The N terminus of monoamine transporters is a lever required for the action of amphetamines

Author(s)
Sonja Sucic, Stefan Dallinger, Barbara Zdrazil, Rene Weissensteiner, Trine Nygaard Jorgensen, Marion Holy, Oliver Kudlacek, Stefan Seidel, Joo Hee Cha, Ulrik Gether, Amy H. Newman, Gerhard Ecker, Michael Freissmuth, Harald H. Sitte
Abstract

The serotonin transporter (SERT) terminates neurotransmission by removing serotonin from the synaptic cleft. In addition, it is the site of action of antidepressants (which block the transporter) and of amphetamines (which induce substrate efflux). We explored the functional importance of the N terminus in mediating the action of amphetamines by focusing initially on the highly conserved threonine residue at position 81, a candidate site for phosphorylation by protein kinase C. Molecular dynamics simulations of the wild type SERT, compared with its mutations SERTT81A and SERTT81D, suggested structural changes in the inner vestibule indicative of an opening of the inner vestibule. Predictions from this model (e. g. the preferential accumulation of SERTT81A in the inward conformation, its reduced turnover number, and a larger distance between its N and C termini) were verified. Most importantly, SERTT81A (and the homologous mutations in noradrenaline and dopamine) failed to support amphetamine-induced efflux, and this was not remedied by aspartate at this position. Amphetamine-induced currents through SERTT81A were comparable with those through the wild type transporter. Both abundant Na+ entry and accumulation of SERTT81A in the inward facing conformation ought to favor amphetamine-induced efflux. Thus, we surmised that the N terminus must play a direct role in driving the transporter into a state that supports amphetamine-induced efflux. This hypothesis was verified by truncating the first 64 amino acids and by tethering the N terminus to an additional transmembrane helix. Either modification abolished amphetamine-induced efflux. We therefore conclude that the N terminus of monoamine transporters acts as a lever that sustains reverse transport.

Organisation(s)
Department of Biochemistry and Cell Biology
External organisation(s)
Medizinische Universität Wien, Technical University of Denmark (DTU), Seoul National University (SNU), University of Baltimore
Journal
Journal of Biological Chemistry
Volume
285
Pages
10924-10938
No. of pages
15
ISSN
0021-9258
DOI
https://doi.org/10.1074/jbc.M109.083154
Publication date
2010
Peer reviewed
Yes
Austrian Fields of Science 2012
301201 Pharmaceutical and drug analysis
Portal url
https://ucrisportal.univie.ac.at/en/publications/369cf26f-63ef-4dea-bac3-4019888f88c1