Structural basis of subunit selectivity for competitive NMDA receptor antagonists with preference for GluN2A over GluN2B subunits
Abstract
NMDA-type glutamate receptors are ligand-gated ion channels that contribute to excitatory neurotransmission in the central nervous system (CNS). Most NMDA receptors comprise two glycine-binding GluN1 and two glutamate-binding GluN2 subunits (GluN2A–D). We describe highly potent (S)-5-[(R)-2-amino-2-carboxyethyl]-4,5-dihydro-1H-pyrazole-3-carboxylic acid (ACEPC) competitive GluN2 antagonists, of which ST3 has a binding affinity of 52 nM at GluN1/2A and 782 nM at GluN1/2B receptors. This 15-fold preference of ST3 for GluN1/2A over GluN1/2B is improved compared with NVP-AAM077, a widely used GluN2A-selective antagonist, which we show has 11-fold preference for GluN1/2A over GluN1/2B. Crystal structures of the GluN1/2A agonist binding domain (ABD) heterodimer with bound ACEPC antagonists reveal a binding mode in which the ligands occupy a cavity that extends toward the subunit interface between GluN1 and GluN2A ABDs. Mutational analyses show that the GluN2A preference of ST3 is primarily mediated by four nonconserved residues that are not directly contacting the ligand, but positioned within 12 Å of the glutamate binding site. Two of these residues influence the cavity occupied by ST3 in a manner that results in favorable binding to GluN2A, but occludes binding to GluN2B. Thus, we reveal opportunities for the design of subunit-selective competitive NMDA receptor antagonists by identifying a cavity formore »
- Authors:
-
[1]
- Univ. of Montana, Missoula, MT (United States)
- Univ. of Milan (Italy)
- John Hopkins Medical School, Baltimore, MD (United States)
- Publication Date:
- Research Org.:
- Argonne National Laboratory (ANL), Argonne, IL (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER); National Inst. of Health
- OSTI Identifier:
- 1400292
- Grant/Contract Number:
- AC02-06CH11357; P20 GM103546; R01 NS097536
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Proceedings of the National Academy of Sciences of the United States of America
- Additional Journal Information:
- Journal Volume: 114; Journal Issue: 33; Journal ID: ISSN 0027-8424
- Publisher:
- National Academy of Sciences
- Country of Publication:
- United States
- Language:
- ENGLISH
- Subject:
- 60 APPLIED LIFE SCIENCES; 59 BASIC BIOLOGICAL SCIENCES; synaptic transmission; Schild analysis; kinetic modeling; X-ray crystallography; PEAQX
Citation Formats
Lind, Genevieve E., Mou, Tung-Chung, Tamborini, Lucia, Pomper, Martin G., De Micheli, Carlo, Conti, Paola, Pinto, Andrea, and Hansen, Kasper B. Structural basis of subunit selectivity for competitive NMDA receptor antagonists with preference for GluN2A over GluN2B subunits. United States: N. p., 2017.
Web. doi:10.1073/pnas.1707752114.
Lind, Genevieve E., Mou, Tung-Chung, Tamborini, Lucia, Pomper, Martin G., De Micheli, Carlo, Conti, Paola, Pinto, Andrea, & Hansen, Kasper B. Structural basis of subunit selectivity for competitive NMDA receptor antagonists with preference for GluN2A over GluN2B subunits. United States. https://doi.org/10.1073/pnas.1707752114
Lind, Genevieve E., Mou, Tung-Chung, Tamborini, Lucia, Pomper, Martin G., De Micheli, Carlo, Conti, Paola, Pinto, Andrea, and Hansen, Kasper B. Mon .
"Structural basis of subunit selectivity for competitive NMDA receptor antagonists with preference for GluN2A over GluN2B subunits". United States. https://doi.org/10.1073/pnas.1707752114. https://www.osti.gov/servlets/purl/1400292.
@article{osti_1400292,
title = {Structural basis of subunit selectivity for competitive NMDA receptor antagonists with preference for GluN2A over GluN2B subunits},
author = {Lind, Genevieve E. and Mou, Tung-Chung and Tamborini, Lucia and Pomper, Martin G. and De Micheli, Carlo and Conti, Paola and Pinto, Andrea and Hansen, Kasper B.},
abstractNote = {NMDA-type glutamate receptors are ligand-gated ion channels that contribute to excitatory neurotransmission in the central nervous system (CNS). Most NMDA receptors comprise two glycine-binding GluN1 and two glutamate-binding GluN2 subunits (GluN2A–D). We describe highly potent (S)-5-[(R)-2-amino-2-carboxyethyl]-4,5-dihydro-1H-pyrazole-3-carboxylic acid (ACEPC) competitive GluN2 antagonists, of which ST3 has a binding affinity of 52 nM at GluN1/2A and 782 nM at GluN1/2B receptors. This 15-fold preference of ST3 for GluN1/2A over GluN1/2B is improved compared with NVP-AAM077, a widely used GluN2A-selective antagonist, which we show has 11-fold preference for GluN1/2A over GluN1/2B. Crystal structures of the GluN1/2A agonist binding domain (ABD) heterodimer with bound ACEPC antagonists reveal a binding mode in which the ligands occupy a cavity that extends toward the subunit interface between GluN1 and GluN2A ABDs. Mutational analyses show that the GluN2A preference of ST3 is primarily mediated by four nonconserved residues that are not directly contacting the ligand, but positioned within 12 Å of the glutamate binding site. Two of these residues influence the cavity occupied by ST3 in a manner that results in favorable binding to GluN2A, but occludes binding to GluN2B. Thus, we reveal opportunities for the design of subunit-selective competitive NMDA receptor antagonists by identifying a cavity for ligand binding in which variations exist between GluN2A and GluN2B subunits. In conclusion, this structural insight suggests that subunit selectivity of glutamate-site antagonists can be mediated by mechanisms in addition to direct contributions of contact residues to binding affinity.},
doi = {10.1073/pnas.1707752114},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 33,
volume = 114,
place = {United States},
year = {Mon Jul 31 00:00:00 EDT 2017},
month = {Mon Jul 31 00:00:00 EDT 2017}
}
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