Atlas of Circadian Metabolism Reveals System-wide Coordination and Communication between Clocks

Kenneth A. Dyar; Dominik Lutter; Anna Artati; Nicholas J. Ceglia; Yu Liu; Danny Armenta; Martin Jastroch; Sandra Schneider; Sara de Mateo; Marlene Cervantes; Serena Abbondante; Paola Tognini; Ricardo Orozco-Solis; Kenichiro Kinouchi; Christina Wang; Ronald Swerdloff; Seba Nadeef; Selma Masri; Pierre Magistretti; Valerio Orlando; Emiliana Borrelli; N. Henriette Uhlenhaut; Pierre Baldi; Jerzy Adamski; Matthias H. Tschöp; Kristin Eckel-Mahan; Paolo Sassone-Corsi

doi:10.1016/j.cell.2018.08.042

Atlas of Circadian Metabolism Reveals System-wide Coordination and Communication between Clocks

Kenneth A. Dyar, Dominik Lutter, Anna Artati, Nicholas J. Ceglia, Yu Liu, Danny Armenta, Martin Jastroch, Sandra Schneider, Sara de Mateo, Marlene Cervantes, Serena Abbondante, Paola Tognini, Ricardo Orozco-Solis, Kenichiro Kinouchi, Christina Wang, Ronald Swerdloff, Seba Nadeef, Selma Masri, Pierre Magistretti, Valerio OrlandoEmiliana Borrelli, N. Henriette Uhlenhaut, Pierre Baldi, Jerzy Adamski^*, Matthias H. Tschöp, Kristin Eckel-Mahan, Paolo Sassone-Corsi

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

201 Scopus citations

Abstract

Metabolic diseases are often characterized by circadian misalignment in different tissues, yet how altered coordination and communication among tissue clocks relate to specific pathogenic mechanisms remains largely unknown. Applying an integrated systems biology approach, we performed 24-hr metabolomics profiling of eight mouse tissues simultaneously. We present a temporal and spatial atlas of circadian metabolism in the context of systemic energy balance and under chronic nutrient stress (high-fat diet [HFD]). Comparative analysis reveals how the repertoires of tissue metabolism are linked and gated to specific temporal windows and how this highly specialized communication and coherence among tissue clocks is rewired by nutrient challenge. Overall, we illustrate how dynamic metabolic relationships can be reconstructed across time and space and how integration of circadian metabolomics data from multiple tissues can improve our understanding of health and disease. Circadian metabolite profiles of eight different tissues under standard and high-fat diet uncover highly specialized communication and coherence among tissue clocks and how this is rewired by nutrient challenge.

Original language	English (US)
Pages (from-to)	1571-1585.e11
Journal	Cell
Volume	174
Issue number	6
DOIs	https://doi.org/10.1016/j.cell.2018.08.042
State	Published - Sep 6 2018

Bibliographical note

Funding Information:
This work was supported by NIH grant GM123558 and DARPA grant D17AP00002 (P.B.); DFG Emmy Noether NHU 275/1-1 (N.H.U.); the Alexander von Humboldt Foundation (M.H.T.); NIH DK114037 (K.E.M.); by INSERM (Institut National de la Sante et de la Recherche Medicale, France), KAUST (King Abdullah University of Science and Technology), National Institutes of Health , and Novo Nordisk Foundation Challenge Grant NNF140C0011493 (P.S.-C.); and by the German Federal Ministry of Education and Research (BMBF) to the German Center Diabetes Research (DZD e.V.) grant to J.A.

Funding Information:
This work was supported by NIH grant GM123558 and DARPA grant D17AP00002 (P.B.); DFG Emmy Noether NHU 275/1-1 (N.H.U.); the Alexander von Humboldt Foundation (M.H.T.); NIH DK114037 (K.E.M.); by INSERM (Institut National de la Sante et de la Recherche Medicale, France), KAUST (King Abdullah University of Science and Technology), National Institutes of Health, and Novo Nordisk Foundation Challenge Grant NNF140C0011493 (P.S.-C.); and by the German Federal Ministry of Education and Research (BMBF) to the German Center Diabetes Research (DZD e.V.) grant to J.A.

Publisher Copyright:
© 2018 Elsevier Inc.

