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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 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 fasting conditions. Besides, changes in amino acid profiles were observed, which may play crucial roles in the regulation of energy metabolism, neurotransmitter signaling, and anti-inflammatory and antioxidant in response to STF. 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 investigation.

SUBMITTER: Shao Y

PROVIDER: S-EPMC10484938 | biostudies-literature | 2023 Sep

REPOSITORIES: biostudies-literature

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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:BackgroundSevere trauma, including burns, triggers a systemic response that significantly impacts on the liver, which plays a key role in the metabolic and immune responses aimed at restoring homeostasis. While many of these changes are likely regulated at the gene expression level, there is a need to better understand the dynamics and expression patterns of burn injury-induced genes in order to identify potential regulatory targets in the liver. Herein we characterized the response within the first 24 h in a standard animal model of burn injury using a time series of microarray gene expression data.MethodsRats were subjected to a full thickness dorsal scald burn injury covering 20% of their total body surface area while under general anesthesia. Animals were saline resuscitated and sacrificed at defined time points (0, 2, 4, 8, 16, and 24 h). Liver tissues were explanted and analyzed for their gene expression profiles using microarray technology. Sham controls consisted of animals handled similarly but not burned. After identifying differentially expressed probe sets between sham and burn conditions over time, the concatenated data sets corresponding to these differentially expressed probe sets in burn and sham groups were combined and analyzed using a "consensus clustering" approach.ResultsThe clustering method of expression data identified 621 burn-responsive probe sets in four different co-expressed clusters. Functional characterization revealed that these four clusters are mainly associated with pro-inflammatory response, anti-inflammatory response, lipid biosynthesis, and insulin-regulated metabolism. Cluster 1 pro-inflammatory response is rapidly up-regulated (within the first 2 h) following burn injury, while Cluster 2 anti-inflammatory response is activated later on (around 8 h post-burn). Cluster 3 lipid biosynthesis is down-regulated rapidly following burn, possibly indicating a shift in the utilization of energy sources to produce acute phase proteins, which serve the anti-inflammatory response. Cluster 4 insulin-regulated metabolism was down-regulated late in the observation window (around 16 h post-burn), which suggests a potential mechanism to explain the onset of hypermetabolism, a delayed but well-known response that is characteristic of severe burns and trauma with potential adverse outcome.ConclusionsSimultaneous analysis and comparison of gene expression profiles for both burn and sham control groups provided a more accurate estimation of the activation time, expression patterns, and characteristics of a certain burn-induced response based on which the cause-effect relationships among responses were revealed.

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

Publications

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

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