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Mechanistic ion channel interactions in red cells of patients with Gárdos channelopathy

Julia M. Jansen, Min Qiao, Laura Hertz, Xijia Wang, Elisa Fermo, Anna Zaninoni, Raffaella Colombatti, Ingolf Bernhardt, Paola Bianchi, Lars Kaestner

2021Blood Advances22 citationsDOIOpen Access PDF

Abstract

In patients with Gárdos channelopathy (p.R352H), an increased concentration of intracellular Ca2+ was previously reported. This is a surprising finding because the Gárdos channel (KCa3.1) is a K+ channel. Here, we confirm the increased intracellular Ca2+ for patients with the KCa3.1 mutation p.S314P. Furthermore, we provide the concept of KCa3.1 activity resulting in a flickering of red blood cell (RBC) membranepotential, which activates the CaV2.1 channel allowing Ca2+ to enter the RBC. Activity of the nonselective cation channel Piezo1 modulates the aforementioned interplay in away that a closed Piezo1 is in favor of the KCa3.1-CaV2.1 interaction. In contrast, Piezo1 openings compromise the membrane potential flickering, thus limiting the activity of CaV2.1. With the compound NS309, we mimic a gain-of-function mutation of KCa3.1. Assessing the RBC Ca2+ response by Fluo-4-based flow cytometry and by measuring the membrane potential using the Macey-Bennekou-Egée method, we provide data that support the concept of the KCa3.1/CaV2.1/Piezo1 interplay as a partial explanation for an increased number of high Ca2+ RBCs. With the pharmacological inhibition of KCa3.1 (TRAM34 and Senicapoc), CaV2.1 (ω-agatoxin TK), and Piezo1 (GsMTx-4), we could project the NS309 behavior of healthy RBCs to the RBCs of Gárdos channelopathy patients.

Topics & Concepts

ChannelopathyPIEZO1IntracellularBiophysicsIon channelChemistryFlow cytometryInward-rectifier potassium ion channelBand 3MembraneCell biologyBiochemistryBiologyNeuroscienceMolecular biologyMembrane proteinReceptorMechanosensitive channelsErythrocyte Function and PathophysiologyIon channel regulation and functionPancreatic function and diabetes
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