Mechanistic Insights into the Adenosine A1 Receptor’s Positive Allosteric Modulation for Non-Opioid Analgesics

The adenosine A1 receptor (A<sub>1</sub>R) is a promising target for pain treatment. However, the development of therapeutic agonists is hampered by adverse effects, mainly including sedation, bradycardia, hypotension, or respiratory depression. Recently discovered molecules able to over...

Full description

Saved in:
Bibliographic Details
Main Authors: Tal Weizmann, Abigail Pearce, Peter Griffin, Achille Schild, Maren Flaßhoff, Philipp Grossenbacher, Martin Lochner, Christopher A. Reynolds, Graham Ladds, Giuseppe Deganutti
Format: Article
Language:English
Published: MDPI AG 2024-12-01
Series:Cells
Subjects:
Online Access:https://www.mdpi.com/2073-4409/13/24/2121
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1846105391310569472
author Tal Weizmann
Abigail Pearce
Peter Griffin
Achille Schild
Maren Flaßhoff
Philipp Grossenbacher
Martin Lochner
Christopher A. Reynolds
Graham Ladds
Giuseppe Deganutti
author_facet Tal Weizmann
Abigail Pearce
Peter Griffin
Achille Schild
Maren Flaßhoff
Philipp Grossenbacher
Martin Lochner
Christopher A. Reynolds
Graham Ladds
Giuseppe Deganutti
author_sort Tal Weizmann
collection DOAJ
description The adenosine A1 receptor (A<sub>1</sub>R) is a promising target for pain treatment. However, the development of therapeutic agonists is hampered by adverse effects, mainly including sedation, bradycardia, hypotension, or respiratory depression. Recently discovered molecules able to overcome this impediment are the positive allosteric modulator MIPS521 and the A1R-selective agonist BnOCPA, which are both potent and powerful analgesics with fewer side effects. While BnOCPA directly activates the A<sub>1</sub>R from the canonical orthosteric site, MIPS521 binds to an allosteric site, acting in concert with orthosteric adenosine and tuning its pharmacology. Given their overlapping profile in pain models but distinct mechanisms of action, we combined pharmacology and microsecond molecular dynamics simulations to address MIPS521 and BnOCPA activity and their reciprocal influence when bound to the A1R. We show that MIPS521 changes adenosine and BnOCPA G protein selectivity in opposite ways and propose a structural model where TM7 dynamics are differently affected and involved in the G protein preferences of adenosine and BnOCPA.
format Article
id doaj-art-f4b2272fbbb04102bcc335b3deb5398b
institution Kabale University
issn 2073-4409
language English
publishDate 2024-12-01
publisher MDPI AG
record_format Article
series Cells
spelling doaj-art-f4b2272fbbb04102bcc335b3deb5398b2024-12-27T14:16:39ZengMDPI AGCells2073-44092024-12-011324212110.3390/cells13242121Mechanistic Insights into the Adenosine A1 Receptor’s Positive Allosteric Modulation for Non-Opioid AnalgesicsTal Weizmann0Abigail Pearce1Peter Griffin2Achille Schild3Maren Flaßhoff4Philipp Grossenbacher5Martin Lochner6Christopher A. Reynolds7Graham Ladds8Giuseppe Deganutti9Centre for Health and Life Sciences, Coventry University, Coventry CV1 5FB, UKDepartment of Pharmacology, University of Cambridge, Tennis Court Road, Cambridge CB2 1PD, UKCentre for Health and Life Sciences, Coventry University, Coventry CV1 5FB, UKInstitute of Biochemistry and Molecular Medicine, University of Bern, 3012 Bern, SwitzerlandInstitute of Biochemistry and Molecular Medicine, University of Bern, 3012 Bern, SwitzerlandInstitute of Biochemistry and Molecular Medicine, University of Bern, 3012 Bern, SwitzerlandInstitute of Biochemistry and Molecular Medicine, University of Bern, 3012 Bern, SwitzerlandCentre for Health and Life Sciences, Coventry University, Coventry CV1 5FB, UKDepartment of Pharmacology, University of