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Fecal Microbiota Transplantation from Aged Mice Render Recipient Mice Resistant to MPTP-Induced Nigrostriatal Degeneration Via a Neurogenesis-Dependent but Inflammation-Independent Manner

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Neurotherapeutics

Abstract

Accumulating data support a crucial role of gut microbiota in Parkinson’s disease (PD). However, gut microbiota vary with age and, thus, will affect PD in an age-dependent, but unknown manner. We examined the effects of fecal microbiota transplantation (FMT) pretreatment, using fecal microbiota from young (7 weeks) or aged mice (23 months), on MPTP-induced PD model. Motor function, pathological changes, striatal neurotransmitters, neuroinflammation, gut inflammation and gut permeability were examined. Gut microbiota composition and metabolites, namely short-chain fatty acids (SCFAs), were analyzed. Neurogenesis was also evaluated by measuring the number of doublecortin-positive (DCX+) neurons and Ki67-positive (Ki67+) cells in the hippocampus. Expression of Cd133 mRNA, a cellular stemness marker, in the hippocampus was also examined. Mice who received FMT from young mice showed MPTP-induced motor dysfunction, and reduction of striatal dopamine (DA), dopaminergic neurons and striatal tyrosine hydroxylase (TH) levels. Interestingly and unexpectedly, mice that received FMT from aged mice showed recovery of motor function and rescue of dopaminergic neurons and striatal 5-hydroxytryptamine (5-HT), as well as decreased DA metabolism after MPTP challenge. Further, they showed improved metabolic profiling and a decreased amount of fecal SCFAs. High-throughput sequencing revealed that FMT remarkably reshaped the gut microbiota of recipient mice. For instance, levels of genus Akkermansia and Candidatus Saccharimonas were elevated in fecal samples of recipient mice receiving aged microbiota (AM + MPTP mice) than YM + MPTP mice. Intriguingly, both young microbiota and aged microbiota had no effect on neuroinflammation, gut inflammation or gut permeability. Notably, AM + MPTP mice showed a marked increase in DCX+ neurons, as well as Ki67+ cells and Cd133 expression in the hippocampal dentate gyrus (DG) compared to YM + MPTP mice. These results suggest that FMT from aged mice augments neurogenesis, improves motor function and restores dopaminergic neurons and neurotransmitters in PD model mice, possibly through increasing neurogenesis.

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Data Availability

The data that support the findings of this study are available from the corresponding author upon reasonable request.

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Acknowledgements

This study was supported by National Natural Science Foundation of China (81771384, 81801276, 82171429), Postgraduate Research and Practice Innovation Program of Jiangsu Province (KYCX19 1893), Public Health Research Center at Jiangnan University (JUPH201801), Youth Foundation of Basic Research Program of Jiangnan University in 2021 (JUSRP121063). We are grateful to Dr. Stanley Li Lin for his critical revision on the manuscript, both on language and science.

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  1. Chen-Meng Qiao and Yu Zhou contributed equally.

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  1. Laboratory of Neurodegeneration and Neuroinjury, Wuxi School of Medicine, Jiangnan University, Wuxi, Jiangsu, 214122, China

    Chen-Meng Qiao, Yu Zhou, Wei Quan, Xiao-Yu Ma, Li-Ping Zhao, Yun Shi, Hui Hong, Jian Wu, Gu-Yu Niu, Yu-Nuo Chen, Shan Zhu, Chun Cui, Wei-Jiang Zhao & Yan-Qin Shen

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Contributions

The experiment design and management: Chen-Meng Qiao and Yan-Qin Shen; Animal experiment operation: Chen-Meng Qiao, Yu-Zhou, Wei Quan, Gu-Yu Niu and Xiao-Yu Ma; Tissue collection: Chen-Meng Qiao, Yu-Zhou, Wei Quan, Gu-Yu Niu, Yun Shi, Li-Ping Zhao, Xiao-Yu Ma, Hui Hong and Jian Wu; HPLC/16S rRNA: Chen-Meng Qiao, Yu Zhou and Wei Quan; Quantitative real-time PCR analysis: Yu Zhou and Wei Quan; IF/IHC and image analysis: Yu Zhou, Wei Quan, Chen-Meng Qiao, Xiao-Yu Ma and Wei-Jiang Zhao; Western bolt: Yu Zhou and Wei Quan; Nissl staining: Chen-Meng Qiao, Wei Quan and Xiao-Yu Ma; Statistical analysis: Chen-Meng Qiao and Yu Zhou; Writing and revising of manuscript: Chen-Meng Qiao and Yan-Qin Shen.

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Qiao, CM., Zhou, Y., Quan, W. et al. Fecal Microbiota Transplantation from Aged Mice Render Recipient Mice Resistant to MPTP-Induced Nigrostriatal Degeneration Via a Neurogenesis-Dependent but Inflammation-Independent Manner. Neurotherapeutics 20, 1405–1426 (2023). https://doi.org/10.1007/s13311-023-01420-1

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