Leaky intestine and impaired microbiome in an amyotrophic lateral sclerosis mouse model
Open accessAbstract
Emerging evidence has demonstrated that intestinal homeostasis and the microbiome play essential roles in neurological diseases, such as Parkinson's disease. Amyotrophic lateral sclerosis (ALS) is a fatal neurodegenerative disease characterized by a progressive loss of motor neurons and muscle atrophy. Currently, there is no effective treatment. Most patients die within 3-5 years due to respiratory paralysis. Although the death of motor neurons is a hallmark of ALS, other organs may also contribute to the disease progression. We examined the gut of an ALS mouse model, G93A, which expresses mutant superoxide dismutase (SOD1(G93A)), and discovered a damaged tight junction structure and increased permeability with a significant reduction in the expression levels of tight junction protein ZO-1 and the adherens junction protein E-cadherin. Furthermore, our data demonstrated increased numbers of abnormal Paneth cells in the intestine of G93A mice. Paneth cells are specialized intestinal epithelial cells that can sense microbes and secrete antimicrobial peptides, thus playing key roles in host innate immune responses and shaping the gut microbiome. A decreased level of the antimicrobial peptides defensin 5 alpha was indeed found in the ALS intestine. These changes were associated with a shifted profile of the intestinal microbiome, including reduced levels of Butyrivibrio Fibrisolvens, Escherichia coli, and Fermicus, in G93A mice. The relative abundance of bacteria was shifted in G93A mice compared to wild-type mice. Principal coordinate analysis indicated a difference in fecal microbial communities between ALS and wild-type mice. Taken together, our study suggests a potential novel role of the intestinal epithelium and microbiome in the progression of ALS.
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Growing evidence has indicated alterations in the gut microbiome and impaired intestinal barrier integrity in both ALS patients and animal models.
“Nevertheless, growing evidence has indicated alterations in the gut microbiome and impaired intestinal barrier integrity in both ALS patients and animal models.221–225”
From Microbiota–gut–brain axis and its therapeutic applications in neurodegenerative diseases (2024) · cites this paper as [221]
Reduced butyrate-producing species are identified in ALS patients and SOD1G93A mice.
“Furthermore, studies have identified reduced butyrate-producing species in ALS patients and SOD1G93A mice.221,222,345,346”
From Microbiota–gut–brain axis and its therapeutic applications in neurodegenerative diseases (2024) · cites this paper as [221]
These changes were associated with reduced expression of tight junction and adherent junction proteins, as well as impairment of the intestinal barrier, leading to increased intestinal permeability.
“These changes were associated with reduced expression of tight junction (TJ) and adherent junction (AJ) proteins, as well as impairment of the intestinal barrier, leading to increased intestinal permeability.”
From Modulation of the gut–brain axis via the gut microbiota: a new era in treatment of amyotrophic lateral sclerosis (2023) · cites this paper as [48]
An ALS-specific SOD1G93A mouse model exhibited dysregulation of the intestinal ecology early in the disease progression, before the onset of neuromuscular symptoms.
“A study by Wu et al. (48) found that an ALS-specific SOD1G93A mouse model exhibited dysregulation of the intestinal ecology (characterized by a reduction in the abundance of Vibrio fibrate butyric acidophilus, Escherichia coli, and thick-walled phylum) early in the disease progression, before the onset of neuromuscular symptoms.”
From Modulation of the gut–brain axis via the gut microbiota: a new era in treatment of amyotrophic lateral sclerosis (2023) · cites this paper as [48]
In ALS, there are biological barriers to the gut microbiota and microbial metabolites.
“Clinical and experimental evidence (48) suggests the presence of biological barriers to the gut microbiota and microbial metabolites in ALS.”
From Modulation of the gut–brain axis via the gut microbiota: a new era in treatment of amyotrophic lateral sclerosis (2023) · cites this paper as [48]
In SOD1G93A mice, intestines have impaired tight junction structures, increased permeability, reduced expression of ZO-1 and E-cadherin, reduced normal Paneth cells, and increased IL-17.
“Wu et al. (48) found that the intestines of SOD1G93A mice (with impaired tight junction structures) exhibited increased permeability, significantly reduced expression levels of tight junction protein ZO-1 and adhesion junction protein E-cadherin, significantly reduced normal Paneth cells, and increased levels of inflammatory cytokine IL-17.”
From Modulation of the gut–brain axis via the gut microbiota: a new era in treatment of amyotrophic lateral sclerosis (2023) · cites this paper as [48]
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- Authors
- Wu, S., Yi, J., Zhang, Y.-G., Zhou, J., & Sun, J.
- Affiliations
- Rush University Medical Center (US)
- Kansas City University (US)
- Department of Biochemistry; Rush University Medical Center; Chicago Illinois
- Corresponding author
- Zhou, Jingsong
- Sun, Jun
- Venue
- Physiological Reports
- Publisher
- Wiley
- Published
- 2015-04
- Volume
- 3
- Issue
- 4
- Pages
- e12356
- ISSN
- 2051-817X (ISSN-L)
- PMC
- PMC4425962
- OpenAlex
- W2096776344
- Cited by
- 267
- References
- 52
- Citations by year
- 2026: 18 · 2025: 21 · 2024: 49 · 2023: 29 · 2022: 24 · 2021: 32 · 2020: 27 · 2019: 19 · 2018: 26 · 2017: 13 · 2016: 6 · 2015: 2
- FWCI
- 6.81
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Physiological Reports (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Funders
- NIDDK (KO1 DK075386, 1R03DK089010-01)
- NIAMS/National Institutes of Health (R01 AR057404)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Medicine › Neurology › Amyotrophic Lateral Sclerosis Research
- Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
- Keywords
- amyotrophic lateral sclerosis, intestinal permeability, gut microbiota, SOD1 G93A mouse model, tight junctions, ZO-1, E-cadherin, Paneth cells, antimicrobial peptides, intestinal epithelium, neurodegeneration, Butyrivibrio fibrisolvens, Escherichia coli, Firmicutes
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