Fecal microbiota transplantation protects rotenone-induced Parkinson’s disease mice via suppressing inflammation mediated by the lipopolysaccharide-TLR4 signaling pathway through the microbiota-gut-brain axis

Zhao, Zhe; Ning, Jingwen; Bao, Xiu-qi; Shang, Meiyu; Ma, Jingwei; Li, Gen; Zhang, Dan

doi:10.1186/s40168-021-01107-9

Cited by 617Parkinson's Disease Mechanisms and TreatmentsGut microbiota and healthNeuroinflammation and Neurodegeneration Mechanisms

Fecal microbiota transplantation protects rotenone-induced Parkinson’s disease mice via suppressing inflammation mediated by the lipopolysaccharide-TLR4 signaling pathway through the microbiota-gut-brain axis

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Zhao, Zhe, Ning, Jingwen, Bao, Xiu-qi, Shang, Meiyu, Ma, Jingwei, Li, Gen, Zhang, Dan·2021·Microbiome

DOI 10.1186/s40168-021-01107-9PMC PMC8597301

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Abstract

Background: Parkinson’s disease (PD) is a prevalent neurodegenerative disorder, displaying not only well-known motor deficits but also gastrointestinal dysfunctions. Consistently, it has been increasingly evident that gut microbiota affects the communication between the gut and the brain in PD pathogenesis, known as the microbiota-gut-brain axis. As an approach to re-establishing a normal microbiota community, fecal microbiota transplantation (FMT) has exerted beneficial effects on PD in recent studies. Here, in this study, we established a chronic rotenone-induced PD mouse model to evaluate the protective effects of FMT treatment on PD and to explore the underlying mechanisms, which also proves the involvement of gut microbiota dysbiosis in PD pathogenesis via the microbiota-gut-brain axis. Results: We demonstrated that gut microbiota dysbiosis induced by rotenone administration caused gastrointestinal function impairment and poor behavioral performances in the PD mice. Moreover, 16S RNA sequencing identified the increase of bacterial genera Akkermansia and Desulfovibrio in fecal samples of rotenone-induced mice. By contrast, FMT treatment remarkably restored the gut microbial community, thus ameliorating the gastrointestinal dysfunctions and the motor deficits of the PD mice. Further experiments revealed that FMT administration alleviated intestinal inflammation and barrier destruction, thus reducing the levels of systemic inflammation. Subsequently, FMT treatment attenuated blood-brain barrier (BBB) impairment and suppressed neuroinflammation in the substantia nigra (SN), which further decreased the damage of dopaminergic neurons. Additional mechanistic investigation discovered that FMT treatment reduced lipopolysaccharide (LPS) levels in the colon, the serum, and the SN, thereafter suppressing the TLR4/MyD88/NF-κB signaling pathway and its downstream pro-inflammatory products both in the SN and the colon. Conclusions: Our current study demonstrates that FMT treatment can correct the gut microbiota dysbiosis and ameliorate the rotenone-induced PD mouse model, in which suppression of the inflammation mediated by the LPS-TLR4 signaling pathway both in the gut and the brain possibly plays a significant role. Further, we prove that rotenone-induced microbiota dysbiosis is involved in the genesis of PD via the microbiota-gut-brain axis.

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FMT from normal control mice into neurotoxin-induced PD mice protects dopaminergic neurons by suppressing the TLR4 inflammatory pathway.
“FMT from normal control mice into neurotoxin-induced PD mice could protect dopaminergic neurons by suppressing the TLR4 inflammatory pathway [18, 19]”
From Healthy Human Fecal Microbiota Transplantation into Mice Attenuates MPTP-Induced Neurotoxicity via AMPK/SOD2 Pathway (2023) · cites this paper as [19]
Previous studies have demonstrated that FMT from healthy control mice relieved motor impairments in MPTP/rotenone-induced PD mice.
“Consistently, previous studies have demonstrated that FMT from healthy control mice relieved motor impairments in MPTP/rotenone-induced PD mice [18, 19].”
From Healthy Human Fecal Microbiota Transplantation into Mice Attenuates MPTP-Induced Neurotoxicity via AMPK/SOD2 Pathway (2023) · cites this paper as [19]
FMT from healthy control mice exerted a neuroprotective effect in neurotoxin-induced PD mice.
“FMT from healthy control mice exerted a neuroprotective effect in neurotoxin-induced PD mice [18, 19]”
From Healthy Human Fecal Microbiota Transplantation into Mice Attenuates MPTP-Induced Neurotoxicity via AMPK/SOD2 Pathway (2023) · cites this paper as [19]
Intestinal inflammation is a crucial contributor to PD development.
“Intestinal inflammation is a crucial contributor to PD development [53,54,55,56].”
From Neuroprotective Effects of Bifidobacterium breve CCFM1067 in MPTP-Induced Mouse Models of Parkinson’s Disease (2022) · cites this paper as [54]
Tight junction proteins ZO-1 and occludin contribute significantly to maintenance of the intestinal barrier.
“Tight junction proteins, such as ZO-1 and occludin, contribute significantly to the maintenance of the intestinal barrier, which aids in protecting immune cells underneath the intestinal mucosa from invading infections [54,63,64].”
From Neuroprotective Effects of Bifidobacterium breve CCFM1067 in MPTP-Induced Mouse Models of Parkinson’s Disease (2022) · cites this paper as [54]

