A circadian clock in the sinus node mediates day-night rhythms in Hcn4 and heart rate.


Journal

Heart rhythm
ISSN: 1556-3871
Titre abrégé: Heart Rhythm
Pays: United States
ID NLM: 101200317

Informations de publication

Date de publication:
05 2021
Historique:
received: 05 05 2020
revised: 09 11 2020
accepted: 21 11 2020
pubmed: 6 12 2020
medline: 19 1 2022
entrez: 5 12 2020
Statut: ppublish

Résumé

Heart rate follows a diurnal variation, and slow heart rhythms occur primarily at night. The lower heart rate during sleep is assumed to be neural in origin, but here we tested whether a day-night difference in intrinsic pacemaking is involved. In vivo and in vitro electrocardiographic recordings, vagotomy, transgenics, quantitative polymerase chain reaction, Western blotting, immunohistochemistry, patch clamp, reporter bioluminescence recordings, and chromatin immunoprecipitation were used. The day-night difference in the average heart rate of mice was independent of fluctuations in average locomotor activity and persisted under pharmacological, surgical, and transgenic interruption of autonomic input to the heart. Spontaneous beating rate of isolated (ie, denervated) sinus node (SN) preparations exhibited a day-night rhythm concomitant with rhythmic messenger RNA expression of ion channels including hyperpolarization-activated cyclic nucleotide-gated potassium channel 4 (HCN4). In vitro studies demonstrated 24-hour rhythms in the human HCN4 promoter and the corresponding funny current. The day-night heart rate difference in mice was abolished by HCN block, both in vivo and in the isolated SN. Rhythmic expression of canonical circadian clock transcription factors, for example, Brain and muscle ARNT-Like 1 (BMAL1) and Cryptochrome (CRY) was identified in the SN and disruption of the local clock (by cardiomyocyte-specific knockout of Bmal1) abolished the day-night difference in Hcn4 and intrinsic heart rate. Chromatin immunoprecipitation revealed specific BMAL1 binding sites on Hcn4, linking the local clock with intrinsic rate control. The circadian variation in heart rate involves SN local clock-dependent Hcn4 rhythmicity. Data reveal a novel regulator of heart rate and mechanistic insight into bradycardia during sleep.

Sections du résumé

BACKGROUND
Heart rate follows a diurnal variation, and slow heart rhythms occur primarily at night.
OBJECTIVE
The lower heart rate during sleep is assumed to be neural in origin, but here we tested whether a day-night difference in intrinsic pacemaking is involved.
METHODS
In vivo and in vitro electrocardiographic recordings, vagotomy, transgenics, quantitative polymerase chain reaction, Western blotting, immunohistochemistry, patch clamp, reporter bioluminescence recordings, and chromatin immunoprecipitation were used.
RESULTS
The day-night difference in the average heart rate of mice was independent of fluctuations in average locomotor activity and persisted under pharmacological, surgical, and transgenic interruption of autonomic input to the heart. Spontaneous beating rate of isolated (ie, denervated) sinus node (SN) preparations exhibited a day-night rhythm concomitant with rhythmic messenger RNA expression of ion channels including hyperpolarization-activated cyclic nucleotide-gated potassium channel 4 (HCN4). In vitro studies demonstrated 24-hour rhythms in the human HCN4 promoter and the corresponding funny current. The day-night heart rate difference in mice was abolished by HCN block, both in vivo and in the isolated SN. Rhythmic expression of canonical circadian clock transcription factors, for example, Brain and muscle ARNT-Like 1 (BMAL1) and Cryptochrome (CRY) was identified in the SN and disruption of the local clock (by cardiomyocyte-specific knockout of Bmal1) abolished the day-night difference in Hcn4 and intrinsic heart rate. Chromatin immunoprecipitation revealed specific BMAL1 binding sites on Hcn4, linking the local clock with intrinsic rate control.
CONCLUSION
The circadian variation in heart rate involves SN local clock-dependent Hcn4 rhythmicity. Data reveal a novel regulator of heart rate and mechanistic insight into bradycardia during sleep.

