Identification of the A293 (AVE1231) Binding Site in the Cardiac Two-Pore-Domain Potassium Channel TASK-1: a Common Low Affinity Antiarrhythmic Drug Binding Site.


Journal

Cellular physiology and biochemistry : international journal of experimental cellular physiology, biochemistry, and pharmacology
ISSN: 1421-9778
Titre abrégé: Cell Physiol Biochem
Pays: Germany
ID NLM: 9113221

Informations de publication

Date de publication:
2019
Historique:
received: 21 08 2018
accepted: 30 01 2019
entrez: 20 4 2019
pubmed: 20 4 2019
medline: 3 5 2019
Statut: ppublish

Résumé

The two-pore-domain potassium channel TASK-1 regulates atrial action potential duration. Due to the atrium-specific expression of TASK-1 in the human heart and the functional upregulation of TASK-1 currents in atrial fibrillation (AF), TASK-1 represents a promising target for the treatment of AF. Therefore, detailed knowledge of the molecular determinants of TASK-1 inhibition may help to identify new drugs for the future therapy of AF. In the current study, the molecular determinants of TASK-1 inhibition by the potent and antiarrhythmic compound A293 (AVE1231) were studied in detail. Alanine-scanning mutagenesis together with two-electrode voltage-clamp recordings were combined with in silico docking experiments. Here, we have identified Q126 located in the M2 segment together with L239 and N240 of the M4 segment as amino acids essential for the A293-mediated inhibition of TASK-1. These data indicate a binding site which is different to that of A1899 for which also residues of the pore signature sequence and the late M4 segments are essential. Using in silico docking experiments, we propose a binding site at the lower end of the cytosolic pore, located at the entry to lateral side fenestrations of TASK-1. Strikingly, TASK-1 inhibition by the low affinity antiarrhythmic TASK-1 blockers propafenone, amiodarone and carvedilol was also strongly diminished by mutations at this novel binding site. We have identified the A293 binding site in the central cavity of TASK-1 and propose that this site might represent a conserved site of action for many low affinity antiarrhythmic TASK-1 blockers.

Sections du résumé

BACKGROUND/AIMS OBJECTIVE
The two-pore-domain potassium channel TASK-1 regulates atrial action potential duration. Due to the atrium-specific expression of TASK-1 in the human heart and the functional upregulation of TASK-1 currents in atrial fibrillation (AF), TASK-1 represents a promising target for the treatment of AF. Therefore, detailed knowledge of the molecular determinants of TASK-1 inhibition may help to identify new drugs for the future therapy of AF. In the current study, the molecular determinants of TASK-1 inhibition by the potent and antiarrhythmic compound A293 (AVE1231) were studied in detail.
METHODS METHODS
Alanine-scanning mutagenesis together with two-electrode voltage-clamp recordings were combined with in silico docking experiments.
RESULTS RESULTS
Here, we have identified Q126 located in the M2 segment together with L239 and N240 of the M4 segment as amino acids essential for the A293-mediated inhibition of TASK-1. These data indicate a binding site which is different to that of A1899 for which also residues of the pore signature sequence and the late M4 segments are essential. Using in silico docking experiments, we propose a binding site at the lower end of the cytosolic pore, located at the entry to lateral side fenestrations of TASK-1. Strikingly, TASK-1 inhibition by the low affinity antiarrhythmic TASK-1 blockers propafenone, amiodarone and carvedilol was also strongly diminished by mutations at this novel binding site.
CONCLUSION CONCLUSIONS
We have identified the A293 binding site in the central cavity of TASK-1 and propose that this site might represent a conserved site of action for many low affinity antiarrhythmic TASK-1 blockers.

