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Alterations of fecal microbiota and plasma metabolome in patients with Parkinson's disease with rapid eye movement sleep disorder

ABSTRACT:

Objectives: Patients with Parkinson's disease (PD) with probable Rapid eye movement sleep Behavior Disorder (RBD) (PD-RBD), a specific subtype of PD, is characterized by the presence of more severe motor and non-motor symptoms. This study aimed to elucidate the characteristics and interactions of gut microbiota and plasma metabolic characteristics of PD-RBD, thus screening for the disease mechanisms.

Methods: A total of 100 PD patients, 50 healthy controls (HC) and 16 probable idiopathic RBD (iRBD) patients were collected. There were 33 PD-RBD and 67 patients without probable RBD (PD-nRBD) in PD patients. DNA extraction, PCR amplification and high-throughput sequencing were used for intestinal microbiota analysis and ultra-high liquid chromatography tandem mass spectrometry was used for metabolome analysis. Spearman analysis was applied to investigate the correlation of fecal microbiota and plasma metabolome.

Results: Our findings revealed Lactobacillaceae (P = 0.017), Christensenellaceae (P = 0.017), Fusobacteriaceae (P = 0.018), Lactobacillus (P = 0.035), Christensenellaceae R-7 group (P = 0.035) and Fusobacterium (P = 0.035) were significant different in PD-RBD, PD-nRBD and HC. Moreover, the differential metabolites identified in both PD-nRBD and PD-RBD were 3-Hydroxy-2-methylpyridine-4,5-dicarboxylate (VIP = 5.802) and 3-Methoxy-4-Hydroxyphenylglycol sulfate (VIP = 5.732). Furthermore, our analysis revealed that 3-Methoxy-4-Hydroxyphenylglycol sulfate showed a positive correlation with Lactobacillus (r = 0.197, P = 0.049). Finally, functional analysis indicated that these distinctive microbiota and metabolites were primarily associated with phenylalanine metabolism and vitamin B6 metabolism.

Conclusions: We managed to show that the differential microbiota, differential metabolites and their interactions in PD-RBD compared to PD-nRBD and HC. This furthers our understanding of disease pathogenesis, and offers fresh perspectives on its detection and treatment.

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

PROVIDER: MTBLS11094 | MetaboLights | 2025-05-07

REPOSITORIES: MetaboLights

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Project description:Background: Parkinson's disease (PD) is a common neurodegenerative disorder characterized by both motor and non-motor symptoms, including olfactory dysfunction, which often precedes motor symptoms by several years. However, the underlying mechanisms linking olfactory dysfunction in PD to biological changes remain unclear. Recent studies suggest a potential connection between PD's olfactory dysfunction and alterations in the nasal microbiome and metabolome, but comprehensive investigations are still lacking.This study aims to explore the interplay between nasal microbiota, metabolites, and olfactory function in PD, identify potential biomarkers for early diagnosis, and investigate therapeutic targets for olfactory dysfunction in PD. Methods: From October 1, 2023, to September 30, 2024, 66 potential participants were enrolled, including PD patients with varying degrees of olfactory dysfunction and healthy controls. Nasal samples were collected for 16S rRNA sequencing and metabolomic analysis using GC-MS. The study also used MPTP-induced PD mouse models to assess the protective effects of cholic acid on olfactory function and dopaminergic neurons. Results: The study found significant differences in nasal microbiota composition and metabolite profiles between PD patients and controls, with correlations to the severity of olfactory dysfunction. Specifically, the relative abundances of Corynebacterium, Dolosigranulum, Muribacter, and Moraxella were elevated in the PD group, while the abundances of Hydrogenophaga, Staphylococcus, Klebsiella, and Bacillus decreased. Metabolomic analysis revealed that cholic acid, octanal, hexadecanol, and phytol were significantly altered in PD patients compared to controls, with cholic acid showing potential as a diagnostic biomarker (AUC > 0.97). In MPTP-induced PD mouse models, cholic acid treatment significantly reduced latencies in detecting buried food pellets, and increased tyrosine hydroxylase (TH)-positive fluorescence intensity in the olfactory bulb and substantia nigra. However, cholic acid did not significantly ameliorate motor symptoms in PD mice, as assessed by the open field test, and did not prevent the loss of TH+ cells in the striatum. Conclusion: The findings highlight the interplay between the nasal microbiome, metabolome, and olfactory dysfunction in PD, suggesting that modulating metabolic pathways could be a promising therapeutic strategy. Future research should focus on larger sample sizes, longitudinal studies, and further validation of biomarkers and therapeutic targets to enhance the understanding and management of PD.

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Alterations of fecal microbiota and plasma metabolome in patients with Parkinson's disease with rapid eye movement sleep disorder

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