Identifiants

pubmed: 33278629
pii: S1547-5271(20)31130-9
doi: 10.1016/j.hrthm.2020.11.026
pmc: PMC8073545
pii:
doi:

Substances chimiques

Hcn4 protein, mouse 0
Hyperpolarization-Activated Cyclic Nucleotide-Gated Channels 0
RNA 63231-63-0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

801-810

Subventions

Organisme : British Heart Foundation
ID : FS/19/1/34035
Pays : United Kingdom
Organisme : British Heart Foundation
ID : RG/11/18/29257
Pays : United Kingdom
Organisme : Biotechnology and Biological Sciences Research Council
ID : BB/J003441
Pays : United Kingdom
Organisme : British Heart Foundation
ID : PG/15/16/31330
Pays : United Kingdom

Commentaires et corrections

Type : CommentIn

Informations de copyright

Copyright © 2020 Heart Rhythm Society. Published by Elsevier Inc. All rights reserved.

Auteurs

Alicia D'Souza (A)

Division of Cardiovascular Sciences, University of Manchester, Manchester, United Kingdom. Electronic address: alicia.dsouza@manchester.ac.uk.

Yanwen Wang (Y)

Division of Cardiovascular Sciences, University of Manchester, Manchester, United Kingdom.

Cali Anderson (C)

Division of Cardiovascular Sciences, University of Manchester, Manchester, United Kingdom.

Annalisa Bucchi (A)

Department of Biosciences, University of Milan, Milan, Italy.

Mirko Baruscotti (M)

Department of Biosciences, University of Milan, Milan, Italy.

Servé Olieslagers (S)

Department of Cardiology, Maastricht University, Maastricht, The Netherlands.

Pietro Mesirca (P)

Institut de Génomique Fonctionnelle, Université de Montpellie, CNRS, Montpellier, France.

Anne Berit Johnsen (AB)

Department of Circulation and Medical Imaging, Norwegian University of Science and Technology, Trondheim, Norway.

Svetlana Mastitskaya (S)

Neuroscience, Physiology and Pharmacology, University College London, London, United Kingdom.

Haibo Ni (H)

Division of Cardiovascular Sciences, University of Manchester, Manchester, United Kingdom.

Yu Zhang (Y)

Division of Cardiovascular Sciences, University of Manchester, Manchester, United Kingdom.

Nicholas Black (N)

Division of Cardiovascular Sciences, University of Manchester, Manchester, United Kingdom.

Charlotte Cox (C)

Division of Cardiovascular Sciences, University of Manchester, Manchester, United Kingdom.

Sven Wegner (S)

Division of Cardiovascular Sciences, University of Manchester, Manchester, United Kingdom.

Beatriz Bano-Otalora (B)

Division of Cardiovascular Sciences, University of Manchester, Manchester, United Kingdom.

Cheryl Petit (C)

Division of Cardiovascular Sciences, University of Manchester, Manchester, United Kingdom.

Eleanor Gill (E)

Division of Cardiovascular Sciences, University of Manchester, Manchester, United Kingdom.

Sunil Jit R J Logantha (SJRJ)

Division of Cardiovascular Sciences, University of Manchester, Manchester, United Kingdom; Liverpool Centre for Cardiovascular Sciences, University of Liverpool, Liverpool, UK.

Halina Dobrzynski (H)

Division of Cardiovascular Sciences, University of Manchester, Manchester, United Kingdom.

Nick Ashton (N)

Division of Cardiovascular Sciences, University of Manchester, Manchester, United Kingdom.

George Hart (G)

Division of Cardiovascular Sciences, University of Manchester, Manchester, United Kingdom.

Rai Zhang (R)

School of Civil, Aerospace and Mechanical Engineering, University of Bristol, Bristol, United Kingdom.

Henggui Zhang (H)

Division of Cardiovascular Sciences, University of Manchester, Manchester, United Kingdom.

Elizabeth J Cartwright (EJ)

Division of Cardiovascular Sciences, University of Manchester, Manchester, United Kingdom.

Ulrik Wisloff (U)

Department of Circulation and Medical Imaging, Norwegian University of Science and Technology, Trondheim, Norway.

Matteo E Mangoni (ME)

Department of Biomedical Sciences, Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, Denmark.

Paula A da Costa Martins (PA)

Department of Cardiology, Maastricht University, Maastricht, The Netherlands.

Hugh D Piggins (HD)

School of Physiology, Pharmacology & Neuroscience, University of Bristol, Bristol, United Kingdom.

Dario DiFrancesco (D)

Department of Biosciences, University of Milan, Milan, Italy; IBF-CNR, Milan, Italy.

Mark R Boyett (MR)

Division of Cardiovascular Sciences, University of Manchester, Manchester, United Kingdom; Department of Biomedical Sciences, Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, Denmark.

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