Cambridge, Tennis Court Road, Cambridge CB2 1PD, UKCentre for Health and Life Sciences, Coventry University, Coventry CV1 5FB, UKThe adenosine A1 receptor (A<sub>1</sub>R) is a promising target for pain treatment. However, the development of therapeutic agonists is hampered by adverse effects, mainly including sedation, bradycardia, hypotension, or respiratory depression. Recently discovered molecules able to overcome this impediment are the positive allosteric modulator MIPS521 and the A1R-selective agonist BnOCPA, which are both potent and powerful analgesics with fewer side effects. While BnOCPA directly activates the A<sub>1</sub>R from the canonical orthosteric site, MIPS521 binds to an allosteric site, acting in concert with orthosteric adenosine and tuning its pharmacology. Given their overlapping profile in pain models but distinct mechanisms of action, we combined pharmacology and microsecond molecular dynamics simulations to address MIPS521 and BnOCPA activity and their reciprocal influence when bound to the A1R. We show that MIPS521 changes adenosine and BnOCPA G protein selectivity in opposite ways and propose a structural model where TM7 dynamics are differently affected and involved in the G protein preferences of adenosine and BnOCPA.https://www.mdpi.com/2073-4409/13/24/2121adenosine A1 receptorBnOCPAMIPS521non-opioid analgesiaGPCRs
spellingShingle Tal Weizmann
Abigail Pearce
Peter Griffin
Achille Schild
Maren Flaßhoff
Philipp Grossenbacher
Martin Lochner
Christopher A. Reynolds
Graham Ladds
Giuseppe Deganutti
Mechanistic Insights into the Adenosine A1 Receptor’s Positive Allosteric Modulation for Non-Opioid Analgesics
Cells
adenosine A1 receptor
BnOCPA
MIPS521
non-opioid analgesia
GPCRs
title Mechanistic Insights into the Adenosine A1 Receptor’s Positive Allosteric Modulation for Non-Opioid Analgesics
title_full Mechanistic Insights into the Adenosine A1 Receptor’s Positive Allosteric Modulation for Non-Opioid Analgesics
title_fullStr Mechanistic Insights into the Adenosine A1 Receptor’s Positive Allosteric Modulation for Non-Opioid Analgesics
title_full_unstemmed Mechanistic Insights into the Adenosine A1 Receptor’s Positive Allosteric Modulation for Non-Opioid Analgesics
title_short Mechanistic Insights into the Adenosine A1 Receptor’s Positive Allosteric Modulation for Non-Opioid Analgesics
title_sort mechanistic insights into the adenosine a1 receptor s positive allosteric modulation for non opioid analgesics
topic adenosine A1 receptor
BnOCPA
MIPS521
non-opioid analgesia
GPCRs
url https://www.mdpi.com/2073-4409/13/24/2121
work_keys_str_mv AT talweizmann mechanisticinsightsintotheadenosinea1receptorspositiveallostericmodulationfornonopioidanalgesics
AT abigailpearce mechanisticinsightsintotheadenosinea1receptorspositiveallostericmodulationfornonopioidanalgesics
AT petergriffin mechanisticinsightsintotheadenosinea1receptorspositiveallostericmodulationfornonopioidanalgesics
AT achilleschild mechanisticinsightsintotheadenosinea1receptorspositiveallostericmodulationfornonopioidanalgesics
AT marenflaßhoff mechanisticinsightsintotheadenosinea1receptorspositiveallostericmodulationfornonopioidanalgesics
AT philippgrossenbacher mechanisticinsightsintotheadenosinea1receptorspositiveallostericmodulationfornonopioidanalgesics
AT martinlochner mechanisticinsightsintotheadenosinea1receptorspositiveallostericmodulationfornonopioidanalgesics
AT christopherareynolds mechanisticinsightsintotheadenosinea1receptorspositiveallostericmodulationfornonopioidanalgesics
AT grahamladds mechanisticinsightsintotheadenosinea1receptorspositiveallostericmodulationfornonopioidanalgesics
AT giuseppedeganutti mechanisticinsightsintotheadenosinea1receptorspositiveallostericmodulationfornonopioidanalgesics