Structure-guided design of partial agonists at an opioid receptor

Abstract Chronic pain and opioid overdose deaths highlight the need for non-addictive analgesics with novel mechanisms. The δ opioid receptor (δOR) is a promising target, as it lacks the respiratory depression associated with µ opioid receptor (µOR) agonists. However, early δOR full agonists caused...

Full description

Saved in:
Bibliographic Details
Main Authors: Balazs R. Varga, Sarah M. Bernhard, Amal El Daibani, Saheem A. Zaidi, Jordy H. Lam, Jhoan Aguilar, Kevin Appourchaux, Antonina L. Nazarova, Alexa Kouvelis, Ryosuke Shinouchi, Haylee R. Hammond, Shainnel O. Eans, Violetta Weinreb, Elyssa B. Margolis, Jonathan F. Fay, Xi-Ping Huang, Amynah Pradhan, Vsevolod Katritch, Jay P. McLaughlin, Susruta Majumdar, Tao Che
Format: Article
Language:English
Published: Nature Portfolio 2025-03-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-025-57734-5
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1849772404047347712
author Balazs R. Varga
Sarah M. Bernhard
Amal El Daibani
Saheem A. Zaidi
Jordy H. Lam
Jhoan Aguilar
Kevin Appourchaux
Antonina L. Nazarova
Alexa Kouvelis
Ryosuke Shinouchi
Haylee R. Hammond
Shainnel O. Eans
Violetta Weinreb
Elyssa B. Margolis
Jonathan F. Fay
Xi-Ping Huang
Amynah Pradhan
Vsevolod Katritch
Jay P. McLaughlin
Susruta Majumdar
Tao Che
author_facet Balazs R. Varga
Sarah M. Bernhard
Amal El Daibani
Saheem A. Zaidi
Jordy H. Lam
Jhoan Aguilar
Kevin Appourchaux
Antonina L. Nazarova
Alexa Kouvelis
Ryosuke Shinouchi
Haylee R. Hammond
Shainnel O. Eans
Violetta Weinreb
Elyssa B. Margolis
Jonathan F. Fay
Xi-Ping Huang
Amynah Pradhan
Vsevolod Katritch
Jay P. McLaughlin
Susruta Majumdar
Tao Che
author_sort Balazs R. Varga
collection DOAJ
description Abstract Chronic pain and opioid overdose deaths highlight the need for non-addictive analgesics with novel mechanisms. The δ opioid receptor (δOR) is a promising target, as it lacks the respiratory depression associated with µ opioid receptor (µOR) agonists. However, early δOR full agonists caused seizures, limiting their clinical use. Partial δOR agonists may offer more controlled receptor activation than full agonists, but their development has been hindered by uncertainty regarding the molecular mechanism of partial agonism. Here we show that C6-Quino, a bitopic ligand developed through structure-based design, acts as a selective δOR partial agonist. Functional studies reveal that C6-Quino shows differential activity at G-protein and arrestin pathways and interacts with the sodium binding pocket, confirmed through cryo-EM analysis. C6-Quino demonstrates oral activity, analgesic activity in chronic pain models without causing δOR-related seizures and µOR-related adverse effects which have limited opioid usage in recent times. This discovery outlines a new strategy for developing δOR-targeted analgesics and provides a framework for optimizing signaling profiles of other Class A GPCRs.
format Article
id doaj-art-01277f7bd84242c98c41e0959f62fd74
institution DOAJ
issn 2041-1723
language English
publishDate 2025-03-01
publisher Nature Portfolio
record_format Article
series Nature Communications
spelling doaj-art-01277f7bd84242c98c41e0959f62fd742025-08-20T03:02:19ZengNature PortfolioNature Communications2041-17232025-03-0116111510.1038/s41467-025-57734-5Structure-guided design of partial agonists at an opioid receptorBalazs R. Varga0Sarah M. Bernhard1Amal El Daibani2Saheem A. Zaidi3Jordy H. Lam4Jhoan Aguilar5Kevin Appourchaux6Antonina L. Nazarova7Alexa Kouvelis8Ryosuke Shinouchi9Haylee R. Hammond10Shainnel O. Eans11Violetta Weinreb12Elyssa B. Margolis13Jonathan F. Fay14Xi-Ping Huang15Amynah Pradhan16Vsevolod Katritch17Jay P. McLaughlin18Susruta Majumdar19Tao Che20Center for Clinical Pharmacology, Department of Anesthesiology, Washington University School of MedicineCenter for Clinical Pharmacology, Department of Anesthesiology, Washington University School of MedicineCenter for Clinical Pharmacology, Department of Anesthesiology, Washington University School of MedicineDepartment of Quantitative & Computational Biology and Department of Chemistry, University of Southern CaliforniaDepartment of Quantitative & Computational Biology and Department of Chemistry, University of Southern CaliforniaCenter for Clinical Pharmacology, Department of Anesthesiology, Washington University School of MedicineCenter for Clinical Pharmacology, Department of Anesthesiology, Washington University School of MedicineDepartment of Quantitative & Computational Biology and Department of Chemistry, University of Southern CaliforniaCenter for Clinical Pharmacology, Department of Anesthesiology, Washington University School of MedicineDepartment of