TY - JOUR
T1 - Reshaping circadian metabolism in the suprachiasmatic nucleus and prefrontal cortex by nutritional challenge
AU - Tognini, Paola
AU - Samad, Muntaha
AU - Kinouchi, Kenichiro
AU - Liu, Yu
AU - Helbling, Jean Christophe
AU - Moisan, Marie Pierre
AU - Eckel-Mahan, Kristin L.
AU - Baldi, Pierre
AU - Sassone-Corsi, Paolo
N1 - Funding Information:
ACKNOWLEDGMENTS. We thank all the members of the P.S.-C. laboratory for constructive comments and Jeff Bucktal and Jason Kinchen (Metabolon) for advice on the analysis of metabolic profiles. This work was supported by the NIH (Grant DA036408), INSERM, and Novo Nordisk (Foundation Challenge Grant, to P.S.-C.). K.K. was supported by a Japan Society for the Promotion of Science fellowship. The work of P.B. and Y.L. was supported in part by NIH Grant GM123558 and Defense Advanced Research Projects Agency Grant D17AP00002 (to P.B.). P.T. was supported by the Human Frontiers Science Program (LT 000576/2013) and the European Commission (H2020-MSCA-IF-2016 749697 GaMePLAY).
Publisher Copyright:
© 2020 National Academy of Sciences. All rights reserved.
PY - 2020/11/24
Y1 - 2020/11/24
N2 - Food is a powerful entrainment cue for circadian clocks in peripheral tissues, and changes in the composition of nutrients have been demonstrated to metabolically reprogram peripheral clocks. However, how food challenges may influence circadian metabolism of the master clock in the suprachiasmatic nucleus (SCN) or in other brain areas is poorly understood. Using high-throughput metabolomics, we studied the circadian metabolome profiles of the SCN and medial prefrontal cortex (mPFC) in lean mice compared with mice challenged with a high-fat diet (HFD). Both the mPFC and the SCN displayed a robust cyclic metabolism, with a strikingly high sensitivity to HFD perturbation in an area-specific manner. The phase and amplitude of oscillations were drastically different between the SCN and mPFC, and the metabolic pathways impacted by HFD were remarkably region-dependent. Furthermore, HFD induced a significant increase in the number of cycling metabolites exclusively in the SCN, revealing an unsuspected susceptibility of the master clock to food stress.
AB - Food is a powerful entrainment cue for circadian clocks in peripheral tissues, and changes in the composition of nutrients have been demonstrated to metabolically reprogram peripheral clocks. However, how food challenges may influence circadian metabolism of the master clock in the suprachiasmatic nucleus (SCN) or in other brain areas is poorly understood. Using high-throughput metabolomics, we studied the circadian metabolome profiles of the SCN and medial prefrontal cortex (mPFC) in lean mice compared with mice challenged with a high-fat diet (HFD). Both the mPFC and the SCN displayed a robust cyclic metabolism, with a strikingly high sensitivity to HFD perturbation in an area-specific manner. The phase and amplitude of oscillations were drastically different between the SCN and mPFC, and the metabolic pathways impacted by HFD were remarkably region-dependent. Furthermore, HFD induced a significant increase in the number of cycling metabolites exclusively in the SCN, revealing an unsuspected susceptibility of the master clock to food stress.
KW - Circadian clock
KW - High-fat diet
KW - Metabolome reorganization
KW - Prefrontal cortex
KW - Suprachiasmatic nucleus
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U2 - 10.1073/pnas.2016589117
DO - 10.1073/pnas.2016589117
M3 - Article
C2 - 33172990
AN - SCOPUS:85096884409
SN - 0027-8424
VL - 117
SP - 29904
EP - 29913
JO - Proceedings of the National Academy of Sciences of the United States of America
JF - Proceedings of the National Academy of Sciences of the United States of America
IS - 47
ER -