Compensatory ion transport buffers daily protein rhythms to regulate osmotic balance and cellular physiology

Alessandra Stangherlin, Joseph L. Watson, David C. S. Wong, Silvia Barbiero, Aiwei Zeng, Estere Seinkmane, Sew Peak Chew, Andrew D. Beale, Edward A. Hayter, Alina Guna, Alison J. Inglis, Marrit Putker, Eline Bartolami, Stefan Matile, Nicolas Lequeux, Thomas Pons, Jason Day, Gerben van Ooijen, Rebecca M. Voorhees, David A. Bechtold, Emmanuel Derivery, Rachel S. Edgar, Peter Newham and John S. O’Neill ()
Additional contact information
Alessandra Stangherlin: MRC Laboratory of Molecular Biology
Joseph L. Watson: MRC Laboratory of Molecular Biology
David C. S. Wong: MRC Laboratory of Molecular Biology
Silvia Barbiero: MRC Laboratory of Molecular Biology
Aiwei Zeng: MRC Laboratory of Molecular Biology
Estere Seinkmane: MRC Laboratory of Molecular Biology
Sew Peak Chew: MRC Laboratory of Molecular Biology
Andrew D. Beale: MRC Laboratory of Molecular Biology
Edward A. Hayter: University of Manchester
Alina Guna: UCSF
Alison J. Inglis: California Institute of Technology
Marrit Putker: MRC Laboratory of Molecular Biology
Eline Bartolami: University of Geneva
Stefan Matile: University of Geneva
Nicolas Lequeux: Sorbonne Université
Thomas Pons: Sorbonne Université
Jason Day: University of Cambridge
Gerben van Ooijen: University of Edinburgh
Rebecca M. Voorhees: California Institute of Technology
David A. Bechtold: University of Manchester
Emmanuel Derivery: MRC Laboratory of Molecular Biology
Rachel S. Edgar: Imperial College London
Peter Newham: Clinical Pharmacology and Safety Sciences, R&D, AstraZeneca
John S. O’Neill: MRC Laboratory of Molecular Biology

Nature Communications, 2021, vol. 12, issue 1, 1-14

Abstract: Abstract Between 6–20% of the cellular proteome is under circadian control and tunes mammalian cell function with daily environmental cycles. For cell viability, and to maintain volume within narrow limits, the daily variation in osmotic potential exerted by changes in the soluble proteome must be counterbalanced. The mechanisms and consequences of this osmotic compensation have not been investigated before. In cultured cells and in tissue we find that compensation involves electroneutral active transport of Na+, K+, and Cl− through differential activity of SLC12A family cotransporters. In cardiomyocytes ex vivo and in vivo, compensatory ion fluxes confer daily variation in electrical activity. Perturbation of soluble protein abundance has commensurate effects on ion composition and cellular function across the circadian cycle. Thus, circadian regulation of the proteome impacts ion homeostasis with substantial consequences for the physiology of electrically active cells such as cardiomyocytes.

Date: 2021
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DOI: 10.1038/s41467-021-25942-4

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