Literature DB >> 33551824

Genetic Ablation of G Protein-Gated Inwardly Rectifying K+ Channels Prevents Training-Induced Sinus Bradycardia.

Isabelle Bidaud1,2, Alicia D'Souza3, Gabriella Forte3, Eleonora Torre1,2, Denis Greuet1, Steeve Thirard1, Cali Anderson3, Antony Chung You Chong1,2, Angelo G Torrente1,2, Julien Roussel1, Kevin Wickman4, Mark R Boyett5, Matteo E Mangoni1,2, Pietro Mesirca1,2.   

Abstract

Background: Endurance athletes are prone to bradyarrhythmias, which in the long-term may underscore the increased incidence of pacemaker implantation reported in this population. Our previous work in rodent models has shown training-induced sinus bradycardia to be due to microRNA (miR)-mediated transcriptional remodeling of the HCN4 channel, leading to a reduction of the "funny" (I f) current in the sinoatrial node (SAN). Objective: To test if genetic ablation of G-protein-gated inwardly rectifying potassium channel, also known as I KACh channels prevents sinus bradycardia induced by intensive exercise training in mice.
Methods: Control wild-type (WT) and mice lacking GIRK4 (Girk4 -/-), an integral subunit of I KACh were assigned to trained or sedentary groups. Mice in the trained group underwent 1-h exercise swimming twice a day for 28 days, 7 days per week. We performed electrocardiogram recordings and echocardiography in both groups at baseline, during and after the training period. At training cessation, mice were euthanized and SAN tissues were isolated for patch clamp recordings in isolated SAN cells and molecular profiling by quantitative PCR (qPCR) and western blotting.
Results: At swimming cessation trained WT mice presented with a significantly lower resting HR that was reversible by acute I KACh block whereas Girk4 -/- mice failed to develop a training-induced sinus bradycardia. In line with HR reduction, action potential rate, density of I f, as well as of T- and L-type Ca2+ currents (I CaT and I CaL ) were significantly reduced only in SAN cells obtained from WT-trained mice. I f reduction in WT mice was concomitant with downregulation of HCN4 transcript and protein, attributable to increased expression of corresponding repressor microRNAs (miRs) whereas reduced I CaL in WT mice was associated with reduced Cav1.3 protein levels. Strikingly, I KACh ablation suppressed all training-induced molecular remodeling observed in WT mice.
Conclusion: Genetic ablation of cardiac I KACh in mice prevents exercise-induced sinus bradycardia by suppressing training induced remodeling of inward currents I f, I CaT and I CaL due in part to the prevention of miR-mediated transcriptional remodeling of HCN4 and likely post transcriptional remodeling of Cav1.3. Strategies targeting cardiac I KACh may therefore represent an alternative to pacemaker implantation for bradyarrhythmias seen in some veteran athletes.
Copyright © 2021 Bidaud, D’Souza, Forte, Torre, Greuet, Thirard, Anderson, Chung You Chong, Torrente, Roussel, Wickman, Boyett, Mangoni and Mesirca.

Entities:  

Keywords:  G-protein-gated inwardly rectifying potassium 4 (Girk4); bradycardia; endurance athletes; hyperpolarization-activated cyclic nucleotide-gated 4 (HCN4) channel; sinoatrial node

Year:  2021        PMID: 33551824      PMCID: PMC7857143          DOI: 10.3389/fphys.2020.519382

Source DB:  PubMed          Journal:  Front Physiol        ISSN: 1664-042X            Impact factor:   4.566


  59 in total

1.  Is severe bradycardia in veteran athletes an indication for a permanent pacemaker?

Authors:  R J Northcote; A C Rankin; R Scullion; W Logan
Journal:  BMJ       Date:  1989-01-28

2.  Exercise training-induced bradycardia: evidence for enhanced parasympathetic regulation without changes in intrinsic sinoatrial node function.

