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Review
. 2023 Jan 5;24(2):1008.
doi: 10.3390/ijms24021008.

Photoperiodic Remodeling of Adiposity and Energy Metabolism in Non-Human Mammals

Èlia Navarro-Masip  1 , Alexandre Caron  2 , Miquel Mulero  1 , Lluís Arola  1 , Gerard Aragonès  1
Affiliations
Review

Photoperiodic Remodeling of Adiposity and Energy Metabolism in Non-Human Mammals

Èlia Navarro-Masip et al. Int J Mol Sci. .

Abstract

Energy homeostasis and metabolism in mammals are strongly influenced by seasonal changes. Variations in photoperiod patterns drive adaptations in body weight and adiposity, reflecting changes in the regulation of food intake and energy expenditure. Humans also show distinct patterns of energy balance depending on the season, being more susceptible to gaining weight during a specific time of the year. Changes in body weight are mainly reflected by the adipose tissue, which is a key metabolic tissue and is highly affected by circannual rhythms. Mostly, in summer-like (long-active) photoperiod, adipocytes adopt a rather anabolic profile, more predisposed to store energy, while food intake increases and energy expenditure is reduced. These metabolic adaptations involve molecular modifications, some of which have been studied during the last years and are summarized in this review. In addition, there is a bidirectional relation between obesity and the seasonal responses, with obesity disrupting some of the seasonal responses observed in healthy mammals, and altered seasonality being highly associated with increased risk of developing obesity. This suggests that changes in photoperiod produce important metabolic alterations in healthy organisms. Biological rhythms impact the regulation of metabolism to different extents, some of which are already known, but further research is needed to fully understand the relationship between energy balance and seasonality.

Keywords: adipose tissue; leptin; melatonin; obesity; photoperiod; seasonality.

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Conflict of interest statement

The authors declare no conflict of interest. The funders had no role in the writing of the manuscript or in the decision to publish the results.

