bims-ciryme Biomed News
on Circadian rhythms and metabolism
Issue of 2024–03–17
seven papers selected by
Gabriela Da Silva Xavier, University of Birmingham
  1. Circadian patterns of behaviour change during pregnancy in mice.
  2. Tob Regulates the Timing of Sleep Onset at Night in Drosophila.
  3. Metabolic plasticity and obesity-associated changes in diurnal postexercise metabolism in mice.
  4. Dietary restriction modulates ultradian rhythms and autocorrelation properties in mice behavior.
  5. Secretion of glucagon, GLP-1 and GIP may be affected by circadian rhythm in healthy males.
  6. Recommendations for measuring and standardizing light for laboratory mammals to improve welfare and reproducibility in animal research.
  7. Protocol to study circadian food-anticipatory poking in mice using the feeding experimentation device version 3.
  1. J Physiol. 2024 Mar 13.
    Circadian patterns of behaviour change during pregnancy in mice.
    Georgia S Clarke, Andrew D Vincent, Sharon R Ladyman, Kathryn L Gatford, Amanda J Page.
      Food intake and activity adapt during pregnancy to meet the increased energy demands. In comparison to non-pregnant females, pregnant mice consume more food, eating larger meals during the light phase, and reduce physical activity. How pregnancy changes the circadian timing of behaviour was less clear. We therefore randomised female C57BL/6J mice to mating for study until early (n = 10), mid- (n = 10) or late pregnancy (n = 11) or as age-matched, non-pregnant controls (n = 12). Mice were housed individually in Promethion cages with a 12 h light-12 h dark cycle [lights on at 07.00 h, Zeitgeber (ZT)0] for behavioural analysis. Food intake between ZT10 and ZT11 was greater in pregnant than non-pregnant mice on days 6.5-12.5 and 12.5-17.5. In mice that exhibited a peak in the last 4 h of the light phase (ZT8-ZT12), peaks were delayed by 1.6 h in the pregnant compared with the non-pregnant group. Food intake immediately after dark-phase onset (ZT13-ZT14) was greater in the pregnant than non-pregnant group during days 12.5-17.5. Water intake patterns corresponded to food intake. From days 0.5-6.5 onwards, the pregnant group moved less during the dark phase, with decreased probability of being awake, in comparison to the non-pregnant group. The onset of dark-phase activity, peaks in activity, and wakefulness were all delayed during pregnancy. In conclusion, increased food intake during pregnancy reflects increased amplitude of eating behaviour, without longer duration. Decreases in activity also contribute to positive energy balance in pregnancy, with delays to all measured behaviours evident from mid-pregnancy onwards. KEY POINTS: Circadian rhythms synchronise daily behaviours including eating, drinking and sleep, but how these change in pregnancy is unclear. Food intake increased, with delays in peaks of food intake behaviour late in the light phase from days 6.5 to 12.5 of pregnancy, in comparison to the non-pregnant group. The onset of activity after lights off (dark phase) was delayed in pregnant compared with non-pregnant mice. Activity decreased by ∼70% in the pregnant group, particularly in the dark (active) phase, with delays in peaks of wakefulness evident from days 0.5-6.5 of pregnancy onwards. These behavioural changes contribute to positive energy balance during pregnancy. Delays in circadian behaviours during mouse pregnancy were time period and pregnancy stage specific, implying different regulatory mechanisms.
    Keywords:  circadian; food intake; physical activity; pregnancy
    DOI:  https://doi.org/10.1113/JP285553
  2. J Neurosci. 2024 Mar 14. pii: e0389232024. [Epub ahead of print]
    Tob Regulates the Timing of Sleep Onset at Night in Drosophila.
    Emily Han, Sang Soo Lee, Kristen H Park, Ian D Blum, Qiang Liu, Anuradha Mehta, Isabelle Palmer, Habon Issa, Alice Han, Matt P Brown, Victor M Sanchez-Franco, Miguel Velasco, Masashi Tabuchi, Mark N Wu.
      Sleep is regulated by homeostatic sleep drive and the circadian clock. While tremendous progress has been made in elucidating the molecular components of the core circadian oscillator, the output mechanisms by which this robust oscillator generates rhythmic sleep behaviour remain poorly understood. At the cellular level, growing evidence suggests that subcircuits in the master circadian pacemaker suprachiasmatic nucleus (SCN) in mammals and in the clock network in Drosophila regulate distinct aspects of sleep. Thus, to identify novel molecules regulating the circadian timing of sleep, we conducted a large-scale screen of mouse SCN-enriched genes in Drosophila Here, we show that Tob (Transducer of ERB-B2) regulates the timing of sleep onset at night in female fruit flies. Knockdown of Tob pan-neuronally, either constitutively or conditionally, advances sleep onset at night. We show that Tob is specifically required in "evening neurons" (the LNds and the 5th s-LNv) of the clock network for proper timing of sleep onset. Tob levels cycle in a clock-dependent manner in these neurons. Silencing of these "evening" clock neurons results in an advanced sleep onset at night, similar to that seen with Tob knockdown. Finally, sharp intracellular recordings demonstrate that the amplitude and kinetics of LNd post-synaptic potentials (PSPs) cycle between day and night, and this cycling is attenuated with Tob knockdown in these cells. Our data suggest that Tob acts as a clock-output molecule in a subset of clock neurons to potentiate their activity in the evening and enable the proper timing of sleep onset at night.Significance Summary Well-timed, high quality sleep is critical for human health and function. Elucidating how sleep is regulated by the circadian clock may reveal molecular targets for intervening in this process. However, our understanding of the genetic mechanisms underlying clock regulation of sleep is limited. From a high-throughput behavioral screen in Drosophila, we identified a novel clock output gene tob (transducer of erb-b2) required for proper timing of sleep onset at night. Tob levels cycle under clock control, and we show that Tob facilitates post-synaptic potentiation in a specific population of clock neurons. Our work suggests a molecular mechanism by which the clock regulates sleep onset by potentiating the function of a subset of clock neurons at night.
