Polyphenols and hormonal balance -
In addition, cherry consumption reduced the cumulative energy intake when consumed in the LD photoperiod, whereas no effect was observed after grape consumption. The photoperiod or fruit consumption did not significantly alter hour energy expenditure Table 2 and Fig.
Effect of photoperiod and seasonal fruit supplementation on oxygen consumption VO 2 in obese animals. Notably, a positive hour energy balance was observed in all experimental conditions, except for those placed in the SD photoperiod. Cherry significantly reduced hours energy balance when consumed in the LD photoperiod, indicating that the lower 24 h-energy balance exhibited by obese animals in this photoperiod was a direct consequence of the reduced energy intake.
These data totally differ from those obtained in non-obese animals, in which cherry reduced energy balance in both photoperiods and in the case of animals placed on LD that was due to an increase in hour energy expenditure.
Finally, the photoperiod also modulated RQ values in obese animals. Specifically, these animals presented a significant increase in RQ values in the SD photoperiod, indicating that the LD photoperiod favored lipid use as energetic substrates whereas the SD photoperiod favored carbohydrates.
In addition, cherry consumption in the SD photoperiod significantly decreased RQ values in obese animals. The circulating levels of leptin were similar in all three groups of animals Fig.
Effect of photoperiod and seasonal fruit consumption on hypothalamic leptin sensitivity in obese animals. C , D Gene expression of long form of leptin receptor Obrb and negative regulator molecules Socs3 and Ptp1b were analyzed. Among them, only Socs3 mRNA levels were sensitive to the photoperiod, increasing its values in the SD photoperiod Fig.
Interestingly, grape consumption enhanced the gene expression of Socs3 in the SD photoperiod, whereas cherry consumption repressed both Socs3 and Ptp1b gene expression when consumed in the SD photoperiod, indicating that the expression of genes involved in the regulation of leptin signaling was more sensitive to modulation by the photoperiod and fruit consumption in obese animals than in non-obese ones.
We also investigated the hypothalamic mRNA levels of Pomc , Agrp , Npy , Mc4r and Npy1r. Obese animals placed in the SD photoperiod presented a marked overexpression of the orexigenic Agrp neuropeptide Fig.
Additionally, cherry consumption also modulated the gene expression of Mc4r and Npy1r by repressing the genes when cherry was consumed in the SD photoperiod Fig. These results indicate that in the SD photoperiod, hypothalamic Socs3 and Agrp gene expression was up-regulated in obese animals compared to that in the LD photoperiod.
In contrast, the consumption of grape or cherry strongly reversed this photoperiod-dependent gene expression pattern, repressing the overexpression of Agrp when fruits were consumed in the SD photoperiod.
Effect of photoperiod and seasonal fruit supplementation on hypothalamic neuropeptides regulated by leptin in obese animals. Values were normalized against LD-Control group.
Great attention has been paid to calorie consumption and diet composition to improve metabolic health and decrease obesity However, there is a lack of studies focusing on seasonal foods and their detrimental or beneficial effects when consumed in- or out-of-season.
Seasonality plays an important role in all organisms to maintain life balance Here, we present the results of this novel approach, showing that seasonal fruits can modulate the leptin system depending on the photoperiod in which they are consumed, in both healthy and obese animals.
The Siberian hamster Phodopus sungorus is the most widely used animal model to study photoperiod responses However, in this study we opted for the Fischer strain rat because rat metabolism is more similar to that of humans 23 , and this strain is sensitive to the photoperiod Non-obese animals presented the characteristic phenotype described for Fischer rats placed in the LD or SD photoperiods, displaying lower fat mass 25 , 26 and leptin concentrations 25 , 27 in the SD condition.
However, these rats did not present a significant reduction in body weight described as typical for the SD photoperiod. Remarkably, animals placed for a long period of time in a SD photoperiod become refractory to light cycle conditions, shifting to a LD physiology in order to accomplish reproduction and preserve species survival Specifically, this time is considered to be 10 weeks for Fischer rats 29 , and rats in our experiment were kept 14 weeks at SD; thus, they could be in a refractory state.
However, we selected 4 weeks of adaptation to the photoperiod plus 10 weeks of fruit treatment because we aimed to determine the long-term effect of seasonal fruit consumption in animals already adapted to a specific photoperiod.
The fat mass percentage reduction observed in non-obese rats placed at SD was associated with a lower energy balance close to zero , which can be ascribed to increased energy expenditure rather than reduced food intake, as described by other authors 25 , Leptin is essential in the regulation of central energy homeostasis However, we did not observe any change in the expression of neuropeptides regulated by leptin or their receptors in second-order of non-obese animals at SD.