Feces of patients with PD transplanted in germ-free mice showed severe motor impairments, inflammation, and other pathological symptoms.
“the feces of patients with PD transplanted in germ-free mice showed severe motor impairments, inflammation, and other pathological symptoms [12].”
From Neuroprotective Effects of Sodium Butyrate by Restoring Gut Microbiota and Inhibiting TLR4 Signaling in Mice with MPTP-Induced Parkinson’s Disease (2023) · cites this paper as [12]
Due to increased intestinal permeability, microbial toxins and pro-inflammatory mediators produced as a result of gut dysbiosis can leak into the circulation causing systemic inflammation, in turn destroying the blood-brain barrier and causing neuroinflammation.
“Due to increased intestinal permeability, microbial toxins and pro-inflammatory mediators produced as a result of gut dysbiosis can leak into the circulation causing systemic inflammation, in turn destroying the blood–brain barrier and causing neuroinflammation [12,64].”
From Neuroprotective Effects of Sodium Butyrate by Restoring Gut Microbiota and Inhibiting TLR4 Signaling in Mice with MPTP-Induced Parkinson’s Disease (2023) · cites this paper as [12]
Consistent preclinical studies and a handful of human case reports have shown that FMT might reduce motor and non-motor symptoms, as well as constipation, in PD at least in the short term.
“Concerning PD, consistent preclinical studies and a handful of human case reports have shown that FMT might be exploited to reduce motor and non-motor symptoms, as well as constipation, at least in the short term [40,465,469,470,471,472,473,474,475,476,477] (Table 4).”
From The Interplay between Gut Microbiota and Parkinson’s Disease: Implications on Diagnosis and Treatment (2022) · cites this paper as [470]
FMT appears to protect from gut inflammation by promoting intestinal barrier integrity and reducing LPS levels in the colon, serum, and SN, preventing leaky gut and systemic inflammation.
“Moreover, FMT appears to protect from gut inflammation by promoting intestinal barrier integrity and reducing the levels of LPS in the colon, serum, and SN, therefore preventing leaky gut and systemic inflammation [470].”
From The Interplay between Gut Microbiota and Parkinson’s Disease: Implications on Diagnosis and Treatment (2022) · cites this paper as [470]
Decreased neuroinflammation following FMT has been reported by numerous preclinical studies.
“Notably, decreased neuroinflammation following FMT has been reported by numerous preclinical studies [469,470,471,472].”
From The Interplay between Gut Microbiota and Parkinson’s Disease: Implications on Diagnosis and Treatment (2022) · cites this paper as [470]
Fecal matter transplantation from healthy mice to PD recipient mice improved physical performance, ameliorated motor symptoms and reduced dysbiosis in several independent studies.
“Conversely, fecal matter transplantation from healthy mice to PD recipient mice improved physical performance, ameliorated motor symptoms and reduced dysbiosis in several independent studies [469,470,471,472].”
From The Interplay between Gut Microbiota and Parkinson’s Disease: Implications on Diagnosis and Treatment (2022) · cites this paper as [470]
FMT re-establishes eubiosis by disadvantaging growth of Desulfovibrio, Akkermansia and Proteobacteria (orders Enterobacteriales and Turicibacteriales), while favoring proliferation of Bacteroidetes and Actinobacteria phyla, particularly Blautia and Prevotella species.
“Looking at the GM composition, there is evidence that FMT re-establishes eubiosis by disadvantaging the growth of Desulfovibrio, Akkermansia and Proteobacteria (orders Enterobacteriales and Turicibacteriales), while simultaneously favoring the proliferation of beneficial bacteria such as Bacteroidetes and Actinobacteria phyla, with a particular effect on Blautia and Prevotella species [469,470,472”
From The Interplay between Gut Microbiota and Parkinson’s Disease: Implications on Diagnosis and Treatment (2022) · cites this paper as [470]
The beneficial effect of FMT on neuroinflammation is ascribed to GM modulating microglia and astrocyte activation in SN by regulating the TLR4/NF-κB pathway and reducing expression of GSK3β, iNOS and IL-1β.
“This beneficial effect should be ascribed to the ability of GM to modulate microglia and astrocyte activation in SN by regulating the TLR4/NF-κB pro-inflammatory pathway and reducing the expression of GSK3β, iNOS and IL-1β, which are implicated in PD pathogenesis and progression [469,470,471,472,478,479,480].”
From The Interplay between Gut Microbiota and Parkinson’s Disease: Implications on Diagnosis and Treatment (2022) · cites this paper as [470]