Keywords

CircadiOmics
circadian rhythms
clock
high-fat diet
metabolism
metabolomics

ASJC Scopus subject areas

Biochemistry, Genetics and Molecular Biology(all)

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10.1016/j.cell.2018.08.042

Cite this

Dyar, K. A., Lutter, D., Artati, A., Ceglia, N. J., Liu, Y., Armenta, D., Jastroch, M., Schneider, S., de Mateo, S., Cervantes, M., Abbondante, S., Tognini, P., Orozco-Solis, R., Kinouchi, K., Wang, C., Swerdloff, R., Nadeef, S., Masri, S., Magistretti, P., ... Sassone-Corsi, P. (2018). Atlas of Circadian Metabolism Reveals System-wide Coordination and Communication between Clocks. Cell, 174(6), 1571-1585.e11. https://doi.org/10.1016/j.cell.2018.08.042

@article{97eb863c23244982b0b0e34cd801691c,

title = "Atlas of Circadian Metabolism Reveals System-wide Coordination and Communication between Clocks",

abstract = "Metabolic diseases are often characterized by circadian misalignment in different tissues, yet how altered coordination and communication among tissue clocks relate to specific pathogenic mechanisms remains largely unknown. Applying an integrated systems biology approach, we performed 24-hr metabolomics profiling of eight mouse tissues simultaneously. We present a temporal and spatial atlas of circadian metabolism in the context of systemic energy balance and under chronic nutrient stress (high-fat diet [HFD]). Comparative analysis reveals how the repertoires of tissue metabolism are linked and gated to specific temporal windows and how this highly specialized communication and coherence among tissue clocks is rewired by nutrient challenge. Overall, we illustrate how dynamic metabolic relationships can be reconstructed across time and space and how integration of circadian metabolomics data from multiple tissues can improve our understanding of health and disease. Circadian metabolite profiles of eight different tissues under standard and high-fat diet uncover highly specialized communication and coherence among tissue clocks and how this is rewired by nutrient challenge.",

keywords = "CircadiOmics, circadian rhythms, clock, high-fat diet, metabolism, metabolomics",

author = "Dyar, {Kenneth A.} and Dominik Lutter and Anna Artati and Ceglia, {Nicholas J.} and Yu Liu and Danny Armenta and Martin Jastroch and Sandra Schneider and {de Mateo}, Sara and Marlene Cervantes and Serena Abbondante and Paola Tognini and Ricardo Orozco-Solis and Kenichiro Kinouchi and Christina Wang and Ronald Swerdloff and Seba Nadeef and Selma Masri and Pierre Magistretti and Valerio Orlando and Emiliana Borrelli and Uhlenhaut, {N. Henriette} and Pierre Baldi and Jerzy Adamski and Tsch{\"o}p, {Matthias H.} and Kristin Eckel-Mahan and Paolo Sassone-Corsi",

note = "Funding Information: This work was supported by NIH grant GM123558 and DARPA grant D17AP00002 (P.B.); DFG Emmy Noether NHU 275/1-1 (N.H.U.); the Alexander von Humboldt Foundation (M.H.T.); NIH DK114037 (K.E.M.); by INSERM (Institut National de la Sante et de la Recherche Medicale, France), KAUST (King Abdullah University of Science and Technology), National Institutes of Health , and Novo Nordisk Foundation Challenge Grant NNF140C0011493 (P.S.-C.); and by the German Federal Ministry of Education and Research (BMBF) to the German Center Diabetes Research (DZD e.V.) grant to J.A. Funding Information: This work was supported by NIH grant GM123558 and DARPA grant D17AP00002 (P.B.); DFG Emmy Noether NHU 275/1-1 (N.H.U.); the Alexander von Humboldt Foundation (M.H.T.); NIH DK114037 (K.E.M.); by INSERM (Institut National de la Sante et de la Recherche Medicale, France), KAUST (King Abdullah University of Science and Technology), National Institutes of Health, and Novo Nordisk Foundation Challenge Grant NNF140C0011493 (P.S.-C.); and by the German Federal Ministry of Education and Research (BMBF) to the German Center Diabetes Research (DZD e.V.) grant to J.A. Publisher Copyright: {\textcopyright} 2018 Elsevier Inc.",

year = "2018",

month = sep,

day = "6",

doi = "10.1016/j.cell.2018.08.042",

language = "English (US)",

volume = "174",

pages = "1571--1585.e11",

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Dyar, KA, Lutter, D, Artati, A, Ceglia, NJ, Liu, Y, Armenta, D, Jastroch, M, Schneider, S, de Mateo, S, Cervantes, M, Abbondante, S, Tognini, P, Orozco-Solis, R, Kinouchi, K, Wang, C, Swerdloff, R, Nadeef, S, Masri, S, Magistretti, P , Orlando, V, Borrelli, E, Uhlenhaut, NH, Baldi, P, Adamski, J, Tschöp, MH, Eckel-Mahan, K & Sassone-Corsi, P 2018, 'Atlas of Circadian Metabolism Reveals System-wide Coordination and Communication between Clocks', Cell, vol. 174, no. 6, pp. 1571-1585.e11. https://doi.org/10.1016/j.cell.2018.08.042

TY - JOUR

T1 - Atlas of Circadian Metabolism Reveals System-wide Coordination and Communication between Clocks

AU - Dyar, Kenneth A.

AU - Lutter, Dominik

AU - Artati, Anna

AU - Ceglia, Nicholas J.