Thus, other hormones, such as prolactin 31 , or an increase in leptin sensitivity 32 , 33 , induced by other leptin signaling components not determined in this study, could participate in this higher energy expenditure observed in SD.
In this sense, small rodents, such as hamsters or field voles Microtus agrestis , develop leptin resistance in LD due to decreased pSTAT3 33 , which was not evaluated in the present study. Our objective was not to directly compare non-obese versus obese animals but rather to describe the fruit and photoperiod effects in the two models separately.
However, it is important to note that the response of obese animals to photoperiod diverged significantly from that of lean animals. Only few studies have focused on the photoperiod effects to animals fed an obesogenic diet.
However, a study using Fischer rats fed a high-fat diet for 4 weeks 25 agrees with our findings for both the loss of photoperiod regulation of fat mass and the photoperiod regulation of food intake, decreasing it in the SD condition.
Thus, obese rats in the present study reduced their energy balance at SD as a consequence of reduced cumulative energy intake, without any modification to energy expenditure. In addition, the photoperiod effect on serum leptin levels was blunted when animals were on the obesogenic diet.
However, leptin system was altered in SD, as indicated by a slight increase of Socs3 and marked overexpression of Agrp mRNA levels in this photoperiod. Notably, it has been reported that leptin resistance associated with LD is caused by high serum leptin levels and Socs3 overexpression 33 whereas leptin sensitivity accompanying SD is associated with Agrp down-regulation in the arcuate nucleus Thus, the pattern of the leptin system in rats fed a cafeteria diet, together with the high serum leptin levels in SD, indicates that obese rats have lost the capacity to modulate leptin sensitivity according to photoperiods.
From all seasonal fruits, red grapes were selected as a representative fruit of autumn SD and cherry as a representative of fruit of spring LD because of their high content of polyphenols 34 , 35 , Red grapes contain mainly flavonoids, including anthocyanins, flavanols monomers and proanthocyanidins , flavonols and non-flavonoids, such as phenolic acids and stilbenes mainly resveratrol 35 , Cherries also contain flavonoids, which include anthocyanins, flavanols monomers and proanthocyanidins , and non-flavonoids such as phenolic acids mainly hydroxycinnamates 37 , Evidently, grape and cherry contain similar classes of polyphenols; cherries contain larger amounts of anthocyanins and hydroxycinnamic acids compared to grapes, but lack flavonols and stilbenes Notably, both fruits were given at a dose that in humans is equivalent to a small portion of fruit, below the serving size established in the European dietary guidelines The consumption of both fruits induced a lower energy balance in non-obese animals under both the SD and LD conditions, indicating that this metabolic effect was independent of the photoperiod condition.
Remarkably, grape and cherry consumption reduced energy balance in different ways, for grape by reducing food intake but for cherry by increasing energy expenditure. The anorexigenic effect of grape consumption agrees with previous reported results demonstrating that grape seed proanthocyanidin extract reduces food intake in obese animals Interestingly, both cherry and grape intake resulted in overexpression of Pomc in the hypothalamus when consumed at SD.
Thus, the enhanced anorexigenic effect of both fruits could account, at least partially, for the lower energy balance observed in rats consuming fruits at SD. However, Pomc was only modulated in SD, indicating the photoperiod-dependent ability of these fruits to modulate leptin signaling.
In addition, cherry consumption also modulated hypothalamic Obrb expression in a photoperiod-dependent manner, increasing its expression in SD, fact that has been related to activation of POMC neurons and increased leptin sensitivity Thus, cherry clearly enhanced the out-of-season central leptin sensitivity in non-obese animals.
Remarkably, neither the energy balance reduction nor leptin sensitivity modulation induced by fruits were reflected in body weight or fat mass accretion. Thus, cherry and mainly grape should modulate other mechanisms that, in turn, counteract the expected fat mass reduction.
In this sense, grape seed proanthocyanidins have adipogenic activity, overexpressing PPARγ, increasing adipocyte number and reducing adipocyte hypertrophy in visceral and subcutaneous fat pads Thus, grape can act at the adipocyte level, counteracting the expected response of white adipose tissue to a lower energy balance sate.
In addition, grape seed proanthocyanidins increase mitochondrial oxidative capacity in skeletal muscle and brown adipose tissue 44 , Thus, the increase in energy expenditure in these organs could also contribute to the lower energy balance observed in rats fed grapes.
In obese rats, grape seed proanthocyanidins also increase hypothalamic leptin sensitivity 11 , associated with the overexpression of Pomc.
In this case, no effects of grape intake were observed in obese animals in either photoperiod. However, grape consumption showed a tendency to decrease Agrp levels in SD without reaching significance.
In contrast, cherries were very effective at modulating the leptin system in obese rats in a photoperiod-dependent mode. Specifically, cherry distinctly repressed the expression of Agrp and Ptp1B in SD.
