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Article

Time-of-Day Circadian Modulation of Grape-Seed Procyanidin Extract (GSPE) in Hepatic Mitochondrial Dynamics in Cafeteria-Diet-Induced Obese Rats

by
Romina M. Rodríguez
1,
Antonio J. Cortés-Espinar
1,
Jorge R. Soliz-Rueda
1,
Christine Feillet-Coudray
2,
François Casas
2,
Marina Colom-Pellicer
1,
Gerard Aragonès
1,
Javier Avila-Román
3,
Begoña Muguerza
1,
Miquel Mulero
1,* and
Maria Josepa Salvadó
1
1
Nutrigenomics Research Group, Department of Biochemistry and Biotechnology, Campus Sescelades, Universitat Rovira i Virgili, 43007 Tarragona, Spain
2
Muscle Dynamics and Metabolism (DMEM), National Research Institute for Agriculture, Food and Environment (INRAE), EMN, UMR 866, Université de Montpellier, 34090 Montpellier, France
3
Molecular and Applied Pharmacology Group (FARMOLAP), Department of Pharmacology, Faculty of Pharmacy, Reina Mercedes Campus, Universidad de Sevilla, 41012 Sevilla, Spain
*
Author to whom correspondence should be addressed.
Nutrients 2022, 14(4), 774; https://doi.org/10.3390/nu14040774
Submission received: 25 December 2021 / Revised: 4 February 2022 / Accepted: 8 February 2022 / Published: 12 February 2022
(This article belongs to the Special Issue Nutrition, Circadian Disruption and Cardiometabolic Health)

Abstract

Major susceptibility to alterations in liver function (e.g., hepatic steatosis) in a prone environment due to circadian misalignments represents a common consequence of recent sociobiological behavior (i.e., food excess and sleep deprivation). Natural compounds and, more concisely, polyphenols have been shown as an interesting tool for fighting against metabolic syndrome and related consequences. Furthermore, mitochondria have been identified as an important target for mediation of the health effects of these compounds. Additionally, mitochondrial function and dynamics are strongly regulated in a circadian way. Thus, we wondered whether some of the beneficial effects of grape-seed procyanidin extract (GSPE) on metabolic syndrome could be mediated by a circadian modulation of mitochondrial homeostasis. For this purpose, rats were subjected to “standard”, “cafeteria” and “cafeteria diet + GSPE” treatments (n = 4/group) for 9 weeks (the last 4 weeks, GSPE/vehicle) of treatment, administering the extract/vehicle at diurnal or nocturnal times (ZT0 or ZT12). For circadian assessment, one hour after turning the light on (ZT1), animals were sacrificed every 6 h (ZT1, ZT7, ZT13 and ZT19). Interestingly, GSPE was able to restore the rhythm on clock hepatic genes (Bmal1, Per2, Cry1, Rorα), as this correction was more evident in nocturnal treatment. Additionally, during nocturnal treatment, an increase in hepatic fusion genes and a decrease in fission genes were observed. Regarding mitochondrial complex activity, there was a strong effect of cafeteria diet at nearly all ZTs, and GSPE was able to restore activity at discrete ZTs, mainly in the diurnal treatment (ZT0). Furthermore, a differential behavior was observed in tricarboxylic acid (TCA) metabolites between GSPE diurnal and nocturnal administration times. Therefore, GSPE may serve as a nutritional preventive strategy in the recovery of hepatic-related metabolic disease by modulating mitochondrial dynamics, which is concomitant to the restoration of the hepatic circadian machinery.
Keywords: grape-seed procyanidin extract; circadian rhythms; clock genes; Zeitgebers; obesity; nutrition; hepatic metabolism; mitochondrial dynamics grape-seed procyanidin extract; circadian rhythms; clock genes; Zeitgebers; obesity; nutrition; hepatic metabolism; mitochondrial dynamics
Graphical Abstract

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MDPI and ACS Style

Rodríguez, R.M.; Cortés-Espinar, A.J.; Soliz-Rueda, J.R.; Feillet-Coudray, C.; Casas, F.; Colom-Pellicer, M.; Aragonès, G.; Avila-Román, J.; Muguerza, B.; Mulero, M.; et al. Time-of-Day Circadian Modulation of Grape-Seed Procyanidin Extract (GSPE) in Hepatic Mitochondrial Dynamics in Cafeteria-Diet-Induced Obese Rats. Nutrients 2022, 14, 774. https://doi.org/10.3390/nu14040774

AMA Style

Rodríguez RM, Cortés-Espinar AJ, Soliz-Rueda JR, Feillet-Coudray C, Casas F, Colom-Pellicer M, Aragonès G, Avila-Román J, Muguerza B, Mulero M, et al. Time-of-Day Circadian Modulation of Grape-Seed Procyanidin Extract (GSPE) in Hepatic Mitochondrial Dynamics in Cafeteria-Diet-Induced Obese Rats. Nutrients. 2022; 14(4):774. https://doi.org/10.3390/nu14040774

Chicago/Turabian Style

Rodríguez, Romina M., Antonio J. Cortés-Espinar, Jorge R. Soliz-Rueda, Christine Feillet-Coudray, François Casas, Marina Colom-Pellicer, Gerard Aragonès, Javier Avila-Román, Begoña Muguerza, Miquel Mulero, and et al. 2022. "Time-of-Day Circadian Modulation of Grape-Seed Procyanidin Extract (GSPE) in Hepatic Mitochondrial Dynamics in Cafeteria-Diet-Induced Obese Rats" Nutrients 14, no. 4: 774. https://doi.org/10.3390/nu14040774

APA Style

Rodríguez, R. M., Cortés-Espinar, A. J., Soliz-Rueda, J. R., Feillet-Coudray, C., Casas, F., Colom-Pellicer, M., Aragonès, G., Avila-Román, J., Muguerza, B., Mulero, M., & Salvadó, M. J. (2022). Time-of-Day Circadian Modulation of Grape-Seed Procyanidin Extract (GSPE) in Hepatic Mitochondrial Dynamics in Cafeteria-Diet-Induced Obese Rats. Nutrients, 14(4), 774. https://doi.org/10.3390/nu14040774

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