Pharmacodynamics, University of FloridaDepartment of Pharmacodynamics, University of FloridaDepartment of Pharmacodynamics, University of FloridaDepartment of Pharmacology School of Medicine, University of North Carolina Chapel HillUCSF Weill Institute for Neurosciences, Department of Neurology, University of CaliforniaDepartment of Biochemistry and Molecular Biology, University of Maryland BaltimoreDepartment of Pharmacology School of Medicine, University of North Carolina Chapel HillCenter for Clinical Pharmacology, Department of Anesthesiology, Washington University School of MedicineDepartment of Quantitative & Computational Biology and Department of Chemistry, University of Southern CaliforniaDepartment of Pharmacodynamics, University of FloridaCenter for Clinical Pharmacology, Department of Anesthesiology, Washington University School of MedicineCenter for Clinical Pharmacology, Department of Anesthesiology, Washington University School of MedicineAbstract Chronic pain and opioid overdose deaths highlight the need for non-addictive analgesics with novel mechanisms. The δ opioid receptor (δOR) is a promising target, as it lacks the respiratory depression associated with µ opioid receptor (µOR) agonists. However, early δOR full agonists caused seizures, limiting their clinical use. Partial δOR agonists may offer more controlled receptor activation than full agonists, but their development has been hindered by uncertainty regarding the molecular mechanism of partial agonism. Here we show that C6-Quino, a bitopic ligand developed through structure-based design, acts as a selective δOR partial agonist. Functional studies reveal that C6-Quino shows differential activity at G-protein and arrestin pathways and interacts with the sodium binding pocket, confirmed through cryo-EM analysis. C6-Quino demonstrates oral activity, analgesic activity in chronic pain models without causing δOR-related seizures and µOR-related adverse effects which have limited opioid usage in recent times. This discovery outlines a new strategy for developing δOR-targeted analgesics and provides a framework for optimizing signaling profiles of other Class A GPCRs.https://doi.org/10.1038/s41467-025-57734-5
spellingShingle Balazs R. Varga
Sarah M. Bernhard
Amal El Daibani
Saheem A. Zaidi
Jordy H. Lam
Jhoan Aguilar
Kevin Appourchaux
Antonina L. Nazarova
Alexa Kouvelis
Ryosuke Shinouchi
Haylee R. Hammond
Shainnel O. Eans
Violetta Weinreb
Elyssa B. Margolis
Jonathan F. Fay
Xi-Ping Huang
Amynah Pradhan
Vsevolod Katritch
Jay P. McLaughlin
Susruta Majumdar
Tao Che
Structure-guided design of partial agonists at an opioid receptor
Nature Communications
title Structure-guided design of partial agonists at an opioid receptor
title_full Structure-guided design of partial agonists at an opioid receptor
title_fullStr Structure-guided design of partial agonists at an opioid receptor
title_full_unstemmed Structure-guided design of partial agonists at an opioid receptor
title_short Structure-guided design of partial agonists at an opioid receptor
title_sort structure guided design of partial agonists at an opioid receptor
url https://doi.org/10.1038/s41467-025-57734-5
work_keys_str_mv AT balazsrvarga structureguideddesignofpartialagonistsatanopioidreceptor
AT sarahmbernhard structureguideddesignofpartialagonistsatanopioidreceptor
AT amaleldaibani structureguideddesignofpartialagonistsatanopioidreceptor
AT saheemazaidi structureguideddesignofpartialagonistsatanopioidreceptor
AT jordyhlam structureguideddesignofpartialagonistsatanopioidreceptor
AT jhoanaguilar structureguideddesignofpartialagonistsatanopioidreceptor
AT kevinappourchaux structureguideddesignofpartialagonistsatanopioidreceptor
AT antoninalnazarova structureguideddesignofpartialagonistsatanopioidreceptor
AT alexakouvelis structureguideddesignofpartialagonistsatanopioidreceptor
AT ryosukeshinouchi structureguideddesignofpartialagonistsatanopioidreceptor
AT hayleerhammond structureguideddesignofpartialagonistsatanopioidreceptor
AT shainneloeans structureguideddesignofpartialagonistsatanopioidreceptor
AT violettaweinreb structureguideddesignofpartialagonistsatanopioidreceptor
AT elyssabmargolis structureguideddesignofpartialagonistsatanopioidreceptor
AT jonathanffay structureguideddesignofpartialagonistsatanopioidreceptor
AT xipinghuang structureguideddesignofpartialagonistsatanopioidreceptor
AT amynahpradhan structureguideddesignofpartialagonistsatanopioidreceptor
AT vsevolodkatritch structureguideddesignofpartialagonistsatanopioidreceptor
AT jaypmclaughlin structureguideddesignofpartialagonistsatanopioidreceptor
AT susrutamajumdar structureguideddesignofpartialagonistsatanopioidreceptor
AT taoche structureguideddesignofpartialagonistsatanopioidreceptor