Microglial Activation Contributes to Cognitive Impairments in Rotenone-Induced Mouse Parkinson’s Disease Model
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Abstract
BACKGROUND: Cognitive decline occurs frequently in Parkinson's disease (PD), which greatly decreases the quality of life of patients. However, the mechanisms remain to be investigated. Neuroinflammation mediated by overactivated microglia is a common pathological feature in multiple neurological disorders, including PD. This study is designed to explore the role of microglia in cognitive deficits by using a rotenone-induced mouse PD model. METHODS: To evaluate the role of microglia in rotenone-induced cognitive deficits, PLX3397, an inhibitor of colony-stimulating factor 1 receptor, and minocycline, a widely used antibiotic, were used to deplete or inactivate microglia, respectively. Cognitive performance of mice among groups was detected by Morris water maze, objective recognition, and passive avoidance tests. Neurodegeneration, synaptic loss, α-synuclein phosphorylation, glial activation, and apoptosis were determined by immunohistochemistry and Western blot or immunofluorescence staining. The gene expression of inflammatory factors and lipid peroxidation were further explored by using RT-PCR and ELISA kits, respectively. RESULTS: Rotenone dose-dependently induced cognitive deficits in mice by showing decreased performance of rotenone-treated mice in the novel objective recognition, passive avoidance, and Morris water maze compared with that of vehicle controls. Rotenone-induced cognitive decline was associated with neurodegeneration, synaptic loss, and Ser129-phosphorylation of α-synuclein and microglial activation in the hippocampal and cortical regions of mice. A time course experiment revealed that rotenone-induced microglial activation preceded neurodegeneration. Interestingly, microglial depletion by PLX3397 or inactivation by minocycline significantly reduced neuronal damage and α-synuclein pathology as well as improved cognitive performance in rotenone-injected mice. Mechanistically, PLX3397 and minocycline attenuated rotenone-induced astroglial activation and production of cytotoxic factors in mice. Reduced lipid peroxidation was also observed in mice treated with combined PLX3397 or minocycline and rotenonee compared with rotenone alone group. Finally, microglial depletion or inactivation was found to mitigate rotenone-induced neuronal apoptosis. CONCLUSIONS: Taken together, our findings suggested that microglial activation contributes to cognitive impairments in a rotenone-induced mouse PD model via neuroinflammation, oxidative stress, and apoptosis, providing novel insight into the immunopathogensis of cognitive deficits in PD.
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CSF1R inhibitors have the potential to attenuate neurodegeneration in toxic PD models involving rotenone, 6-hydroxydopamine, and MPTP.
“several studies have demonstrated the potential of CSF1R inhibitors in attenuating neurodegeneration in toxic PD models involving rotenone24, 6-hydroxydopamine21, and MPTP25.”
From Microglial inhibition alleviates alpha-synuclein propagation and neurodegeneration in Parkinson’s disease mouse model (2024) · cites this paper as [24]
Minocycline molecular changes explain increased striatal dopamine levels and cognitive and locomotor improvements in zebrafish, mouse, and rat models.
“Of note, these molecular changes seem to explain the increased striatal dopamine levels as well as the cognitive and locomotor improvements observed in zebrafish, mouse, and rat models [259,260,264,268,269,270,271].”
From The Interplay between Gut Microbiota and Parkinson’s Disease: Implications on Diagnosis and Treatment (2022) · cites this paper as [260]
Minocycline suppresses microglia activation.
“This effect is mainly ascribable to the minocycline-dependent suppression of microglia activation, which has been reported by several in vivo studies [251,258,259,260,261,262,263].”
From The Interplay between Gut Microbiota and Parkinson’s Disease: Implications on Diagnosis and Treatment (2022) · cites this paper as [260]
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“In addition, several studies have demonstrated the potential of CSF1R inhibitors in attenuating neurodegeneration in toxic PD models involving rotenone 24 , 6-hydroxydopamine 21 , and MPTP 25 .”
BackgroundMicroglial Extracellular Vesicles as Vehicles for Neurodegeneration Spreading
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- Authors
- Zhang, D., Li, S., Hou, L., Jing, L., Ruan, Z., Peng, B., Zhang, X., Hong, J.-S., Zhao, J., & Wang, Q.
- Affiliations
- Dalian Medical University (CN)
- National Institutes of Health (US)
- Corresponding author
- Zhao, Jie
- Wang, Qingshan
- ORCID
- Venue
- Journal of Neuroinflammation
- Published
- 2021-01-05
- Volume
- 18
- Issue
- 1
- Pages
- 4-4
- ISSN
- 1742-2094 (ISSN-L)
- PMC
- PMC7786472
- OpenAlex
- W3111358404
- Cited by
- 187
- References
- 70
- Citations by year
- 2026: 18 · 2025: 40 · 2024: 65 · 2023: 27 · 2022: 24 · 2021: 13
- FWCI
- 12.91
- Type
- journal article
- Language
- en
- Update notices
- correction (2025-05-24)
- Open access
- gold
- doi.org
- Locations
- Journal of Neuroinflammation (publishedVersion, cc-by)
- Research Square (acceptedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, other-oa)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- National Natural Science Foundation of China (81973087)
- Natural Science Foundation of Liaoning Province (2019-MS-077)
- LiaoNing Revitalization Talents Program (XLYC1907026)
- Topics
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Health Sciences › Medicine › Neurology › Parkinson's Disease Mechanisms and Treatments
- Life Sciences › Neuroscience › Neurology › Neurological Disease Mechanisms and Treatments
- Keywords
- Parkinson's disease, cognitive impairment, microglial activation, neuroinflammation, rotenone, PLX3397, minocycline, microglial depletion, alpha-synuclein phosphorylation, neurodegeneration, synaptic loss, astroglial activation, lipid peroxidation, oxidative stress, neuronal apoptosis, hippocampus, immunopathogenesis
- MeSH terms
- Aminopyridines, Animals, Insecticides, Male, Mice, Inbred C57BL, Minocycline, Pyrroles, Rotenone, Microglia, Parkinsonian Disorders, