The cardiomyocyte molecular clock regulates the circadian expression of Kcnh2 and contributes to ventricular repolarization
Open accessAbstract
Background Sudden cardiac death (SCD) follows a diurnal variation. Data suggest the timing of SCD is influenced by circadian (~24-hour) changes in neurohumoral and cardiomyocyte-specific regulation of the heart's electrical properties. The basic helix-loop-helix transcription factors brain muscle arnt-like1 (BMAL1) and circadian locomotor output control kaput (CLOCK) coordinate the circadian expression of select genes.Objective We sought to test whether Bmal1 expression in cardiomyocytes contributes to K(+) channel expression and diurnal changes in ventricular repolarization.Methods We used transgenic mice that allow for the inducible cardiomyocyte-specific deletion of Bmal1 (iCSΔBmal1(-/-)). We used quantitative polymerase chain reaction, voltage clamping, promoter-reporter bioluminescence assays, and electrocardiographic telemetry.Results Although several K(+) channel gene transcripts were downregulated in iCSΔBmal1(-/-)mouse hearts, only Kcnh2 exhibited a robust circadian pattern of expression that was disrupted in iCSΔBmal1(-/-) hearts. Kcnh2 underlies the rapidly activating delayed-rectifier K(+) current, and the rapidly activating delayed-rectifier K(+) current recorded from iCSΔBmal1(-/-) ventricular cardiomyocytes was ~50% smaller than control ventricular myocytes. Promoter-reporter assays demonstrated that the human Kcnh2 promoter is transactivated by the coexpression of BMAL1 and CLOCK. Electrocardiographic analysis showed that iCSΔBmal1(-/-) mice developed a prolongation in the heart rate-corrected QT interval during the light (resting) phase. This was secondary to an augmented circadian rhythm in the uncorrected QT interval without a corresponding change in the RR interval.Conclusion The molecular clock in the heart regulates the circadian expression of Kcnh2, modifies K(+) channel gene expression, and is important for normal ventricular repolarization. Disruption of the cardiomyocyte circadian clock mechanism likely unmasks diurnal changes in ventricular repolarization that could contribute to an increased risk of cardiac arrhythmias/SCD.
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Cardiomyocyte-specific deletion of Bmal1 results in loss of normal circadian expression of the Na+ and K+ channels resulting in decreased heart rate and increased risk of arrhythmias, which could contribute to sudden cardiac death.
“Cardiomyocyte-specific deletion of Bmal1 results in loss of normal circadian expression of the Na + and K + channels resulting in decreased HR and increased risk of arrhythmias (66), which could contribute to sudden cardiac death (67).”
From Role of the circadian system in cardiovascular disease (2018) · cites this paper as [67]
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- Authors
- Schroder, E. A., Burgess, D. E., Zhang, X., Lefta, M., Smith, J. L., Patwardhan, A., Bartos, D. C., Elayi, C. S., Esser, K. A., & Delisle, B. P.
- Affiliations
- University of Kentucky (US)
- Corresponding author
- Delisle, Brian P.
- ORCID
- Venue
- Heart Rhythm
- Publisher
- Elsevier BV
- Published
- 2015-06
- Volume
- 12
- Issue
- 6
- Pages
- 1306-1314
- ISSN
- 1547-5271 (ISSN-L)
- PMC
- PMC4541807
- OpenAlex
- W2037124960
- Cited by
- 86
- References
- 25
- Citations by year
- 2026: 9 · 2025: 8 · 2024: 8 · 2023: 6 · 2022: 10 · 2021: 8 · 2020: 13 · 2019: 7 · 2018: 7 · 2017: 3 · 2016: 6 · 2015: 1
- FWCI
- 4.12
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Heart Rhythm (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Heart, Lung, and Blood Institute (R01HL087039)
- National Institute of Environmental Health Sciences (RC1ES018636)
- National Institute of Arthritis and Musculoskeletal and Skin Diseases (R01AR066082, R01AR055246, AR55246)
- Topics
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiac electrophysiology and arrhythmias
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Circadian rhythm and melatonin
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ion channel regulation and function
- Keywords
- Bmal1, KCNH2, ventricular repolarization, circadian gene expression, sudden cardiac death, diurnal variation, QT interval, cardiac arrhythmias
- MeSH terms
- ERG1 Potassium Channel, Animals, Circadian Rhythm, Cloning, Molecular, Electrocardiography, Heart Rate, Luminescent Measurements, Mice, Transgenic, Potassium Channels, Gene Expression, Myocytes, Cardiac, Mice, Ether-A-Go-Go Potassium Channels, ARNTL Transcription Factors
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