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Structure-based Discovery of Conformationally Selective Inhibitors of the Serotonin Transporter

Isha Singh, Anubha Seth, Christian B. Billesbølle, Joao Braz, Ramona M. Rodriguiz, Kasturi Roy, Bethlehem Bekele, Veronica Craik, Xi-Ping Huang, Danila Boytsov, Parnian Lak, Henry O’donnell, Walter Sandtner, Bryan L. Roth, Allan I. Basbaum, William C. Wetsel, Aashish Manglik, Brian K. Shoichet, Gary Rudnick

bioRxiv Preprint Server June 13, 2022 preprint DOI: 10.1101/2022.06.13.495991 via bioRxiv

Summary

The serotonin transporter (SERT) adopts three conformations, and most antidepressants target its outward-open state. Ibogaine, which targets the inward-open state, has an unusual antidepressant profile but is cardiotoxic. Computational docking of over 200 million small molecules against the ibogaine-stabilized inward-open SERT identified 36 top compounds; 13 inhibited SERT with potencies from 29 to 5000 nM. Optimization yielded two inhibitors with Ki values as low as 3 nM that stabilized an outward-closed state and showed little off-target activity. A cryo-EM structure confirmed the predicted binding geometry. In mice, both compounds showed anxiolytic and antidepressant activity with potencies up to 200 times greater than fluoxetine.

Study at a glance

Characteristics Computational docking and experimental validation
Citations 8
Key finding Two novel inhibitors of the serotonin transporter, identified through computational docking and optimization, showed potent, selective activity and up to 200-fold greater antidepressant potency than fluoxetine in mice.

Abstract

The serotonin transporter (SERT) removes synaptic serotonin and is the target of anti-depressant drugs. SERT adopts three conformations: outward-open, occluded, and inward-open. All known inhibitors target the outward-open state except ibogaine, which has an unusual anti-depressant profile and stabilizes the inward-open conformation. Unfortunately, ibogaine is promiscuous and cardiotoxic, limiting understanding of inward-open state ligands. We computationally docked over 200 million small molecules against the ibogaine stabilized inward-open state of SERT. Thirty-six top-ranking compounds were synthesized and thirteen inhibited with potencies ranging from 29 to 5000 nM. Structure-based optimization led to two novel inhibitors with Ki values down to 3 nM. The new molecules stabilized an outward-closed state of the transporter and had little activity against off-targets. A cryo-EM structure of one of these bound to SERT confirmed the predicted geometry. In mouse behavioral assays, both had anxiolytic and anti-depressant activity, with potencies up to 200 better than fluoxetine.

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