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Progression of intestinal permeability changes and alpha-synuclein expression in a mouse model of Parkinson's disease
Open accessAbstract
Parkinson's disease (PD) is a multifocal degenerative disorder for which there is no cure. The majority of cases are sporadic with unknown etiology. Recent data indicate that untreated patients with de novo PD have increased colonic permeability and that both de novo and premotor patients have pathological expression of α‐synuclein (α‐syn) in their colon. Both endpoints potentially can serve as disease biomarkers and even may initiate PD events through gut‐derived, lipopolysaccharide (LPS)‐induced neuronal injury. Animal models could be ideal for interrogating the potential role of the intestines in the pathogenesis of PD; however, few current animal models of PD encompass these nonmotor features. We sought to establish a progressive model of PD that includes the gastrointestinal (GI) dysfunction present in human patients. C57/BL6 mice were systemically administered one dose of either LPS (2.5 mg/kg) or saline and were sacrificed in monthly intervals (n = 5 mice for 5 months) to create a time‐course. Small and large intestinal permeability was assessed by analyzing the urinary output of orally ingested sugar probes through capillary column gas chromatography. α‐Syn expression was assessed by counting the number of mildly, moderately, and severely affected myenteric ganglia neurons throughout the GI tract, and the counts were validated by quantitative optical density measurements. Nigrostriatal integrity was assessed by tyrosine hydroxylase immunohistochemistry stereology and densitometry. LPS caused an immediate and progressive increase in α‐syn expression in the large intestine but not in the small intestine. Intestinal permeability of the whole gut (large and small intestines) progressively increased between months 2 and 4 after LPS administration but returned to baseline levels at month 5. Selective measurements demonstrated that intestinal permeability in the small intestine remained largely intact, suggesting that gut leakiness was predominately in the large intestine. Phosphorylated serine 129‐α‐syn was identified in a subset of colonic myenteric neurons at months 4 and 5. Although these changes were observed in the absence of nigrostriatal degeneration, an abrupt but insignificant increase in brainstem α‐syn was observed that paralleled the restoration of permeability. No changes were observed over time in controls. LPS, an endotoxin used to model PD, causes sequential increases in α‐syn immunoreactivity, intestinal permeability, and pathological α‐syn accumulation in the colon in a manner similar to that observed in patients with PD. These features are observed without nigrostriatal degeneration and incorporate PD features before the motor syndrome. This allows for the potential use of this model in testing neuroprotective and disease‐modifying therapies, including intestinal‐directed therapies to fortify intestinal barrier integrity. © 2013 International Parkinson and Movement Disorder Society
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“A leaky gut barrier has been linked to PD pathogenesis involving local flux of bacterial toxins, microbes, and potentially molecules like α-synuclein across the gastrointestinal epithelium [29–31]”
From The gut–brain axis in early Parkinson’s disease: from prodrome to prevention (2025) · cites this paper as [30]
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“LPS produced by gut microbiota treatment can increase the accumulation of a-synuclein in the enteric nervous system and increase intestinal permeability.128”
From The role of gut dysbiosis in Parkinson’s disease: mechanistic insights and therapeutic options (2021) · cites this paper as [128]
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“injection of endotoxin into mice induces α-synuclein production and aggregation, as well as loss of dopaminergic neurons in the substantia nigra.”
From The endotoxin hypothesis of neurodegeneration (2019) · cites this paper as [99]
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“A single dose of peripheral endotoxin in mice caused increased expression of α-synuclein in neurons of the large intestine, followed by an increase in large intestinal permeability, in a manner similar to that observed in patients with PD [99].”
From The endotoxin hypothesis of neurodegeneration (2019) · cites this paper as [99]
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Metadata
- Authors
- Kelly, L. P., Carvey, P. M., Keshavarzian, A., Shannon, K. M., Shaikh, M., Bakay, R. A. E., & Kordower, J. H.
- Affiliations
- Rush University (US)
- Utrecht University (NL)
- Corresponding author
- Kordower, Jeffrey H.
- Venue
- Movement Disorders
- Publisher
- Wiley
- Published
- 2013-11-04
- Volume
- 29
- Issue
- 8
- Pages
- 999-1009
- ISSN
- 0885-3185 (ISSN-L)
- 1531-8257
- PMC
- PMC4050039
- OpenAlex
- W2108108635
- Cited by
- 308
- References
- 61
- Citations by year
- 2026: 11 · 2025: 21 · 2024: 28 · 2023: 55 · 2022: 34 · 2021: 54 · 2020: 29 · 2019: 24 · 2018: 18 · 2017: 13 · 2016: 6 · 2015: 9 · 2014: 6
- FWCI
- 4.44
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Movement Disorders (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of Neurological Disorders and Stroke (R01NS055143)
- Topics
- Health Sciences › Medicine › Clinical Neurology › Parkinson's Disease Mechanisms and Treatments
- Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nuclear Receptors and Signaling
- Keywords
- Parkinson's disease, intestinal permeability, alpha-synuclein, lipopolysaccharide, gastrointestinal dysfunction, nigrostriatal degeneration, tyrosine hydroxylase, disease biomarkers, mouse model, gut-brain axis
- MeSH terms
- Animals, Brain, Chromatography, Gas, Colon, Disease Models, Animal, Gastrointestinal Agents, Male, Mice, Inbred C57BL, Parkinson Disease, Permeability, Polysaccharides, Severity of Illness Index, Time Factors, Tyrosine 3-Monooxygenase, Vagus Nerve, Linear Models, Disease Progression, Mice, alpha-Synuclein
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