Identifiants

pubmed: 31001961
doi: 10.33594/000000083
doi:

Substances chimiques

Anti-Arrhythmia Agents 0
Nerve Tissue Proteins 0
Potassium Channels, Tandem Pore Domain 0
potassium channel subfamily K member 3 1HQ3YCN4GS

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

1223-1235

Subventions

Organisme : University of Heidelberg, Faculty of Medicine
ID : Rahel Goitein-Straus Scholarship and Olympia-Morata Scholarship
Pays : Germany
Organisme : German Center for Cardiovascular Research (DZHK)
ID : Excellence Grant
Pays : Germany
Organisme : German Cardiac Society (DGK)
ID : DGK082018 and Otto-Hess Fellowship
Pays : Germany
Organisme : German Heart Foundation /German Foundation of Heart Research
ID : F/41/15 and Kaltenbach Scholarship
Pays : Germany
Organisme : Fondecyt Grant
ID : 1191133
Pays : Chile
Organisme : Millennium Nucleus of Ion Channels Associated Diseases (MiNICAD)
Pays : Chile
Organisme : German Research Foundation (DFG)
ID : SCHM 3358/1-1, DE1482-4/1
Pays : Germany

Informations de copyright

© Copyright by the Author(s). Published by Cell Physiol Biochem Press.

Déclaration de conflit d'intérêts

The authors declare that they have no conflict of interests.

Auteurs

Felix Wiedmann (F)

Department of Cardiology, University of Heidelberg, Heidelberg, Germany.
DZHK (German Center for Cardiovascular Research), partner site Heidelberg-Mannheim, University of Heidelberg, Heidelberg, Germany.
HCR, Heidelberg Center for Heart Rhythm Disorders, University of Heidelberg, Heidelberg, Germany.

Aytug K Kiper (AK)

Institute for Physiology and Pathophysiology, Vegetative Physiology, University of Marburg, Marburg, Germany.

Mauricio Bedoya (M)

Centro de Bioinformática y Simulación Molecular, Universidad de Talca, Talca, Chile.

Antonius Ratte (A)

Department of Cardiology, University of Heidelberg, Heidelberg, Germany.
HCR, Heidelberg Center for Heart Rhythm Disorders, University of Heidelberg, Heidelberg, Germany.

Susanne Rinné (S)

Institute for Physiology and Pathophysiology, Vegetative Physiology, University of Marburg, Marburg, Germany.

Manuel Kraft (M)

Department of Cardiology, University of Heidelberg, Heidelberg, Germany.
DZHK (German Center for Cardiovascular Research), partner site Heidelberg-Mannheim, University of Heidelberg, Heidelberg, Germany.
HCR, Heidelberg Center for Heart Rhythm Disorders, University of Heidelberg, Heidelberg, Germany.

Maximilian Waibel (M)

Department of Cardiology, University of Heidelberg, Heidelberg, Germany.
DZHK (German Center for Cardiovascular Research), partner site Heidelberg-Mannheim, University of Heidelberg, Heidelberg, Germany.
HCR, Heidelberg Center for Heart Rhythm Disorders, University of Heidelberg, Heidelberg, Germany.

Priya Anad (P)

Institute of Nanotechnology, Karlsruhe Institute of Technology, Karlsruhe, Germany.

Wolfgang Wenzel (W)

Institute of Nanotechnology, Karlsruhe Institute of Technology, Karlsruhe, Germany.

Wendy González (W)

Centro de Bioinformática y Simulación Molecular, Universidad de Talca, Talca, Chile.
Millennium Nucleus of Ion Channels-Associated Diseases (MiNICAD), Universidad de Talca, Talca, Chile.

Hugo A Katus (HA)

Department of Cardiology, University of Heidelberg, Heidelberg, Germany.
DZHK (German Center for Cardiovascular Research), partner site Heidelberg-Mannheim, University of Heidelberg, Heidelberg, Germany.
HCR, Heidelberg Center for Heart Rhythm Disorders, University of Heidelberg, Heidelberg, Germany.

Niels Decher (N)

Institute for Physiology and Pathophysiology, Vegetative Physiology, University of Marburg, Marburg, Germany, Decher@staff.uni-marburg.de.

Constanze Schmidt (C)

Department of Cardiology, University of Heidelberg, Heidelberg, Germany.
DZHK (German Center for Cardiovascular Research), partner site Heidelberg-Mannheim, University of Heidelberg, Heidelberg, Germany.
HCR, Heidelberg Center for Heart Rhythm Disorders, University of Heidelberg, Heidelberg, Germany, Constanze.Schmidt@med.uni-heidelberg.de.

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Classifications MeSH