    DOI:  https://doi.org/10.1523/JNEUROSCI.0389-23.2024
  3. Metabolism. 2024 Mar 11. pii: S0026-0495(24)00060-X. [Epub ahead of print] 155834
    Metabolic plasticity and obesity-associated changes in diurnal postexercise metabolism in mice.
    Logan A Pendergrast, Stephen P Ashcroft, Amy M Ehrlich, Jonas T Treebak, Anna Krook, Lucile Dollet, Juleen R Zierath.
       BACKGROUND: Circadian disruption is widespread and increases the risk of obesity. Timing of therapeutic interventions may promote coherent and efficient gating of metabolic processes and restore energy homeostasis.
    AIM: To characterize the diurnal postexercise metabolic state in mice and to identify the influence of diet-induced obesity on identified outcomes.
    METHODS: C57BL6/NTac male mice (6wks of age) were fed a standard chow or high-fat diet for 5 weeks. At week 5, mice were subjected to a 60-min (16 m/min, 5 % incline) running bout (or sham) during the early rest (day) or early active (night) phase. Tissue and serum samples were collected immediately post-exercise (n = 6/group). In vivo glucose oxidation was measured after oral administration of 13C-glucose via 13CO2 exhalation analysis in metabolic cages. Basal and isoproterenol-stimulated adipose tissue lipolysis was assessed ex vivo for 1 h following exercise.
    RESULTS: Lean mice displayed exercise-timing-specific plasticity in metabolic outcomes, including phase-specificity in systemic glucose metabolism and adipose-tissue-autonomous lipolytic activity depending on time of day. Conversely, obesity impaired temporal postexercise differences in whole-body glucose oxidation, as well as the phase- and exercise-mediated induction of lipolysis in isolated adipose tissue. This obesity-induced alteration in diurnal metabolism, as well as the indistinct response to exercise, was observed concomitant with disruption of core clock gene expression in peripheral tissues.
    CONCLUSIONS: Overall, high-fat fed obese mice exhibit metabolic inflexibility, which is also evident in the diurnal exercise response. Our study provides physiological insight into exercise timing-dependent aspects in the dynamic regulation of metabolism and the influence of obesity on this biology.
    Keywords:  Adipose tissue; Circadian rhythm; Exercise; Lipolysis; Time of day
    DOI:  https://doi.org/10.1016/j.metabol.2024.155834
  4. Commun Biol. 2024 Mar 09. 7(1): 303
    Dietary restriction modulates ultradian rhythms and autocorrelation properties in mice behavior.
    Jackelyn Melissa Kembro, Ana Georgina Flesia, Victoria América Acosta-Rodríguez, Joseph S Takahashi, Paula Sofía Nieto.
      Animal behavior emerges from integration of many processes with different spatial and temporal scales. Dynamical behavioral patterns, including daily and ultradian rhythms and the dynamical microstructure of behavior (i.e., autocorrelations properties), can be differentially affected by external cues. Identifying these patterns is important for understanding how organisms adapt to their environment, yet unbiased methods to quantify dynamical changes over multiple temporal scales are lacking. Herein, we combine a wavelet approach with Detrended Fluctuation Analysis to identify behavioral patterns and evaluate changes over 42-days in mice subjected to different dietary restriction paradigms. We show that feeding restriction alters dynamical patterns: not only are daily rhythms modulated but also the presence, phase and/or strength of ~12h-rhythms, as well as the nature of autocorrelation properties of feed-intake and wheel running behaviors. These results highlight the underlying complexity of behavioral architecture and offer insights into the multi-scale impact of feeding habits on physiology.
    DOI:  https://doi.org/10.1038/s42003-024-05991-3
  5. BMC Endocr Disord. 2024 Mar 14. 24(1): 38
    Secretion of glucagon, GLP-1 and GIP may be affected by circadian rhythm in healthy males.
    Dorte B Zilstorff, Michael M Richter, Jens Hannibal, Henrik L Jørgensen, Henriette P Sennels, Nicolai J Wewer Albrechtsen.
