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A metabolome atlas of mouse brain on the global metabolic signature dynamics following short-term fasting

ABSTRACT: Calorie restriction (CR) or a fasting regimen is considered one of the most potent non-pharmacological interventions to prevent chronic metabolic disorders, ameliorate autoimmune diseases, and attenuate aging. Despite efforts, the mechanisms by which CR improves health, particularly brain health, are still not fully understood. Metabolic homeostasis is vital for brain function, and a detailed metabolome atlas of the brain is essential for understanding the networks connecting different brain regions. Herein, we applied gas chromatography–mass spectrometry-based metabolomics and lipidomics, covering 797 structurally annotated metabolites, to investigate the metabolome of seven brain regions in fasted (3, 6, 12, and 24 h) and ad libitum fed mice. Using multivariate and univariate statistical techniques, we generated a metabolome atlas of the mouse brain on the global metabolic signature dynamics across multiple brain regions following short-term fasting (STF). Significant metabolic differences across brain regions along with STF-triggered region-dependent metabolic remodeling were identified. We found that STF elicited triacylglycerol degradation and lipolysis to compensate for energy demand under conditions of food deprivation. Besides, a shift in amino acid patterns, including amino acid neurotransmitter, was observed, which may play crucial roles in the regulation of energy metabolism, neurotransmitter signaling, and anti-inflammatory and antioxidant responses to food restriction. Additionally, this study reported, for the first time, that STF triggers a significant elevation of N-acylethanolamines, a class of neuroprotective lipids, in the brain and liver. These findings provide novel insights into the molecular basis and mechanisms of CR and offer a comprehensive resource for further research.

INSTRUMENT(S): Liquid Chromatography MS - negative - reverse phase, Liquid Chromatography MS - positive, Gas Chromatography MS - positive

PROVIDER: MTBLS8006 | MetaboLights | 2025-07-31

REPOSITORIES: MetaboLights

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A metabolome atlas of mouse brain on the global metabolic signature dynamics following short-term fasting.

Shao Yaping Y Fu Zhenfa Z Wang Yanfeng Y Yang Zhaofei Z Lin Yushan Y Li Song S Cheng Cheng C Wei Min M Liu Zheyi Z Xu Guowang G Le Weidong W

Signal transduction and targeted therapy 20230908 1

Calorie restriction (CR) or a fasting regimen is considered one of the most potent non-pharmacological interventions to prevent chronic metabolic disorders, ameliorate autoimmune diseases, and attenuate aging. Despite efforts, the mechanisms by which CR improves health, particularly brain health, are still not fully understood. Metabolic homeostasis is vital for brain function, and a detailed metabolome atlas of the brain is essential for understanding the networks connecting different brain reg ...[more]

PMID: 37679319

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Project description:Moderate caloric restriction (CR) and weight loss are beneficial for the promotion of health; however, there is controversy regarding the effects of dieting regimens on behavior. In this study, we investigated two different dieting regimens: repeated fasting and refeeding (RFR) and daily feeding of half the amount of food consumed by RFR mice (CR). Mice in both regimens were subjected to 20% reduction in food intake and transiently reduced their body weights during the first 12 days of the study. Open field, light-dark transition, elevated plus maze, and forced swimming tests indicated that CR, but not RFR, reduced anxiety- and depressive-like behaviors, with a peak on day 8. Using a mouse whole genome microarray, we analyzed gene expression in the prefrontal cortex, amygdala, and hypothalamus. In addition to the caloric restriction-responsive genes commonly modified by RFR and CR, each regimen differentially changed the expression of distinct genes in each region. The most profound change was observed in the amygdala of CR mice: 884 genes were specifically up-regulated. Ingenuity pathway analysis showed that these 884 genes significantly modified 9 canonical pathways in the amygdala. alpha-adrenergic and dopamine receptor signaling were the two top-scoring pathways. Quantitative real-time RT-PCR confirmed the up-regulation of 6 genes in these pathways. Ppp1r1b encoded Darpp-32 including dopamine receptor signaling, and the increased protein was specific for CR mice. Our results suggest that moderate CR may modify anxiety- and depressive-like behaviors and alter gene expression especially in the mouse amygdala. Experiment Overall Design: We tested three feeding regimens. One group of mice had ad libitum (AD) access to food, and was used as a control group. The repeated fasting and refeeding (RFR) group of mice were fasted on day 0 and allowed to feed ad libitum on day 1. Amounts of food consumed by the three mice on day 1 were measured. The half amount of food consumed by the RFR mice was given to three mice in another cage for two days (days 0 and 1) (CR group). The fasting followed by refeeding (RFR) and the restriction of food (CR) were repeated up to day 16. Body weights and consumed chow were measured at 20:00 every day, and then the fasting or feeding period was started. In RFR mice, fasting was started on day 0.Total RNA was prepared from the prefrontal cortex, hypothalamus, and amygdala in the mice of each group on day 8. An equal amount of RNA from 4 mice in each group was pooled and used for microarray analysis.

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