Liver and muscle circadian clocks cooperate to support glucose tolerance in mice

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• dc.contributor.author Smith, Jacob G.
• dc.contributor.author Kumar, Arun
• dc.contributor.author Deryagin, Oleg
• dc.contributor.author Vaca Dempere, Mireia, 1994-
• dc.contributor.author Sica, Valentina
• dc.contributor.author Welz, Patrick-Simon
• dc.contributor.author Muñoz Cánoves, Pura, 1962-
• dc.contributor.author Sassone-Corsi, Paolo
• dc.date.accessioned 2023-06-23T06:34:22Z
• dc.date.available 2023-06-23T06:34:22Z
• dc.date.issued 2023
• dc.description.abstract Physiology is regulated by interconnected cell and tissue circadian clocks. Disruption of the rhythms generated by the concerted activity of these clocks is associated with metabolic disease. Here we tested the interactions between clocks in two critical components of organismal metabolism, liver and skeletal muscle, by rescuing clock function either in each organ separately or in both organs simultaneously in otherwise clock-less mice. Experiments showed that individual clocks are partially sufficient for tissue glucose metabolism, yet the connections between both tissue clocks coupled to daily feeding rhythms support systemic glucose tolerance. This synergy relies in part on local transcriptional control of the glucose machinery, feeding-responsive signals such as insulin, and metabolic cycles that connect the muscle and liver. We posit that spatiotemporal mechanisms of muscle and liver play an essential role in the maintenance of systemic glucose homeostasis and that disrupting this diurnal coordination can contribute to metabolic disease.
• dc.description.sponsorship This paper is dedicated to Paolo Sassone-Corsi, a hugely inspiring scientist and mentor who remains an important influence on our work. We also thank P.S.C. Lab animal technician S. Sato and laboratory manager W. Orquiz for their valued contributions, as well as Aintzane Rueda and Alfonso Saera-Vila at Sequentia Biotech (Barcelona) for their work on RNA sequencing read alignment and differential gene expression analysis. J.G.S. was supported by Zymo-CEM Postdoctoral Fellowship (Zymo Research) awarded at the University of California, Irvine. K.B.K. was supported by NIH, NIDDK F32 Fellowship – DK121425. T.S. was supported by a Japan Society for the Promotion of Science (JSPS) fellowship. C.M.G. was supported by the National Cancer Institute of the National Institutes of Health under award T32CA009054 and by the European Union’s Horizon 2020 research and innovation programme under the Marie Skłodowska-Curie grant agreement 749869. P.P. was funded by The Wenner-Gren Foundations, the Foundation Blanceflor Boncompagni Ludovisi, née Bildt and Tore Nilsson Foundation for Medical Science. V.S. was supported by the European Union’s Horizon 2020 research and innovation programme under the Marie Skłodowska-Curie grant agreement 895390. A.V. was supported by the Hitachi-Nomura postdoctoral fellowship awarded through the Department of Biological Chemistry at the University of California, Irvine. The work of S.C., M.S., and P.B. was in part supported by NIH grant GM123558. C.J. was supported by the AASLD Foundation Pinnacle Research Award in Liver Disease, the Edward Mallinckrodt, Jr. Foundation Award, and NIH/NIAAA R01 AA029124. P.-S.W. is supported by grant RYC2019026661-I funded by MCIN/AEI/10.13039/501100011033 and by “ESF Investing in your future.” Financial support for the S.M. laboratory is provided through the NIH/NCI (grants R01CA244519, R01CA259370, and K22CA212045). Research in the S.A.B. lab is supported partially by the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation programme (grant agreement 787041), the Government of Cataluña (SGR grant), the Government of Spain (MINECO), the La Marató/TV3 Foundation, the Foundation Lilliane Bettencourt, the Spanish Association for Cancer Research (AECC), and the Worldwide Cancer Research Foundation (WCRF). The IRB Barcelona is a Severo Ochoa Center of Excellence (MINECO award SEV-2015-0505). P.M.-C. acknowledges funding from MICINN-RTI2018-096068, ERC-2016-AdG-741966, LaCaixa-HEALTH-HR17-00040, MDA, UPGRADE-H2020-825825, AFM, DPP-Spain, Fundació La MaratóTV3- 80/19-202021, MWRF, and María-de-Maeztu Program for Units of Excellence to UPF (MDM-2014-0370), and the Severo-Ochoa Program for Centers of Excellence to CNIC (SEV2015-0505). Work in the P.S.-C. laboratory is supported by NIH grants R21DK114652 and R21AG053592, a Challenge Grant from the Novo Nordisk Foundation (NNF202585), KAUST funding (OSR-2019-CRG8-URF/1/4042), and via access to the Genomics High Throughput Facility Shared Resource of the Cancer Center Support Grant (CA-62203) and the UCI and NIH-shared instrumentation grants 1S10RR025496-01, 1S10OD010794-01, and 1S10OD021718-01.
• dc.format.mimetype application/pdf
• dc.identifier.citation Smith JG, Koronowski KB, Mortimer T, Sato T, Greco CM, Petrus P, et al. Liver and muscle circadian clocks cooperate to support glucose tolerance in mice. Cell Rep. 2023 Jun 1;42(6):112588. DOI: 10.1016/j.celrep.2023.112588
• dc.identifier.doi http://dx.doi.org/10.1016/j.celrep.2023.112588
• dc.identifier.issn 2211-1247
• dc.identifier.uri http://hdl.handle.net/10230/57313
• dc.language.iso eng
• dc.publisher Elsevier
• dc.relation.ispartof Cell Rep. 2023 Jun 1;42(6):112588
• dc.relation.projectID info:eu-repo/grantAgreement/EC/H2020/749869
• dc.relation.projectID info:eu-repo/grantAgreement/EC/H2020/787041
• dc.relation.projectID info:eu-repo/grantAgreement/EC/H2020/741966
• dc.relation.projectID info:eu-repo/grantAgreement/EC/H2020/825825
• dc.rights © 2023 The Author(s). This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
• dc.rights.accessRights info:eu-repo/semantics/openAccess
• dc.rights.uri http://creativecommons.org/licenses/by-nc-nd/4.0/
• dc.subject.keyword Bmal1
• dc.subject.keyword CP: Metabolism
• dc.subject.keyword Autonomy
• dc.subject.keyword Circadian rhythms
• dc.subject.keyword Endocrinology
• dc.subject.keyword Glucose
• dc.subject.keyword Inter-organ crosstalk
• dc.subject.keyword Liver
• dc.subject.keyword Metabolism
• dc.subject.keyword Muscle
• dc.subject.keyword Systems biology
• dc.title Liver and muscle circadian clocks cooperate to support glucose tolerance in mice
• dc.type info:eu-repo/semantics/article
• dc.type.version info:eu-repo/semantics/publishedVersion