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Prebiotics modulate the microbiota–gut–brain axis and ameliorate cognitive impairment in APP/PS1 mice

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Abstract

Purpose

Prebiotics, including fructo-oligosaccharides (FOS) and galacto-oligosaccharides (GOS), stimulate beneficial gut bacteria and may be helpful for patients with Alzheimer’s disease (AD). This study aimed to compare the effects of FOS and GOS, alone or in combination, on AD mice and to identify their underlying mechanisms.

Methods

Six-month-old APP/PS1 mice and wild-type mice were orally administered FOS, GOS, FOS + GOS or water by gavage for 6 weeks and then subjected to relative assays, including behavioral tests, biochemical assays and 16S rRNA sequencing.

Results

Through behavioral tests, we found that GOS had the best effect on reversing cognitive impairment in APP/PS1 mice, followed by FOS + GOS, while FOS had no effect. Through biochemical techniques, we found that GOS and FOS + GOS had effects on multiple targets, including diminishing Aβ burden and proinflammatory IL-1β and IL-6 levels, and changing the concentrations of neurotransmitters GABA and 5-HT in the brain. In contrast, FOS had only a slight anti-inflammatory effect. Moreover, through 16S rRNA sequencing, we found that prebiotics changed composition of gut microbiota. Notably, GOS increased relative abundance of Lactobacillus, FOS increased that of Bifidobacterium, and FOS + GOS increased that of both. Furthermore, prebiotics downregulated the expression levels of proteins of the TLR4-Myd88-NF-κB pathway in the colons and cortexes, suggesting the involvement of gut–brain mechanism in alleviating neuroinflammation.

Conclusion

Among the three prebiotics, GOS was the optimal one to alleviate cognitive impairment in APP/PS1 mice and the mechanism was attributed to its multi-target role in alleviating Aβ pathology and neuroinflammation, changing neurotransmitter concentrations, and modulating gut microbiota.

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Data availability

All data used during the study are available from the corresponding author by request.

Abbreviations

AD:

Alzheimer’s disease

APP/PS1:

APPswe/PS1dE9 transgenic mice

WT:

Wild-type

Tg:

Transgenic

FOS:

Fructo-oligosaccharides

GOS:

Galacto-oligosaccharides

GABA:

Gamma-aminobutyric acid

5-HT:

5-Hydroxytryptamine

Ach:

Acetylcholine

Glu:

Glutamate

Gln:

l-Glutamine

DA:

Dopamine

5-HIAA:

5-Hydroxyindole acetic acid

NMDA:

N-Methyl-d-aspartate

LPS:

Lipopolysaccharide

TLR4:

Toll like receptor 4

TLRs:

Toll like receptors

Myd88:

Myeloid differentiation primary response gene 88

NF-κB:

Nuclear factor-κB

IL-6:

Interleukin 6

IL-1β:

Interleukin 1β

TNF-α:

Tumor necrosis factor α

IL-10:

Interleukin 10

CNS:

Central nervous system

GluN1:

N-Methyl-aspartate receptor subunit 1

GluN2B:

N-Methyl-aspartate receptor subunit 2B

GluR1:

Glutamate AMPA receptor subunit A1

GluR2:

Glutamate AMPA receptor subunit A2

LC/MS:

Liquid chromatography/mass spectrometry

SCFAs:

Short-chain fatty acids

OF:

Open field test

NOR:

Novel object recognition test

EPM:

Elevated plus maze test

ST:

Social test

MWM:

Morris water maze test

IHC:

Immunohistochemistry staining

WB:

Western blot

RT‒PCR:

Reverse transcriptase polymerase chain reaction

IBA1:

Ionized calcium-binding adaptor 1

GFAP:

Glial fibrillary acidic protein

ASD:

Autism spectrum disorder

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Funding

This work was supported in part by the National Natural Science Foundation of China (Grant number 81974220), the Central Health Research Project (Grant number 2020ZD10), the National Science Fund for Distinguished Young Scholars (Grant number 81625025), and the Cultivated Fund of Capital Medical University (Grant number QNPY2022002, PYZ22051).

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Author notes

  1. Shujuan Zhang and Shuang Lv contributed equally to this work.

Authors and Affiliations

  1. Department of Rehabilitation Medicine, Xuan Wu Hospital, Capital Medical University, 45 Chang Chun Street, Beijing, 100053, China

    Shujuan Zhang & Weiqun Song

  2. Peking University China-Japan Friendship School of Clinical Medicine, Beijing, 100029, China

    Shujuan Zhang, Shuang Lv, Xiaoqian Niu, Ziyuan Yang & Dantao Peng

  3. Department of Neurology, China-Japan Friendship Hospital, 2 Yinghuayuan East Street, Chaoyang District, Beijing, 100029, China

    Shujuan Zhang, Shuang Lv, Xiaoqian Niu, Ziyuan Yang & Dantao Peng

  4. Department of Rheumatology, the First Hospital of Hebei Medical University, No. 89 Donggang Road, Yuhua District, Shijiazhuang, 050031, Hebei, China

    Shuang Lv

  5. State Key Laboratory of Cognitive Neuroscience and Learning and IDG/McGovern Institute for Brain Research, Beijing Normal University, Beijing, 100875, China

    Zhanjun Zhang

  6. Department of Cardiovasology, the First Hospital of Hebei Medical University, No. 89 Donggang Road, Yuhua District, Shijiazhuang, 050031, Hebei, China

    Yiming Li

  7. Institute of Basic Research in Clinical Medicine, China Academy of Chinese Medical Sciences, Beijing, 100700, China

    Dongfeng Wei

  8. Department of Neurology, Graduate School of Peking Union Medical College and Chinese Academy of Medical Sciences, Beijing, 100005, China

    Xiao Zhou

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  1. Shujuan Zhang
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Contributions

DP, ZZ and WS designed research; SZ, SL, YL, DW, XZ, XN, and ZY performed research; SZ and SL analyzed data; and SZ, SL, DP and ZZ wrote the paper. All authors have read and approved the final manuscript.

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Correspondence to Weiqun Song, Zhanjun Zhang or Dantao Peng.

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Zhang, S., Lv, S., Li, Y. et al. Prebiotics modulate the microbiota–gut–brain axis and ameliorate cognitive impairment in APP/PS1 mice. Eur J Nutr 62, 2991–3007 (2023). https://doi.org/10.1007/s00394-023-03208-7

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