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      Intake of an Obesogenic Cafeteria Diet Affects Body Weight, Feeding Behavior, and Glucose and Lipid Metabolism in a Photoperiod-Dependent Manner in F344 Rats

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          Abstract

          We previously demonstrated that chronic exposure to different photoperiods induced marked variations in several glucose and lipid metabolism-related parameters in normoweight Fischer 344 (F344) rats. Here, we examined the effects of the combination of an obesogenic cafeteria diet (CAF) and the chronic exposure to three different day lengths (L12, 12 h light/day; L18, 18 h light/day; and L6, 6 h light/day) in this rat strain. Although no changes were observed during the first 4 weeks of adaptation to the different photoperiods in which animals were fed a standard diet, the addition of the CAF for the subsequent 7 weeks triggered profound physiologic and metabolic alterations in a photoperiod-dependent manner. Compared with L12 rats, both L6 and L18 animals displayed lower body weight gain and cumulative food intake in addition to decreased energy expenditure and locomotor activity. These changes were accompanied by differences in food preferences and by a sharp upregulation of the orexigenic genes Npy and Ghsr in the hypothalamus, which could be understood as a homeostatic mechanism for increasing food consumption to restore body weight control. L18 rats also exhibited higher glycemia than the L6 group, which could be partly attributed to the decreased pAkt2 levels in the soleus muscle and the downregulation of Irs1 mRNA levels in the gastrocnemius muscle. Furthermore, L6 animals displayed lower whole-body lipid utilization than the L18 group, which could be related to the lower lipid intake and to the decreased mRNA levels of the fatty acid transporter gene Fatp1 observed in the soleus muscle. The profound differences observed between L6 and L18 rats could be related with hepatic and muscular changes in the expression of circadian rhythm-related genes Cry1, Bmal1, Per2, and Nr1d1. Although further research is needed to elucidate the pathophysiologic relevance of these findings, our study could contribute to emphasize the impact of the consumption of highly palatable and energy dense foods regularly consumed by humans on the physiological and metabolic adaptations that occur in response to seasonal variations of day length, especially in diseases associated with changes in food intake and preference such as obesity and seasonal affective disorder.

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          Most cited references39

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          Adipose tissue in control of metabolism.

          Adipose tissue plays a central role in regulating whole-body energy and glucose homeostasis through its subtle functions at both organ and systemic levels. On one hand, adipose tissue stores energy in the form of lipid and controls the lipid mobilization and distribution in the body. On the other hand, adipose tissue acts as an endocrine organ and produces numerous bioactive factors such as adipokines that communicate with other organs and modulate a range of metabolic pathways. Moreover, brown and beige adipose tissue burn lipid by dissipating energy in the form of heat to maintain euthermia, and have been considered as a new way to counteract obesity. Therefore, adipose tissue dysfunction plays a prominent role in the development of obesity and its related disorders such as insulin resistance, cardiovascular disease, diabetes, depression and cancer. In this review, we will summarize the recent findings of adipose tissue in the control of metabolism, focusing on its endocrine and thermogenic function.
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            Human responses to the geophysical daily, annual and lunar cycles.

            Collectively the daily, seasonal, lunar and tidal geophysical cycles regulate much of the temporal biology of life on Earth. The increasing isolation of human societies from these geophysical cycles, as a result of improved living conditions, high-quality nutrition and 24/7 working practices, have led many to believe that human biology functions independently of them. Yet recent studies have highlighted the dominant role that our circadian clock plays in the organisation of 24 hour patterns of behaviour and physiology. Preferred wake and sleep times are to a large extent driven by an endogenous temporal program that uses sunlight as an entraining cue. The alarm clock can drive human activity rhythms but has little direct effect on our endogenous 24 hour physiology. In many situations, our biology and our society appear to be in serious opposition, and the damaging consequences to our health under these circumstances are increasingly recognised. The seasons dominate the lives of non-equatorial species, and until recently, they also had a marked influence on much of human biology. Despite human isolation from seasonal changes in temperature, food and photoperiod in the industrialised nations, the seasons still appear to have a small, but significant, impact upon when individuals are born and many aspects of health. The seasonal changes that modulate our biology, and how these factors might interact with the social and metabolic status of the individual to drive seasonal effects, are still poorly understood. Lunar cycles had, and continue to have, an influence upon human culture, though despite a persistent belief that our mental health and other behaviours are modulated by the phase of the moon, there is no solid evidence that human biology is in any way regulated by the lunar cycle.
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              Annual rhythms that underlie phenology: biological time-keeping meets environmental change.

              Seasonal recurrence of biological processes (phenology) and its relationship to environmental change is recognized as being of key scientific and public concern, but its current study largely overlooks the extent to which phenology is based on biological time-keeping mechanisms. We highlight the relevance of physiological and neurobiological regulation for organisms' responsiveness to environmental conditions. Focusing on avian and mammalian examples, we describe circannual rhythmicity of reproduction, migration and hibernation, and address responses of animals to photic and thermal conditions. Climate change and urbanization are used as urgent examples of anthropogenic influences that put biological timing systems under pressure. We furthermore propose that consideration of Homo sapiens as principally a 'seasonal animal' can inspire new perspectives for understanding medical and psychological problems.
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                Author and article information

                Contributors
                Journal
                Front Physiol
                Front Physiol
                Front. Physiol.
                Frontiers in Physiology
                Frontiers Media S.A.
                1664-042X
                26 November 2018
                2018
                : 9
                : 1639
                Affiliations
                [1] 1Eurecat, Centre Tecnològic de Catalunya, Technological Unit of Nutrition and Health , Reus, Spain
                [2] 2Nutrigenomics Research Group, Department of Biochemistry and Biotechnology, Universitat Rovira i Virgili , Tarragona, Spain
                Author notes

                Edited by: Ovidiu Constantin Baltatu, Anhembi Morumbi University, Brazil

                Reviewed by: Alan Rosenwasser, University of Maine, France; Arcady A. Putilov, Humboldt-Universität zu Berlin, Germany

                This article was submitted to Integrative Physiology, a section of the journal Frontiers in Physiology

                Article
                10.3389/fphys.2018.01639
                6275206
                38fb1125-a366-4fe8-bee2-99daca2adb63
                Copyright © 2018 Mariné-Casadó, Domenech-Coca, del Bas, Bladé, Arola and Caimari.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 13 August 2018
                : 30 October 2018
                Page count
                Figures: 7, Tables: 2, Equations: 0, References: 54, Pages: 16, Words: 0
                Categories
                Physiology
                Original Research

                Anatomy & Physiology
                photoperiod,circannual rhythms,cafeteria diet,metabolic syndrome,feeding behavior,glucose homeostasis

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