatly improved efficacy and tolerability for treating major depressive disorder (MDD) compared with selective reuptake inhibitors. Pioneer studies provided valuable information on structure, function, and pharmacology of drugs targeting both hSERT and hNET (serotonin-norepinephrine reuptake inhibitors, SNRIs), and the differential binding mechanism between SNRIs and selective inhibitors of 5-HT (SSRIs) or NE (sNRIs) to their corresponding targets was expected to be able to facilitate the discovery of a privileged drug-like scaffold with improved efficacy. However, the dual-target mechanism of SNRIs was still elusive, and the binding mode distinguishing SNRIs from SSRIs and sNRIs was also unclear. Herein, an integrated computational strategy was adopted to discover the binding mode shared by all FDA approved SNRIs. The comparative analysis of binding free energy at the per-residue level discovered that residues Phe335, Leu337, Gly338, and Val343 located at the transmembrane domain 6 (TM6) of hSERT (the corresponding residues Phe317, Leu319, Gly320, and Val325 in hNET) were the determinants accounting for SNRIs' dual-acting inhibition, while residues lining TM3 and 8 (Ile172, Ser438, Thr439, and Leu443 in hSERT; Val148, Ser419, Ser420, and Met424 in hNET) contributed less to the binding of SNRIs than that of SSRIs and sNRIs. Based on these results, the distances between an SNRI's centroid and the centroids of its two aromatic rings (measuring the depth of rings stretching into hydrophobic pockets) were discovered as the key to the SNRIs' dual-targeting mechanism. This finding revealed SNRIs' binding mechanism at an atomistic level, which could be further utilized as structural blueprints for the rational design of privileged drug-like scaffolds treating MDD.

Keywords: Serotonin−norepinephrine reuptake inhibitor; binding mode; dual-target drug; major depressive disorder; molecular dynamics.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Binding Sites / drug effects
  • Depressive Disorder, Major / drug therapy*
  • Humans
  • Molecular Dynamics Simulation
  • Norepinephrine / pharmacology*
  • Norepinephrine Plasma Membrane Transport Proteins / drug effects*
  • Norepinephrine Plasma Membrane Transport Proteins / metabolism
  • Selective Serotonin Reuptake Inhibitors / pharmacology*

Substances

  • Norepinephrine Plasma Membrane Transport Proteins
  • SLC6A2 protein, human
  • Serotonin Uptake Inhibitors
  • Norepinephrine