Molecular and functional characterization of a new potassium conductance in mouse ventricular fibroblasts

Abstract The present work is aimed at identifying and characterizing, at a molecular and functional level, new ionic conductances potentially involved in the excitation–secretion coupling and proliferation of cardiac ventricular fibroblasts. Among potassium channel transcripts which were screened by...

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Published inJournal of molecular and cellular cardiology Vol. 46; no. 4; pp. 508 - 517
Main Authors Benamer, Najate, Moha Ou Maati, Hamid, Demolombe, Sophie, Cantereau, Anne, Delwail, Adriana, Bois, Patrick, Bescond, Jocelyn, Faivre, Jean-François
Format Journal Article
LanguageEnglish
Published England Elsevier Ltd 01.04.2009
Elsevier
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Abstract Abstract The present work is aimed at identifying and characterizing, at a molecular and functional level, new ionic conductances potentially involved in the excitation–secretion coupling and proliferation of cardiac ventricular fibroblasts. Among potassium channel transcripts which were screened by high-throughput real-time PCR, SUR2 and Kir6.1 mRNAs were found to be the most abundant in ventricular fibroblasts. The corresponding proteins were not detected by western blot following 5 days of cell culture, but had appeared at 7 days, increasing with extended cell culture duration as the fibroblasts differentiated into myofibroblasts. Using the inside-out configuration of the patch-clamp technique, single potassium channels could be recorded. These had properties similar to those reported for SUR2/Kir6.1 channels, i.e. activation by pinacidil, inhibition by glibenclamide and activation by intracellular UDP. As already reported for this molecular signature, they were insensitive to intracellular ATP. In the whole-cell configuration, these channels have been shown to be responsible for a glibenclamide-sensitive macroscopic potassium current which can be activated not only by pinacidil, but also by nanomolar concentrations of the sphingolipid sphingosine-1-phosphate (S1P). The activation of this current resulted in an increase in cell proliferation and a decrease in IL-6 secretion, suggesting it has a functional role in situations where S1P increases. Overall, this work demonstrates for the first time that SUR2/Kir6.1 channels represent a significant potassium conductance in ventricular fibroblasts which may be activated in physio-pathological conditions and which may impact on fibroblast proliferation and function.
AbstractList The present work is aimed at identifying and characterizing, at a molecular and functional level, new ionic conductances potentially involved in the excitation-secretion coupling and proliferation of cardiac ventricular fibroblasts. Among potassium channel transcripts which were screened by high-throughput real-time PCR, SUR2 and Kir6.1 mRNAs were found to be the most abundant in ventricular fibroblasts. The corresponding proteins were not detected by western blot following 5 days of cell culture, but had appeared at 7 days, increasing with extended cell culture duration as the fibroblasts differentiated into myofibroblasts. Using the inside-out configuration of the patch-clamp technique, single potassium channels could be recorded. These had properties similar to those reported for SUR2/Kir6.1 channels, i.e. activation by pinacidil, inhibition by glibenclamide and activation by intracellular UDP. As already reported for this molecular signature, they were insensitive to intracellular ATP. In the whole-cell configuration, these channels have been shown to be responsible for a glibenclamide-sensitive macroscopic potassium current which can be activated not only by pinacidil, but also by nanomolar concentrations of the sphingolipid sphingosine-1-phosphate (S1P). The activation of this current resulted in an increase in cell proliferation and a decrease in IL-6 secretion, suggesting it has a functional role in situations where S1P increases. Overall, this work demonstrates for the first time that SUR2/Kir6.1 channels represent a significant potassium conductance in ventricular fibroblasts which may be activated in physio-pathological conditions and which may impact on fibroblast proliferation and function.
The present work is aimed at identifying and characterizing, at a molecular and functional level, new ionic conductances potentially involved in the excitation–secretion coupling and proliferation of cardiac ventricular fibroblasts. Among potassium channel transcripts which were screened by high-throughput real-time PCR, SUR2 and Kir6.1 mRNAs were found to be the most abundant in ventricular fibroblasts. The corresponding proteins were not detected by western blot following 5 days of cell culture, but had appeared at 7 days, increasing with extended cell culture duration as the fibroblasts differentiated into myofibroblasts. Using the inside-out configuration of the patch-clamp technique, single potassium channels could be recorded. These had properties similar to those reported for SUR2/Kir6.1 channels, i.e. activation by pinacidil, inhibition by glibenclamide and activation by intracellular UDP. As already reported for this molecular signature, they were insensitive to intracellular ATP. In the whole-cell configuration, these channels have been shown to be responsible for a glibenclamide-sensitive macroscopic potassium current which can be activated not only by pinacidil, but also by nanomolar concentrations of the sphingolipid sphingosine-1-phosphate (S1P). The activation of this current resulted in an increase in cell proliferation and a decrease in IL-6 secretion, suggesting it has a functional role in situations where S1P increases. Overall, this work demonstrates for the first time that SUR2/Kir6.1 channels represent a significant potassium conductance in ventricular fibroblasts which may be activated in physio-pathological conditions and which may impact on fibroblast proliferation and function.
