Kinetics of endothelin-1 and effect selective ETA antagonism on ETB activation: a mathematical modeling analysis

IntroductionEndothelin-1 (ET-1) regulates renal and vascular function, but the clinical utility of selective ETA receptor antagonists has been limited due to associated fluid retention. The mechanisms underlying fluid retention remain poorly understood but could be a consequence of changes in ET-1 b...

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Main Authors: K. Melissa Hallow, Peter J. Greasley, Hiddo J. L. Heerspink, Hongtao Yu
Format: Article
Language:English
Published: Frontiers Media S.A. 2024-11-01
Series:Frontiers in Pharmacology
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Online Access:https://www.frontiersin.org/articles/10.3389/fphar.2024.1332388/full
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author K. Melissa Hallow
K. Melissa Hallow
Peter J. Greasley
Hiddo J. L. Heerspink
Hiddo J. L. Heerspink
Hongtao Yu
author_facet K. Melissa Hallow
K. Melissa Hallow
Peter J. Greasley
Hiddo J. L. Heerspink
Hiddo J. L. Heerspink
Hongtao Yu
author_sort K. Melissa Hallow
collection DOAJ
description IntroductionEndothelin-1 (ET-1) regulates renal and vascular function, but the clinical utility of selective ETA receptor antagonists has been limited due to associated fluid retention. The mechanisms underlying fluid retention remain poorly understood but could be a consequence of changes in ET-1 binding to the unantagonized ETB receptor, either through increased ET-1 or non-selective ETB.MethodsA mathematical model of ET-1 kinetics was developed to quantify effects of ETA antagonist exposure and selectivity on concentrations of ET-1 and its complexes with ETA and ETB receptors. The model describes ET-1 production, tissue and plasma distribution, ETA and ETB receptor binding, and receptor-mediated clearance, and was calibrated and validated with human ET-1 infusion studies.ResultsThe model confirmed the significant role of ETB in ET-1 clearance. By varying both drug ETA selectivity (Kib/Kia) and concentration over a wide range, simulations predicted that while selective ETA antagonist (selectivity >1) always decreased [ET1-ETA], the change in [ET1-ETB] was more complex. It increased up to 45% as drug concentrations approached and exceeded Kia, but the increase was diminished as drug concentration increased further and fell below baseline at high concentrations. The drug concentration required to cause a decrease in [ET1-ETB] was lower as ETA selectivity decreased.DiscussionThis is the first mechanistic mathematical model of ET-1 kinetics that describes receptor-mediated clearance, and the consequence of ETB blockade on ET-1 concentrations. It provides a useful tool that can coupled with experimental studies to quantitively understand and investigate this complex and dynamic system.
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spelling doaj-art-35527bed2919432ba86cbe10281ef2482025-08-20T01:53:31ZengFrontiers Media S.A.Frontiers in Pharmacology1663-98122024-11-011510.3389/fphar.2024.13323881332388Kinetics of endothelin-1 and effect selective ETA antagonism on ETB activation: a mathematical modeling analysisK. Melissa Hallow0K. Melissa Hallow1Peter J. Greasley2Hiddo J. L. Heerspink3Hiddo J. L. Heerspink4Hongtao Yu5School of Chemical, Materials, and Biomedical Engineering, University of Georgia, Athens, GA, United StatesDepartment of Epidemiology and Biostatistics, University of Georgia, Athens, GA, United StatesEarly Clinical Development, Research and Early Development, Cardiovascular, Renal and Metabolism (CVRM), Biopharmaceuticals, R&D, AstraZeneca, Gothenburg, SwedenDepartment of Clinical Pharmacy and Pharmacology, University of Groningen, Groningen, NetherlandsThe George Institute for Global Health, Sydney, AustraliaClinical Pharmacology and Quantitative Pharmacology, Clinical Pharmacology and Safety Sciences, R&D, AstraZeneca, Gaithersburg, MD, United StatesIntroductionEndothelin-1 (ET-1) regulates renal and vascular function, but the clinical utility of selective ETA receptor antagonists has been limited due to associated fluid retention. The mechanisms underlying fluid retention remain poorly understood but could be a consequence of changes in ET-1 binding to the unantagonized ETB receptor, either through increased ET-1 or non-selective ETB.MethodsA mathematical model of ET-1 kinetics was developed to quantify effects of ETA antagonist exposure and selectivity on concentrations of ET-1 and its complexes with ETA and ETB receptors. The model describes ET-1 production, tissue and plasma distribution, ETA and ETB receptor binding, and receptor-mediated clearance, and was calibrated and validated with human ET-1 infusion studies.ResultsThe model confirmed the significant role of ETB in ET-1 clearance. By varying both drug ETA selectivity (Kib/Kia) and concentration over a wide range, simulations predicted that while selective ETA antagonist (selectivity >1) always decreased [ET1-ETA], the change in [ET1-ETB] was more complex. It increased up to 45% as drug concentrations approached and exceeded Kia, but the increase was diminished as drug concentration increased further and fell below baseline at high concentrations. The drug concentration required to cause a decrease in [ET1-ETB] was lower as ETA selectivity decreased.DiscussionThis is the first mechanistic mathematical model of ET-1 kinetics that describes receptor-mediated clearance, and the consequence of ETB blockade on ET-1 concentrations. It provides a useful tool that can coupled with experimental studies to quantitively understand and investigate this complex and dynamic system.https://www.frontiersin.org/articles/10.3389/fphar.2024.1332388/fullendothelinendothelin receptor antagonistmathematical modelingkineticsETAETB
spellingShingle K. Melissa Hallow
K. Melissa Hallow
Peter J. Greasley
Hiddo J. L. Heerspink
Hiddo J. L. Heerspink
Hongtao Yu
Kinetics of endothelin-1 and effect selective ETA antagonism on ETB activation: a mathematical modeling analysis
Frontiers in Pharmacology
endothelin
endothelin receptor antagonist
mathematical modeling
kinetics
ETA
ETB
title Kinetics of endothelin-1 and effect selective ETA antagonism on ETB activation: a mathematical modeling analysis
title_full Kinetics of endothelin-1 and effect selective ETA antagonism on ETB activation: a mathematical modeling analysis
title_fullStr Kinetics of endothelin-1 and effect selective ETA antagonism on ETB activation: a mathematical modeling analysis
title_full_unstemmed Kinetics of endothelin-1 and effect selective ETA antagonism on ETB activation: a mathematical modeling analysis
title_short Kinetics of endothelin-1 and effect selective ETA antagonism on ETB activation: a mathematical modeling analysis
title_sort kinetics of endothelin 1 and effect selective eta antagonism on etb activation a mathematical modeling analysis
topic endothelin
endothelin receptor antagonist
mathematical modeling
kinetics
ETA
ETB
url https://www.frontiersin.org/articles/10.3389/fphar.2024.1332388/full
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