       BACKGROUND: Glucagon is secreted from pancreatic alpha cells in response to low blood glucose and increases hepatic glucose production. Furthermore, glucagon enhances hepatic protein and lipid metabolism during a mixed meal. Glucagon-like peptide-1 (GLP-1) and glucose-dependent insulinotropic polypeptide (GIP) are secreted from gut endocrine cells during meals and control glucose homeostasis by potentiating insulin secretion and inhibiting food intake. Both glucose homeostasis and food intake have been reported to be affected by circadian rhythms and vice versa. In this study, we investigated whether the secretion of glucagon, GLP-1 and GIP was affected by circadian rhythms.
    METHODS: A total of 24 healthy men with regular sleep schedules were examined for 24 h at the hospital ward with 15 h of wakefulness and 9 h of sleep. Food intake was standardized, and blood samples were obtained every third hour. Plasma concentrations of glucagon, GLP-1 and GIP were measured, and data were analyzed by rhythmometric statistical methods. Available data on plasma glucose and plasma C-peptide were also included.
    RESULTS: Plasma concentrations of glucagon, GLP-1, GIP, C-peptide and glucose fluctuated with a diurnal 24-h rhythm, with the highest levels during the day and the lowest levels during the night: glucagon (p < 0.0001, peak time 18:26 h), GLP-1 (p < 0.0001, peak time 17:28 h), GIP (p < 0.0001, peak time 18:01 h), C-peptide (p < 0.0001, peak time 17.59 h), and glucose (p < 0.0001, peak time 23:26 h). As expected, we found significant correlations between plasma concentrations of C-peptide and GLP-1 and GIP but did not find correlations between glucose concentrations and concentrations of glucagon, GLP-1 and GIP.
    CONCLUSIONS: Our results demonstrate that under meal conditions that are similar to that of many free-living individuals, plasma concentrations of glucagon, GLP-1 and GIP were observed to be higher during daytime and evening than overnight. These findings underpin disturbed circadian rhythm as a potential risk factor for diabetes and obesity.
    TRIAL REGISTRATION: ClinicalTrials.gov Identifier: NCT06166368. Registered 12 December 2023.
    Keywords:  Circadian rhythm; GIP; GLP-1; Glucagon; Glucagon stimulation; Incretin hormones; Metabolism
    DOI:  https://doi.org/10.1186/s12902-024-01566-9
  6. PLoS Biol. 2024 Mar;22(3): e3002535
    Recommendations for measuring and standardizing light for laboratory mammals to improve welfare and reproducibility in animal research.
    Robert J Lucas, Annette E Allen, George C Brainard, Timothy M Brown, Robert T Dauchy, Altug Didikoglu, Michael Tri H Do, Brianna N Gaskill, Samer Hattar, Penny Hawkins, Roelof A Hut, Richard J McDowell, Randy J Nelson, Jan-Bas Prins, Tiffany M Schmidt, Joseph S Takahashi, Vandana Verma, Vootele Voikar, Sara Wells, Stuart N Peirson.
      Light enables vision and exerts widespread effects on physiology and behavior, including regulating circadian rhythms, sleep, hormone synthesis, affective state, and cognitive processes. Appropriate lighting in animal facilities may support welfare and ensure that animals enter experiments in an appropriate physiological and behavioral state. Furthermore, proper consideration of light during experimentation is important both when it is explicitly employed as an independent variable and as a general feature of the environment. This Consensus View discusses metrics to use for the quantification of light appropriate for nonhuman mammals and their application to improve animal welfare and the quality of animal research. It provides methods for measuring these metrics, practical guidance for their implementation in husbandry and experimentation, and quantitative guidance on appropriate light exposure for laboratory mammals. The guidance provided has the potential to improve data quality and contribute to reduction and refinement, helping to ensure more ethical animal use.
    DOI:  https://doi.org/10.1371/journal.pbio.3002535
  7. STAR Protoc. 2024 Mar 11. pii: S2666-1667(24)00100-X. [Epub ahead of print]5(2): 102935
    Protocol to study circadian food-anticipatory poking in mice using the feeding experimentation device version 3.
    David E Ehichioya, Ishrat Masud, S K Tahajjul Taufique, Byeongha Jeong, Sofia Farah, Averey Eischeid, Khaviya Balaji, Melody Shen, Joseph S Takahashi, Shin Yamazaki.
      Food-anticipatory nose poking is a unique food-seeking behavior driven by the food-entrainable oscillator. Here, we present a protocol to record a novel food-seeking nose poking behavior in mice under temporally restricted feeding followed by food deprivation using the open-source feeding experimentation device version 3 (FED3). We describe steps for setting up the FED3 and cage, training, and habituation. We then detail procedures for setting up the schedule for time-restricted feeding and food deprivation and for generating ethograms from FED3 data. For complete details on the use and execution of this protocol, please refer to Ehichioya et al.1.
    Keywords:  Behavior; Neuroscience
    DOI:  https://doi.org/10.1016/j.xpro.2024.102935
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