AU - Liu, Yu

AU - Armenta, Danny

AU - Jastroch, Martin

AU - Schneider, Sandra

AU - de Mateo, Sara

AU - Cervantes, Marlene

AU - Abbondante, Serena

AU - Tognini, Paola

AU - Orozco-Solis, Ricardo

AU - Kinouchi, Kenichiro

AU - Wang, Christina

AU - Swerdloff, Ronald

AU - Nadeef, Seba

AU - Masri, Selma

AU - Magistretti, Pierre

AU - Orlando, Valerio

AU - Borrelli, Emiliana

AU - Uhlenhaut, N. Henriette

AU - Baldi, Pierre

AU - Adamski, Jerzy

AU - Tschöp, Matthias H.

AU - Eckel-Mahan, Kristin

AU - Sassone-Corsi, Paolo

N1 - Funding Information: This work was supported by NIH grant GM123558 and DARPA grant D17AP00002 (P.B.); DFG Emmy Noether NHU 275/1-1 (N.H.U.); the Alexander von Humboldt Foundation (M.H.T.); NIH DK114037 (K.E.M.); by INSERM (Institut National de la Sante et de la Recherche Medicale, France), KAUST (King Abdullah University of Science and Technology), National Institutes of Health , and Novo Nordisk Foundation Challenge Grant NNF140C0011493 (P.S.-C.); and by the German Federal Ministry of Education and Research (BMBF) to the German Center Diabetes Research (DZD e.V.) grant to J.A. Funding Information: This work was supported by NIH grant GM123558 and DARPA grant D17AP00002 (P.B.); DFG Emmy Noether NHU 275/1-1 (N.H.U.); the Alexander von Humboldt Foundation (M.H.T.); NIH DK114037 (K.E.M.); by INSERM (Institut National de la Sante et de la Recherche Medicale, France), KAUST (King Abdullah University of Science and Technology), National Institutes of Health, and Novo Nordisk Foundation Challenge Grant NNF140C0011493 (P.S.-C.); and by the German Federal Ministry of Education and Research (BMBF) to the German Center Diabetes Research (DZD e.V.) grant to J.A. Publisher Copyright: © 2018 Elsevier Inc.

PY - 2018/9/6

Y1 - 2018/9/6

N2 - Metabolic diseases are often characterized by circadian misalignment in different tissues, yet how altered coordination and communication among tissue clocks relate to specific pathogenic mechanisms remains largely unknown. Applying an integrated systems biology approach, we performed 24-hr metabolomics profiling of eight mouse tissues simultaneously. We present a temporal and spatial atlas of circadian metabolism in the context of systemic energy balance and under chronic nutrient stress (high-fat diet [HFD]). Comparative analysis reveals how the repertoires of tissue metabolism are linked and gated to specific temporal windows and how this highly specialized communication and coherence among tissue clocks is rewired by nutrient challenge. Overall, we illustrate how dynamic metabolic relationships can be reconstructed across time and space and how integration of circadian metabolomics data from multiple tissues can improve our understanding of health and disease. Circadian metabolite profiles of eight different tissues under standard and high-fat diet uncover highly specialized communication and coherence among tissue clocks and how this is rewired by nutrient challenge.

AB - Metabolic diseases are often characterized by circadian misalignment in different tissues, yet how altered coordination and communication among tissue clocks relate to specific pathogenic mechanisms remains largely unknown. Applying an integrated systems biology approach, we performed 24-hr metabolomics profiling of eight mouse tissues simultaneously. We present a temporal and spatial atlas of circadian metabolism in the context of systemic energy balance and under chronic nutrient stress (high-fat diet [HFD]). Comparative analysis reveals how the repertoires of tissue metabolism are linked and gated to specific temporal windows and how this highly specialized communication and coherence among tissue clocks is rewired by nutrient challenge. Overall, we illustrate how dynamic metabolic relationships can be reconstructed across time and space and how integration of circadian metabolomics data from multiple tissues can improve our understanding of health and disease. Circadian metabolite profiles of eight different tissues under standard and high-fat diet uncover highly specialized communication and coherence among tissue clocks and how this is rewired by nutrient challenge.

KW - CircadiOmics

KW - circadian rhythms

KW - clock

KW - high-fat diet

KW - metabolism

KW - metabolomics

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U2 - 10.1016/j.cell.2018.08.042

DO - 10.1016/j.cell.2018.08.042

M3 - Article

C2 - 30193114

AN - SCOPUS:85052853191

SN - 0092-8674

VL - 174

SP - 1571-1585.e11

JO - Cell

JF - Cell

IS - 6

ER -

Atlas of Circadian Metabolism Reveals System-wide Coordination and Communication between Clocks

Abstract

Bibliographical note

Keywords

ASJC Scopus subject areas

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