Detrimental effects of constant light exposure and high‐fat diet on circadian energy metabolism and insulin sensitivity

Coomans, Claudia P.; Berg, Sjoerd A.A. van den; Houben, Thijs; Klinken, Jan-Bert van; Berg, Rosa van den; Pronk, Amanda; Havekes, Louis M.; Romijn, Johannes A.; Dijk, Ko Willems van; Biermasz, Nienke R.; Meijer, Johanna H.

doi:10.1096/fj.12-210898

Cited by 219 publications

(213 citation statements)

References 53 publications

(60 reference statements)

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“…These data are in line with observations in field voles: switching the day length from 8-to 16-h increased body weight by 24% in 4 wk compared with animals that remained on a day length of 8 h (14). Accordingly, we previously showed that prolonging day length from 12 to 24 h decreases energy expenditure in mice without increasing food intake or locomotor activity (11). Although acute light exposure at night can reduce locomotor activity (15) and prolonged light exposure affects wheel-running activity (16,17), our present study confirms previous reports from us (11) and others (18) that prolonged light exposure does not decrease spontaneous locomotor activity.…”

Section: Discussionsupporting

confidence: 91%

“…Accordingly, we previously showed that prolonging day length from 12 to 24 h decreases energy expenditure in mice without increasing food intake or locomotor activity (11). Although acute light exposure at night can reduce locomotor activity (15) and prolonged light exposure affects wheel-running activity (16,17), our present study confirms previous reports from us (11) and others (18) that prolonged light exposure does not decrease spontaneous locomotor activity. Together, these studies support the idea that prolonged daily light exposure increases body fat mass through a decrease in energy expenditure rather than to an increase in food intake or decrease of locomotor activity.…”

Section: Discussionsupporting

confidence: 91%

“…1H). Therefore, the positive correlation between day length and adiposity is not explained by hyperphagia, consistent with our previous observations that exposure of mice to constant light decreases energy expenditure rather than increasing food intake (11 Fig. S2 A and B).…”

Section: Prolonged Daily Light Exposure Increases Adiposity Withoutsupporting

confidence: 92%

“…Constant light disrupts the central circadian clock, evidenced by an immediate reduction in the circadian amplitude of SCN electrical activity. Moreover, constant light induces body weight gain and insulin resistance, even faster than high-fat diet, which was not caused by increased food intake or reduced locomotor activity (11). Therefore, disruption of the central biological clock likely induces weight gain by decreasing energy expenditure.…”

mentioning

confidence: 99%

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Prolonged daily light exposure increases body fat mass through attenuation of brown adipose tissue activity

Kooijman¹,

Berg²,

Ramkisoensing

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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120

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Disruption of circadian rhythmicity is associated with obesity and related disorders, including type 2 diabetes and cardiovascular disease. Specifically, prolonged artificial light exposure associates with obesity in humans, although the underlying mechanism is unclear. Here, we report that increasing the daily hours of light exposure increases body adiposity through attenuation of brown adipose tissue (BAT) activity, a major contributor of energy expenditure. Mice exposed to a prolonged day length of 16-and 24-h light, compared with regular 12-h light, showed increased adiposity without affecting food intake or locomotor activity. Mechanistically, we demonstrated that prolonged day length decreases sympathetic input into BAT and reduces β3-adrenergic intracellular signaling. Concomitantly, prolonging day length decreased the uptake of fatty acids from triglyceride-rich lipoproteins, as well as of glucose from plasma selectively by BAT. We conclude that impaired BAT activity is an important mediator in the association between disturbed circadian rhythm and adiposity, and anticipate that activation of BAT may overcome the adverse metabolic consequences of disturbed circadian rhythmicity. M odern world society is subjected to disturbances of circadian rhythms by shift work, sleep deprivation, and environmental light pollution. Importantly, the increasing prevalence of obesity is associated with a disrupted sleep-wake pattern in humans (1) and coincides with the availability of artificial light (2, 3). Additionally, a recent study revealed a relationship between exposure to light at night and obesity in a cross-sectional analysis of over 100,000 women (4). Light input is the most important cue for generation of circadian (∼24 h) rhythms by the master clock. Both in rodents and humans the master clock is situated in the suprachiasmatic nucleus (SCN) of the hypothalamus. The SCN is responsible for synchronization of peripheral clocks throughout the body, which is mediated by endocrine and neuronal signals (5). A causal role for a disturbed circadian rhythm in the development of obesity has been demonstrated by animal studies. Mice with genetically dysfunctional clock genes develop obesity and insulin resistance (6-9). Moreover, specific ablation of the SCN induces acute weight gain (10). These results indicate a crucial role for the SCN in the regulation of adiposity.Interestingly, we previously showed that prolonged light exposure only is sufficient to enhance weight gain in mice. Constant light disrupts the central circadian clock, evidenced by an immediate reduction in the circadian amplitude of SCN electrical activity. Moreover, constant light induces body weight gain and insulin resistance, even faster than high-fat diet, which was not caused by increased food intake or reduced locomotor activity (11). Therefore, disruption of the central biological clock likely induces weight gain by decreasing energy expenditure.Recently, it has been recognized that brown adipose tissue (BAT) importantly contributes to energy ...

