Microglia, inflammation and gut microbiota responses in a progressive monkey model of Parkinson's disease: A case series
Open accessAbstract
Inflammation has been linked to the development of nonmotor symptoms in Parkinson's disease (PD), which greatly impact patients' quality of life and can often precede motor symptoms. Suitable animal models are critical for our understanding of the mechanisms underlying disease and the associated prodromal disturbances. The neurotoxin 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP)-treated monkey model is commonly seen as a “gold standard” model that closely mimics the clinical motor symptoms and the nigrostriatal dopaminergic loss of PD, however MPTP toxicity extends to other nondopaminergic regions. Yet, there are limited reports monitoring the MPTP-induced progressive central and peripheral inflammation as well as other nonmotor symptoms such as gastrointestinal function and microbiota. We report 5 cases of progressive parkinsonism in non-human primates to gain a broader understanding of MPTP-induced central and peripheral inflammatory dysfunction to understand the potential role of inflammation in prodromal/pre-motor features of PD-like degeneration. We measured inflammatory proteins in plasma and CSF and performed [18F]FEPPA PET scans to evaluate translocator proteins (TSPO) or microglial activation. Monkeys were also evaluated for working memory and executive function using various behavior tasks and for gastrointestinal hyperpermeability and microbiota composition. Additionally, monkeys were treated with a novel TNF inhibitor XPro1595 (10 mg/kg, n = 3) or vehicle (n = 2) every three days starting 11 weeks after the initiation of MPTP to determine whether XPro1595 would alter inflammation and microglial behavior in a progressive model of PD. The case studies revealed that earlier and robust [18F]FEPPA PET signals resulted in earlier and more severe parkinsonism, which was seen in male cases compared to female cases. Potential other sex differences were observed in circulating inflammation, microbiota diversity and their metabolites. Additional studies with larger group sizes of both sexes would enable confirmation and extension of these findings. If these findings reflect potential differences in humans, these sex differences have significant implications for therapeutic development of inflammatory targets in the clinic.
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Cytokines and chemokines related to gut microbiota or pathogen-derived products may be involved in the pathogenesis of intestinal inflammation via TLRs.
“Cytokines and chemokines related to gut microbiota or pathogen-derived products may be involved in the pathogenesis of intestinal inflammation via TLRs.122”
From The role of gut dysbiosis in Parkinson’s disease: mechanistic insights and therapeutic options (2021) · cites this paper as [122]
The Gastrointestinal Assessments methods describe measuring gut microbiota and circulating LPS, while the Introduction discusses the pro-inflammatory cytokine TNF in Parkinson’s disease. Neither passage links microbiota- or pathogen-derived products to intestinal inflammation through TLRs; searches for TLR and toll-like receptors found no passage addressing that mechanism. (LLM, conf=0.76)
Experimental — accuracy not yet measuredThe increase in TLR4, TLR5 and the proinflammatory factor IL-6 and the decrease in the anti-inflammatory factor IL-10 in the mucosa of patients with irritable bowel syndrome were related to alterations in the gut microbiota.
“The increase in TLR4, TLR5 and the proinflammatory factor IL-6 and the decrease in the anti-inflammatory factor IL-10 in the mucosa of patients with irritable bowel syndrome were related to alterations in the gut microbiota.122”
From The role of gut dysbiosis in Parkinson’s disease: mechanistic insights and therapeutic options (2021) · cites this paper as [122]
The Discussion addresses gut-microbiota changes in a monkey model of Parkinson’s disease, while the Materials and Methods describe gastrointestinal measurements in those monkeys. Searches for irritable bowel syndrome, TLR4, TLR5, IL-6 and IL-10 found no passage linking the claimed mucosal changes to gut microbiota in patients with irritable bowel syndrome. (LLM, conf=0.78)
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- Authors
- Joers, V., Masilamoni, G., Kempf, D., Weiss, A. R., Rotterman, T. M., Murray, B., Yalcin-Cakmakli, G., Voll, R. J., Goodman, M. M., Howell, L., Bachevalier, J., Green, S. J., Naqib, A., Shaikh, M., Engen, P. A., Keshavarzian, A., Barnum, C. J., Nye, J. A., Smith, Y., & Tansey, M. G.
- Affiliations
- Emory University (US)
- Oregon National Primate Research Center (US)
- Georgia Institute of Technology (US)
- University of Illinois Chicago (US)
- Rush University Medical Center (US)
- Corresponding author
- Joers, Valerie
- ORCID
- Venue
- Neurobiology of Disease
- Publisher
- Elsevier BV
- Published
- 2020-10
- Volume
- 144
- Pages
- 105027
- ISSN
- 0969-9961 (ISSN-L)
- PMC
- PMC7484290
- OpenAlex
- W3044513361
- Cited by
- 56
- References
- 101
- Citations by year
- 2026: 3 · 2025: 9 · 2024: 7 · 2023: 10 · 2022: 12 · 2021: 13 · 2020: 2
- FWCI
- 4.00
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Neurobiology of Disease (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- Michael J. Fox Foundation for Parkinson's Research
- National Institutes of Health
- Parkinson's Disease Foundation
- Topics
- Health Sciences › Medicine › Neurology › Parkinson's Disease Mechanisms and Treatments
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Nuclear Receptors and Signaling
- Keywords
- Parkinson's disease, MPTP, nonhuman primate model, microglial activation, neuroinflammation, gut microbiota, non-motor symptoms, translocator protein (TSPO), TNF inhibitor, XPro1595, sex differences, executive function, prodromal Parkinson's disease
- MeSH terms
- Gastrointestinal Microbiome, Tumor Necrosis Factor Inhibitors, Anilides, Animals, Behavior, Animal, Cognition, Disease Models, Animal, Fatty Acids, Volatile, Female, Inflammation, Macaca mulatta, Magnetic Resonance Imaging, Male, Neurotoxins, Pyridines, Tumor Necrosis Factor-alpha, 1-Methyl-4-phenyl-1,2,3,6-tetrahydropyridine, Microglia, Disease Progression, Parkinsonian Disorders, Positron-Emission Tomography
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