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A Low-Protein, High-Carbohydrate Diet Exerts a Neuroprotective Effect on Mice with 1-Methyl-4-phenyl-1,2,3,6-tetrahydropyridine-Induced Parkinson’s Disease by Regulating the Microbiota-Metabolite–Brain Axis and Fibroblast Growth Factor 21

  • Chuanqi Chu
    Chuanqi Chu
    State Key Laboratory of Food Science and Technology, Jiangnan University, Wuxi, Jiangsu 214122, China
    School of Food Science and Technology, Jiangnan University, Wuxi, Jiangsu 214122, China
    More by Chuanqi Chu
  • Tiantian Li
    Tiantian Li
    State Key Laboratory of Food Science and Technology, Jiangnan University, Wuxi, Jiangsu 214122, China
    School of Food Science and Technology, Jiangnan University, Wuxi, Jiangsu 214122, China
    More by Tiantian Li
  • Leilei Yu*
    Leilei Yu
    State Key Laboratory of Food Science and Technology, Jiangnan University, Wuxi, Jiangsu 214122, China
    School of Food Science and Technology, Jiangnan University, Wuxi, Jiangsu 214122, China
    *Email address: [email protected] (L.-L. Yu).
    More by Leilei Yu
  • Yiwen Li
    Yiwen Li
    Department of Food Science and Technology, The University of Georgia, Athens, Georgia 30602, United States
    More by Yiwen Li
  • Miaoyu Li
    Miaoyu Li
    State Key Laboratory of Food Science and Technology, Jiangnan University, Wuxi, Jiangsu 214122, China
    School of Food Science and Technology, Jiangnan University, Wuxi, Jiangsu 214122, China
    More by Miaoyu Li
  • Min Guo
    Min Guo
    State Key Laboratory of Food Science and Technology, Jiangnan University, Wuxi, Jiangsu 214122, China
    School of Food Science and Technology, Jiangnan University, Wuxi, Jiangsu 214122, China
    More by Min Guo
  • Jianxin Zhao
    Jianxin Zhao
    State Key Laboratory of Food Science and Technology, Jiangnan University, Wuxi, Jiangsu 214122, China
    School of Food Science and Technology, Jiangnan University, Wuxi, Jiangsu 214122, China
    More by Jianxin Zhao
  • Qixiao Zhai
    Qixiao Zhai
    State Key Laboratory of Food Science and Technology, Jiangnan University, Wuxi, Jiangsu 214122, China
    School of Food Science and Technology, Jiangnan University, Wuxi, Jiangsu 214122, China
    More by Qixiao Zhai
  • Fengwei Tian*
    Fengwei Tian
    State Key Laboratory of Food Science and Technology, Jiangnan University, Wuxi, Jiangsu 214122, China
    School of Food Science and Technology, Jiangnan University, Wuxi, Jiangsu 214122, China
    *Email address: [email protected] (F.-W. Tian).
    More by Fengwei Tian
  • , and 
  • Wei Chen
    Wei Chen
    State Key Laboratory of Food Science and Technology, Jiangnan University, Wuxi, Jiangsu 214122, China
    School of Food Science and Technology, Jiangnan University, Wuxi, Jiangsu 214122, China
    National Engineering Research Center for Functional Food, Jiangnan University, Wuxi, Jiangsu 214122, China
    More by Wei Chen
Cite this: J. Agric. Food Chem. 2023, 71, 23, 8877–8893
Publication Date (Web):June 2, 2023
https://doi.org/10.1021/acs.jafc.2c07606
Copyright © 2023 American Chemical Society

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    Abstract

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    Parkinson’s disease (PD) is closely linked to lifestyle factors, particularly dietary patterns, which have attracted interest as potential disease-modifying factors. Eating a low-protein, high-carbohydrate (LPHC) diet is a promising dietary intervention against brain aging; however, its protective effect on PD remains elusive. Here, we found that an LPHC diet ameliorated 1-methyl-4-phenyl-1,2,3,6-tetrathydropyridine (MPTP)-induced motor deficits, decreased dopaminergic neuronal death, and increased the levels of striatal dopamine, serotonin, and their metabolites in PD mice. Levels of fibroblast growth factor 21 (FGF-21), a member of the fibroblast growth factor family, were elevated in PD mice following LPHC treatment. Furthermore, the administration of FGF-21 exerted a protective effect on MPTP-induced PC12 cells, similar to the effect of an LPHC diet in MPTP-induced mice. Sequencing of the 16S rDNA from fecal microbiota revealed that an LPHC diet normalized the gut bacterial composition imbalance in PD mice, as evidenced by the increased abundance of the genera Bifidobacterium, Ileibacterium, Turicibacter, and Blautia and decreased abundance of Bilophila, Alistipes, and Bacteroides. PICRUSt-predicted fecal microbiome function revealed that an LPHC diet suppressed lipopolysaccharide biosynthesis and the citrate cycle (TCA cycle), biosynthesis of ubiquinone and other terpenoid-quinones, and oxidative phosphorylation pathways caused by MPTP, and enhanced the biosynthesis of amino acids, carbohydrate metabolism, and biosynthesis of other secondary metabolites. A nonmetabolomic analysis of the serum and feces showed that an LPHC diet significantly increased the levels of aromatic amino acids (AAAs), including tryptophan, tyrosine, and phenylalanine. In addition, an LPHC diet elevated the serum concentrations of bile acids (BAs), particularly tauroursodeoxycholic acid (TUDCA) and taurine. Collectively, our current findings point to the potential mechanism of administering an LPHC diet in attenuating movement impairments in MPTP-induced PD mice, with AAAs, microbial metabolites (TUDCA and taurine), and FGF-21 as key mediators along the gut-microbiota–brain axis.

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    Supporting Information

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    The Supporting Information is available free of charge at https://pubs.acs.org/doi/10.1021/acs.jafc.2c07606.

    • Protocols of the behavioral test, measurement of neurotransmitters, immunohistochemistry and image analysis, Nissl staining, enzyme-linked immunosorbent assay, gut microbiota profiling, functional prediction analysis, fecal and serum untargeted metabolomics analysis, metabolomic data analysis, cell culture and treatments, cell viability assay, released lactate dehydrogenase activity assay and mitochondrial membrane potential assay are described in the Supplementary Methods part; the nutrient compositions and ingredients of the experimental diets are described in Table S1; Supplemental data for the effect FGF-21 on cell survival in MPTP-injured PC12 cells (Figure S1); the pattern search analysis (Figure S2) and univariate statistical comparisons (Figure S3) of the gut microbiome; the scores plot of the 3D-PLS-DA analysis of fecal metabolites and serumal metabolites (Figure S4); correlation heatmap analysis and network analysis between differential gut microbiotas and the level of FGF-21 in serum and midbrain (Figure S5) (PDF)

    • Results of enrichment analysis based on SMPDB for differential fecal metabolites (Table S2); the differential fecal metabolites among the three groups (Table S3); results of enrichment analysis based on KEGG for differential serum metabolites (Table S4); the differential serumal metabolites among the three groups (Table S5) (XLSX)

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