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

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 an...

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Autores: Smith, Jacob G., Kumar, Arun, Deryagin, Oleg, Vaca Dempere, Mireia, 1994-, Sica, Valentina, Welz, Patrick-Simon, Muñoz Cánoves, Pura, 1962-, Sassone-Corsi, Paolo
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2023
País:España
Institución:Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)
Repositorio:Recercat. Dipósit de la Recerca de Catalunya
OAI Identifier:oai:recercat.cat:10230/57313
Acceso en línea:http://hdl.handle.net/10230/57313
http://dx.doi.org/10.1016/j.celrep.2023.112588
Access Level:acceso abierto
Palabra clave:Bmal1
CP: Metabolism
Autonomy
Circadian rhythms
Endocrinology
Glucose
Inter-organ crosstalk
Liver
Metabolism
Muscle
Systems biology
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oai_identifier_str oai:recercat.cat:10230/57313
network_acronym_str ES
network_name_str España
repository_id_str
dc.title.none.fl_str_mv Liver and muscle circadian clocks cooperate to support glucose tolerance in mice
title Liver and muscle circadian clocks cooperate to support glucose tolerance in mice
spellingShingle Liver and muscle circadian clocks cooperate to support glucose tolerance in mice
Smith, Jacob G.
Bmal1
CP: Metabolism
Autonomy
Circadian rhythms
Endocrinology
Glucose
Inter-organ crosstalk
Liver
Metabolism
Muscle
Systems biology
title_short Liver and muscle circadian clocks cooperate to support glucose tolerance in mice
title_full Liver and muscle circadian clocks cooperate to support glucose tolerance in mice
title_fullStr Liver and muscle circadian clocks cooperate to support glucose tolerance in mice
title_full_unstemmed Liver and muscle circadian clocks cooperate to support glucose tolerance in mice
title_sort Liver and muscle circadian clocks cooperate to support glucose tolerance in mice
dc.creator.none.fl_str_mv Smith, Jacob G.
Kumar, Arun
Deryagin, Oleg
Vaca Dempere, Mireia, 1994-
Sica, Valentina
Welz, Patrick-Simon
Muñoz Cánoves, Pura, 1962-
Sassone-Corsi, Paolo
author Smith, Jacob G.
author_facet Smith, Jacob G.
Kumar, Arun
Deryagin, Oleg
Vaca Dempere, Mireia, 1994-
Sica, Valentina
Welz, Patrick-Simon
Muñoz Cánoves, Pura, 1962-
Sassone-Corsi, Paolo
author_role author
author2 Kumar, Arun
Deryagin, Oleg
Vaca Dempere, Mireia, 1994-
Sica, Valentina
Welz, Patrick-Simon
Muñoz Cánoves, Pura, 1962-
Sassone-Corsi, Paolo
author2_role author
author
author
author
author
author
author
dc.subject.none.fl_str_mv Bmal1
CP: Metabolism
Autonomy
Circadian rhythms
Endocrinology
Glucose
Inter-organ crosstalk
Liver
Metabolism
Muscle
Systems biology
topic Bmal1
CP: Metabolism
Autonomy
Circadian rhythms
Endocrinology
Glucose
Inter-organ crosstalk
Liver
Metabolism
Muscle
Systems biology
description 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.
publishDate 2023
dc.date.none.fl_str_mv 2023
2023
2023
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10230/57313
http://dx.doi.org/10.1016/j.celrep.2023.112588
url http://hdl.handle.net/10230/57313
http://dx.doi.org/10.1016/j.celrep.2023.112588
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv Cell Rep. 2023 Jun 1;42(6):112588
info:eu-repo/grantAgreement/EC/H2020/749869
info:eu-repo/grantAgreement/EC/H2020/787041
info:eu-repo/grantAgreement/EC/H2020/741966
info:eu-repo/grantAgreement/EC/H2020/825825
dc.rights.none.fl_str_mv http://creativecommons.org/licenses/by-nc-nd/4.0/
info:eu-repo/semantics/openAccess
rights_invalid_str_mv http://creativecommons.org/licenses/by-nc-nd/4.0/
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv Elsevier
publisher.none.fl_str_mv Elsevier
dc.source.none.fl_str_mv reponame:Recercat. Dipósit de la Recerca de Catalunya
instname:Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)
instname_str Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)
reponame_str Recercat. Dipósit de la Recerca de Catalunya
collection Recercat. Dipósit de la Recerca de Catalunya
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spelling Liver and muscle circadian clocks cooperate to support glucose tolerance in miceSmith, Jacob G.Kumar, ArunDeryagin, OlegVaca Dempere, Mireia, 1994-Sica, ValentinaWelz, Patrick-SimonMuñoz Cánoves, Pura, 1962-Sassone-Corsi, PaoloBmal1CP: MetabolismAutonomyCircadian rhythmsEndocrinologyGlucoseInter-organ crosstalkLiverMetabolismMuscleSystems biologyPhysiology 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.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.Elsevier202320232023info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionapplication/pdfapplication/pdfhttp://hdl.handle.net/10230/57313http://dx.doi.org/10.1016/j.celrep.2023.112588reponame:Recercat. Dipósit de la Recerca de Catalunyainstname:Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)InglésCell Rep. 2023 Jun 1;42(6):112588info:eu-repo/grantAgreement/EC/H2020/749869info:eu-repo/grantAgreement/EC/H2020/787041info:eu-repo/grantAgreement/EC/H2020/741966info:eu-repo/grantAgreement/EC/H2020/825825© 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/).http://creativecommons.org/licenses/by-nc-nd/4.0/info:eu-repo/semantics/openAccessoai:recercat.cat:10230/573132026-05-29T05:05:01Z
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