Figures

Figure 1
Figure 1
Melatonin seasonal signaling in the hypothalamus. In mammals, a luminous signal is received by melanopsin-containing cells in the retina, and is transferred to the SCN in the hypothalamus. Pinealocytes receive the information via SNS and respond by synthesizing and secreting melatonin. MT1 receptors in the “calendar cells” of the Pars Tuberalis detect melatonin signal, that acts by inhibiting EYA3 function, and therefore blocking TSHβ secretion. Depending on the duration of melatonin signaling, the inhibition of this pathway is stronger (during the SP or winter) or lighter (during the LP or summer). In summer-like photoperiod, TSHβ is released and acts by inhibiting DIO3 and stimulating DIO2 function in tanycytes. DIO2 induces T3 production and favors a rather anabolic state in the CNS, increasing food intake and reducing energy expenditure. In the winter-like photoperiod, TSHβ is not released by tanycytes and DIO3 increases its functionality, converting T4 into inactive metabolites of T3, favoring a rather catabolic state by reducing food intake and increasing energy expenditure. Abbreviations: CNS: Central Nervous System; DIO2: Deiodinase 2; DIO3: Deiodinase 3; EYA3: Eyes absent 3; LP: Long Photoperiod; SCN: Suprachiasmatic Nucleus; SNS: Sympathetic Nervous System; SP: Short Photoperiod; T3: Triiodothyronine; T4: Thyroxine; TSHβ: Thyroid Stimulating Hormone β Subunit.
Figure 2
Figure 2
Schematic representation of adipogenesis and its molecular regulation. Non-expressing Myf5 mesenchymal stem cell (MSC) transitions to committed white preadipocyte, where adipogenic stimuli allows its proliferation through the activation of pro-adipogenic transcription factors, such as peroxisome proliferator-activated receptor γ (PPARγ) and some members of CCAAT/enhancer binding protein family (C/EBPs). Then, the preadipocyte goes through clonal expansion, which is the beginning of its differentiation and is also enhanced by PPARγ and C/EBPs, among others. During the differentiation phase, the adipocyte shows its typical morphological characteristics, such as a high amount of fat content, an eccentric nucleus and low content of mitochondria. The final step is the terminal differentiation, where the adipocyte is already mature and functional. During the early and mature differentiation, adipocytes express specific markers such as Adipocyte fatty acid binding protein 2 (aP2), glucose transporter 4 (GLUT4), lipoprotein lipase (LPL), phosphoenol pyruvate carboxykinase (PEPK) or adipocyte triglyceride lipase (ATGL). Adipogenesis is negatively regulated by some molecules and/or signaling pathways such as shown on the left side of the figure. Contrarily, positive regulators allow the development of this process (shown on the right side). Other abbreviations: AMPK: Adenosine Monophosphate-Activated Protein Kinase; BMP4: Bone morphogenic protein 4; CREB: Cyclic AMP Response Element-Binding Protein; Pref-1: Preadipocyte Factor 1; SIRT1: Histone Deacetylase Sirtuin 1; SREBP1: Sterol Regulatory Element-Binding Protein 1; TAZ: Transcriptional-Coactivator with PDZ-Binding Motif; ZFP423: Zinc Finger Protein 423.
Figure 3
Figure 3
Regulation of lipid metabolism in adipocytes. The presence of insulin and/or a feeding state enhances the process of lipogenesis and de novo lipogenesis (marked by dashed arrows). On the one hand, the adipocytes obtain FFA (free fatty acids) through the LPL (lipoprotein lipase)-mediated breakdown of TG (triglycerides) from its circulating transporters. These FFA enter the adipocytes through the CD36 (cluster of differentiation 36) membrane transporter and are again converted into TG, by DGAT (diacylglycerol acyltransferase). On the other hand, adipocytes can convert glucose into FFA via de novo lipogenesis. This process is inhibited by a fasting state or the growth hormone which, together with many other cues, activate lipolysis (marked by solid arrows). In this case, the increase of cAMP activates the PKA (protein kinase A) function, and that promotes the activity of lipolytic enzymes. Hence, TG are converted into Glycerol and FFA, that go into circulation and are used by peripheral tissues that need energy. Other abbreviations: β-AR: β-adrenergic receptor; AC: adenylyl cyclase; ACAC: acetyl-CoA carboxylase 1; ATGL: adipocyte triglyceride lipase; DAG: diacylglycerol; FAS: fatty acid synthase; HSL: hormone sensitive lipase; MAG: monoacylglycerol; MGL: monoacylglycerol lipase; NA: noradrenaline; VLDL-TG: triglyceride containing-very low-density lipoprotein.
Figure 4
Figure 4
Hypothalamic regulation of food intake. When the energy balance of the organism is positive, the concentration of leptin, insulin and cholecystokinin (CKK), among others, is increased. These hormones activate the POMC/CART-expressing neurons, that upregulate the expression of anorexigenic molecules (such as orexin, Crh and TSH) in the PVN and the VMN, favoring a reduction in food intake. On the other hand, during fasting, ghrelin levels are increased and leptin levels are reduced. These changes activate the AgRP-expressing neurons, which are indeed suppressed by high leptin concentrations. This group of neurons act by stimulating food intake through the PVN, LH and DMN, while suppressing PB and VMN, preventing reduced feeding. Abbreviations: POMC: pro-opiomelanocortin; CART: cocaine- and amphetamine-regulated transcript; Crh: corticotropin-releasing hormone; TSH: thyroid-stimulating hormone; PVN: Paraventricular Nucleus; VMN: Ventromedial Nucleus; AgRP: agouti-related peptide; LH: Lateral Hypothalamus; DMN: Dorsomedial Hypothalamic Nucleus; PB: Parabranchial Nucleus.
Figure 5
Figure 5
Photoperiod-dependent adaptations in energy and lipid metabolisms and the alterations caused by obesity in mammals. In healthy conditions, seasonal rhythms are regulated in mammals and adiposity, body weight, food intake, leptin signaling and browning in the adipose tissue are increased in summer photoperiod, while energy expenditure is reduced. The contrary happens in winter photoperiod, where melatonin levels are increased. However, in obesity, the biologic seasonal rhythmicity is dysregulated and energy and lipid metabolisms are altered. Anabolism is accentuated in summer photoperiod, and in winter photoperiod there is an increase in adiposity, lean mass, BAT mass and leptin signaling, while adiponectin levels are lowered and energy expenditure drops. Abbreviations: BAT: Brown Adipose Tissue.
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References

    1. Dardente H., Wood S., Ebling F., Sáenz de Miera C. An Integrative View of Mammalian Seasonal Neuroendocrinology. J. Neuroendocrinol. 2019;31:e12729. doi: 10.1111/jne.12729. - DOI - PubMed
    1. Helfer G., Barrett P., Morgan P.J. A Unifying Hypothesis for Control of Body Weight and Reproduction in Seasonally Breeding Mammals. J. Neuroendocrinol. 2019;31:e12680. doi: 10.1111/jne.12680. - DOI - PubMed
    1. Moreno J.P., Crowley S.J., Alfano C.A., Thompson D. Physiological Mechanisms Underlying Children’s Circannual Growth Patterns and Their Contributions to the Obesity Epidemic in Elementary School Age Children. Obes. Rev. 2020;21:e12973. doi: 10.1111/obr.12973. - DOI - PMC - PubMed
    1. Yokoya M., Higuchi Y. Day Length May Make Geographical Difference in Body Size and Proportions: An Ecological Analysis of Japanese Children and Adolescents. PLoS ONE. 2019;14:e0210265. doi: 10.1371/journal.pone.0210265. - DOI - PMC - PubMed
    1. Ebling F.J.P. On the Value of Seasonal Mammals for Identifying Mechanisms Underlying the Control of Food Intake and Body Weight. Horm. Behav. 2014;66:56–65. doi: 10.1016/j.yhbeh.2014.03.009. - DOI - PMC - PubMed

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