Interestingly, Ptp1b is a negative regulator of the leptin signaling pathway, and its inhibition increases leptin sensitivity in obese animals Furthermore, Mc4r and Npy1r were also repressed in SD, indicating that cherry was also effective in modulating the response in second-order neurons.
Together, these results suggest that cherry intake improves central leptin sensitivity out-of-season in obese animals. This reduction in the orexigenic signal Agrp of cherry agrees with the decreased cumulative food intake in obese rats that consumed cherry in SD.
In contrast, the photoperiod-dependent effect of cherry on hypothalamic leptin sensitivity completely differs from the lower energy balance and RQ values observed in obese rats consuming cherry at LD. Thus, as stated in non-obese animals, a cherry effect that increases energy expenditure in brown adipose tissue when it is consumed in season cannot be excluded.
The xenohormesis hypothesis 46 , as defined by Howitz and Sinclair, proposes that animal uses chemical signals from plants, mainly polyphenols, to determine the environmental status or food supply.
This acknowledgment would allow animals to respond in advance to environmental alterations, thus increasing their probability of survival. Therefore, the specific polyphenol content in grape and cherry could act as a distinctive mark, informing rats of environmental conditions such as photoperiod. Reinforcing this idea, previous studies by our group have demonstrated that grape proanthocyanidins modulate circadian rhythms at the hypothalamic level Nevertheless, cherries are also rich on melatonin 48 , a hormone that provides information about day length, controlling seasonal phenotypic adjustments Interestingly, melatonin reduces the energy expenditure induced by cold exposure in the Siberian hamster placed at LD 50 and stimulates Pomc expression in mice Therefore, the melatonin contained in cherries could significantly contribute to the metabolic effects induced by cherry intake observed in this study.
In summary, fruit consumption decreased the energy balance in non-obese and obese animals in a photoperiod-independent manner. Grape reduced cumulative food intake, whereas cherry increased energy expenditure.
In contrast, both fruits modulated the leptin system in a photoperiod-dependent way, increasing leptin sensitivity in SD. In obese animals, only cherry intake modulated the leptin system, repressing Agrp and Ptp1B in SD.
Thus, cherry intake modulated the central leptin system when consumed out-of-season in both obese animals and non-obese animals. Royal Down sweet cherries Prunus avium L. were purchased in Mercabarna Barcelona, Spain. Black grapes Vitis vinifera L. of the Grenache variety were kindly provided by the producer Tarragona, Spain.
Cherry pits were removed, and grapes were kept intact. Fruits were frozen in liquid nitrogen and later ground. The nutritional and polyphenol composition of both fruits has been widely characterized and can be found as in Supplementary Tables S1 — S4.
The animals were pair-housed and distributed in two different rooms according to photoperiod. They were fed a standard chow diet Panlab 04, Barcelona, Spain with water ad libitum.
These animals were fed a standard chow diet plus a cafeteria diet with water ad libitum. Animals were sacrificed by decapitation at the start of the light cycle lights on at am.
The hypothalamus was dissected and frozen immediately in liquid nitrogen. Body weight and food intake were measured weekly. In the last week of the study, animals were subjected to magnetic resonance imaging MRI using EchoMRI Echo Medical Systems, LLC. Data is expressed as a percentage of total body weight.
The program Metabolism 2. The hypothalamus was processed to extract total RNA using TRIzol LS Reagent Thermo Fisher, Madrid, Spain followed by an RNeasy Mini Kit Qiagen, Barcelona, Spain.
RNA quantity and purity were measured with a NanoDrop spectrophotometer Thermo Scientific, Madrid, Spain. RNA quality was assessed on a denaturing agarose gel. Reverse transcription was performed to obtain cDNA using the High-Capacity Complementary DNA Reverse Transcription Kit Thermo Fisher.
Gene expression was analyzed by quantitative PCR using the iTaq Universal SYBR Green Supermix Bio-Rad in the ABI prism HT real-time PCR system Applied Biosystems using primers obtained from Biomers.
net Ulm, Germany. The forward and reverse primers used in this study can be found as Supplementary Table S5. The relative expression of each gene was calculated referring to Ppia and Rplp0 housekeeping genes and normalized to the control group.
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According to the authors, there is a need to raise public awareness about the possible side effects of polyphenols supplementation, especially in the case of vulnerable subpopulations. Keywords: DNA damage; cytochrome P; drug interactions; mutations; polyphenols; prooxidant activity; side effect; toxicity.
Abstract Polyphenols are an important component of plant-derived food with a wide spectrum of beneficial effects on human health.
Publication types Review. Substances Polyphenols Antioxidants. Grants and funding.
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