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Intestinal pathology and gut microbiota alterations in a methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) mouse model of Parkinson's disease
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Novel phloroglucinol derivative Compound 21 protects experimental autoimmune encephalomyelitis rats via inhibiting Th1/Th17 cell infiltration
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Gut Microbiota Dynamics in Parkinsonian Mice
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Microbiota–gut–brain axis and its therapeutic applications in neurodegenerative diseases
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Microplastics-perturbed gut microbiota triggered the testicular disorder in male mice: Via fecal microbiota transplantation
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Healthy Human Fecal Microbiota Transplantation into Mice Attenuates MPTP-Induced Neurotoxicity via AMPK/SOD2 Pathway
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The Endotoxin Hypothesis of Parkinson's Disease
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Neuroprotective Effects of Bifidobacterium breve CCFM1067 in MPTP-Induced Mouse Models of Parkinson’s Disease
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Toll-like receptors and NLRP3 inflammasome-dependent pathways in Parkinson’s disease: mechanisms and therapeutic implications
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Lactobacillus plantarum CCFM405 against Rotenone-Induced Parkinson’s Disease Mice via Regulating Gut Microbiota and Branched-Chain Amino Acids Biosynthesis
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Role of gut microbiota-derived branched-chain amino acids in the pathogenesis of Parkinson’s disease: An animal study
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Minimally invasive vagus nerve stimulation modulates mast cell degranulation via the microbiota-gut-brain axis to ameliorate blood-brain barrier and intestinal barrier damage following ischemic stroke
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IgA nephropathy: gut microbiome regulates the production of hypoglycosilated IgA1 via the TLR4 signaling pathway
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Authors: Zhao, Z., Ning, J., Bao, X.-Q., Shang, M., Ma, J., Li, G., & Zhang, D.
Affiliations: Chinese Academy of Medical Sciences & Peking Union Medical College (CN)
Corresponding author: Zhang, Dan
ORCID: Zhao, Zhe
Ma, Jingwei
Li, Gen
Zhang, Dan
Venue: Microbiome
Publisher: Springer Science and Business Media LLC
Published: 2021-11-17
Volume: 9
Issue: 1
Pages: 226-226
ISSN: 2049-2618 (ISSN-L)
DOI: 10.1186/s40168-021-01107-9
PMC: PMC8597301
OpenAlex: W3211876735
Cited by: 616
References: 100
Citations by year: 2026: 122 · 2025: 179 · 2024: 183 · 2023: 91 · 2022: 39 · 2019: 1 · 2013: 1
FWCI: 37.52
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
creativecommons.org/licenses/by/4.0 (tdm)
creativecommons.org/licenses/by/4.0 (vor)
Locations: Microbiome (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders: National Sciences Foundation of China (81773718, 81630097, 81773589)
The National Key Research and Development Program of China (SQ2018YFA090025-04)
CAMS Innovation Fund for Medical Sciences (2016-I2M-3-011)
The Drug Innovation Major Project (2018ZX09711001-003-020, 2018ZX09711001-003-005, 2018ZX09711001-008-005)
CAMS The Fundamental Research Funds for the Central Universities (2018RC350002)
CAMS & PUMC Innovation Fund for Graduate (2019-1007-23)
Topics: Health Sciences › Medicine › Neurology › Parkinson's Disease Mechanisms and Treatments
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
Keywords: Parkinson's disease, fecal microbiota transplantation, microbiota-gut-brain axis, rotenone-induced neurotoxicity, gut dysbiosis, lipopolysaccharide, TLR4/MyD88/NF-κB signaling, neuroinflammation, blood-brain barrier, dopaminergic neuron damage, Akkermansia, Desulfovibrio, intestinal barrier dysfunction, gastrointestinal dysfunction
MeSH terms: Gastrointestinal Microbiome, Fecal Microbiota Transplantation, Brain-Gut Axis, Animals, Inflammation, Lipopolysaccharides, Mice, Inbred C57BL, Parkinson Disease, Rotenone, Signal Transduction, Toll-Like Receptor 4, Mice

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Fecal microbiota transplantation protects rotenone-induced Parkinson’s disease mice via suppressing inflammation mediated by the lipopolysaccharide-TLR4 signaling pathway through the microbiota-gut-brain axis

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