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Section: Discussionsupporting

confidence: 91%

Section: Discussionsupporting

confidence: 91%

Section: Prolonged Daily Light Exposure Increases Adiposity Withoutsupporting

confidence: 92%

mentioning

confidence: 99%

See 2 more Smart Citations

Prolonged daily light exposure increases body fat mass through attenuation of brown adipose tissue activity

Kooijman¹,

Berg²,

Ramkisoensing

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

120

View full text Add to dashboard Cite

show abstract

“…Both rodent and human studies confirm that daily rhythms of blood glucose and insulin secretion are regulated by the timing system [53][54][55], whilst lesions of the SCN or environmental circadian disruption can lead to insulin resistance and obesity [56,57]. The molecular clock is essential for glucose metabolism, as evidenced by the impairment of glucose tolerance and insulin sensitivity upon disruption of core clock gene expression [51,[58][59][60][61][62][63].…”

Section: The Timing System and Glucose Homeostasismentioning

confidence: 94%

Chronomedicine and type 2 diabetes: shining some light on melatonin

et al. 2016

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In mammals, the circadian timing system drives rhythms of physiology and behaviour, including the daily rhythms of feeding and activity. The timing system coordinates temporal variation in the biochemical landscape with changes in nutrient intake in order to optimise energy balance and maintain metabolic homeostasis. Circadian disruption (e.g. as a result of shift work or jet lag) can disturb this continuity and increase the risk of cardiometabolic disease. Obesity and metabolic disease can also disturb the timing and amplitude of the clock in multiple organ systems, further exacerbating disease progression. As our understanding of the synergy between the timing system and metabolism has grown, an interest has emerged in the development of novel clock-targeting pharmaceuticals or nutraceuticals for the treatment of metabolic dysfunction. Recently, the pineal hormone melatonin has received some attention as a potential chronotherapeutic drug for metabolic disease. Melatonin is well known for its sleep-promoting effects and putative activity as a chronobiotic drug, stimulating coordination of biochemical oscillations through targeting the internal timing system. Melatonin affects the insulin secretory activity of the pancreatic beta cell, hepatic glucose metabolism and insulin sensitivity. Individuals with type 2 diabetes mellitus have lower night-time serum melatonin levels and increased risk of comorbid sleep disturbances compared with healthy individuals. Further, reduced melatonin levels, and mutations and/or genetic polymorphisms of the melatonin receptors are associated with an increased risk of developing type 2 diabetes. Herein we review our understanding of molecular clock control of glucose homeostasis, detail the influence of circadian disruption on glucose metabolism in critical peripheral tissues, explore the contribution of melatonin signalling to the aetiology of type 2 diabetes, and discuss the pros and cons of melatonin chronopharmacotherapy in disease management.

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