Authors:  George E Billman; Kristen L Cagnoli; Thomas Csepe; Ning Li; Patrick Wright; Peter J Mohler; Vadim V Fedorov
Journal:  J Appl Physiol (1985)       Date:  2015-03-06

3.  Analysis of the chronotropic effect of acetylcholine on sinoatrial node cells.

Authors:  Henggui Zhang; Arun V Holden; Denis Noble; Mark R Boyett
Journal:  J Cardiovasc Electrophysiol       Date:  2002-05

Review 4.  A coupled SYSTEM of intracellular Ca2+ clocks and surface membrane voltage clocks controls the timekeeping mechanism of the heart's pacemaker.

Authors:  Edward G Lakatta; Victor A Maltsev; Tatiana M Vinogradova
Journal:  Circ Res       Date:  2010-03-05       Impact factor: 17.367

5.  Bradycardia and slowing of the atrioventricular conduction in mice lacking CaV3.1/alpha1G T-type calcium channels.

Authors:  Matteo E Mangoni; Achraf Traboulsie; Anne-Laure Leoni; Brigitte Couette; Laurine Marger; Khai Le Quang; Elodie Kupfer; Anne Cohen-Solal; José Vilar; Hee-Sup Shin; Denis Escande; Flavien Charpentier; Joël Nargeot; Philippe Lory
Journal:  Circ Res       Date:  2006-05-11       Impact factor: 17.367

6.  Contribution of L-type Ca2+ current to electrical activity in sinoatrial nodal myocytes of rabbits.

Authors:  E E Verheijck; A C van Ginneken; R Wilders; L N Bouman
Journal:  Am J Physiol       Date:  1999-03

7.  Effects of muscarinic receptor stimulation on Ca2+ transient, cAMP production and pacemaker frequency of rabbit sinoatrial node cells.

Authors:  Marcel M G J van Borren; Arie O Verkerk; Ronald Wilders; Najat Hajji; Jan G Zegers; Jan Bourier; Hanno L Tan; Etienne E Verheijck; Stephan L M Peters; Astrid E Alewijnse; Jan-Hindrik Ravesloot
Journal:  Basic Res Cardiol       Date:  2009-07-29       Impact factor: 17.165

8.  Electrocardiographic findings in male veteran endurance athletes.

Authors:  R J Northcote; G P Canning; D Ballantyne
Journal:  Br Heart J       Date:  1989-02

9.  Contribution of two types of calcium currents to the pacemaker potentials of rabbit sino-atrial node cells.

Authors:  N Hagiwara; H Irisawa; M Kameyama
Journal:  J Physiol       Date:  1988-01       Impact factor: 5.182

10.  Cardiac arrhythmia induced by genetic silencing of 'funny' (f) channels is rescued by GIRK4 inactivation.

Authors:  Pietro Mesirca; Jacqueline Alig; Angelo G Torrente; Jana Christina Müller; Laurine Marger; Anne Rollin; Claire Marquilly; Anne Vincent; Stefan Dubel; Isabelle Bidaud; Anne Fernandez; Anika Seniuk; Birgit Engeland; Jasmin Singh; Lucile Miquerol; Heimo Ehmke; Thomas Eschenhagen; Joel Nargeot; Kevin Wickman; Dirk Isbrandt; Matteo E Mangoni
Journal:  Nat Commun       Date:  2014-08-21       Impact factor: 14.919

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  2 in total

Review 1.  The multiple facets of mitochondrial regulations controlling cellular thermogenesis.

Authors:  Florian Beignon; Naig Gueguen; Hélène Tricoire-Leignel; César Mattei; Guy Lenaers
Journal:  Cell Mol Life Sci       Date:  2022-09-20       Impact factor: 9.207

2.  Proteomic Analysis of Cardiac Adaptation to Exercise by High Resolution Mass Spectrometry.

Authors:  Afnan Saleh Al-Menhali; Cali Anderson; Alexander V Gourine; Andrey Y Abramov; Alicia D'Souza; Morana Jaganjac
Journal:  Front Mol Biosci       Date:  2021-09-01
  2 in total

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