Abstract The present work is aimed at identifying and characterizing, at a molecular and functional level, new ionic conductances potentially involved in the excitation–secretion coupling and proliferation of cardiac ventricular fibroblasts. Among potassium channel transcripts which were screened by high-throughput real-time PCR, SUR2 and Kir6.1 mRNAs were found to be the most abundant in ventricular fibroblasts. The corresponding proteins were not detected by western blot following 5 days of cell culture, but had appeared at 7 days, increasing with extended cell culture duration as the fibroblasts differentiated into myofibroblasts. Using the inside-out configuration of the patch-clamp technique, single potassium channels could be recorded. These had properties similar to those reported for SUR2/Kir6.1 channels, i.e. activation by pinacidil, inhibition by glibenclamide and activation by intracellular UDP. As already reported for this molecular signature, they were insensitive to intracellular ATP. In the whole-cell configuration, these channels have been shown to be responsible for a glibenclamide-sensitive macroscopic potassium current which can be activated not only by pinacidil, but also by nanomolar concentrations of the sphingolipid sphingosine-1-phosphate (S1P). The activation of this current resulted in an increase in cell proliferation and a decrease in IL-6 secretion, suggesting it has a functional role in situations where S1P increases. Overall, this work demonstrates for the first time that SUR2/Kir6.1 channels represent a significant potassium conductance in ventricular fibroblasts which may be activated in physio-pathological conditions and which may impact on fibroblast proliferation and function.
Author Cantereau, Anne
Bescond, Jocelyn
Faivre, Jean-François
Demolombe, Sophie
Delwail, Adriana
Bois, Patrick
Moha Ou Maati, Hamid
Benamer, Najate
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Issue 4
Keywords SUR2/Kir6.1
Cardiac fibroblasts
K-channel
IL-6
Sphingosine-1-phosphate
SUR2/Kir6.1 K-channel Cardiac fibroblasts IL-6 Sphingosine-1-phosphate
Language English
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Snippet Abstract The present work is aimed at identifying and characterizing, at a molecular and functional level, new ionic conductances potentially involved in the...
The present work is aimed at identifying and characterizing, at a molecular and functional level, new ionic conductances potentially involved in the...
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SubjectTerms Actins - metabolism
Animals
ATP-Binding Cassette Transporters - genetics
ATP-Binding Cassette Transporters - metabolism
Cardiac fibroblasts
Cardiology and cardiovascular system
Cardiovascular
Cell Proliferation - drug effects
Cells, Cultured
Cellular Biology
Fibroblasts - cytology
Fibroblasts - drug effects
Fibroblasts - metabolism
Fibroblasts - secretion
Gene Expression Regulation - drug effects
Glyburide - pharmacology
Heart Ventricles - cytology
Heart Ventricles - metabolism
Human health and pathology
IL-6
Interleukin-6 - secretion
Ion Channel Gating - drug effects
K-channel
KATP Channels
Life Sciences
Lysophospholipids - pharmacology
Mice
Pharmaceutical sciences
Pharmacology
Pinacidil - pharmacology
Potassium Channels, Inwardly Rectifying - genetics
Potassium Channels, Inwardly Rectifying - metabolism
Protein Subunits - genetics
Protein Subunits - metabolism
Receptors, Drug - genetics
Receptors, Drug - metabolism
RNA, Messenger - genetics
RNA, Messenger - metabolism
Sphingosine - analogs & derivatives
Sphingosine - pharmacology
Sphingosine-1-phosphate
Subcellular Processes
Sulfonylurea Receptors
SUR2/Kir6.1
Title Molecular and functional characterization of a new potassium conductance in mouse ventricular fibroblasts
URI https://www.clinicalkey.es/playcontent/1-s2.0-S0022282808014752
https://dx.doi.org/10.1016/j.yjmcc.2008.12.016
https://www.ncbi.nlm.nih.gov/pubmed/19166858
https://search.proquest.com/docview/67008780
https://hal.science/hal-00397628
Volume 46
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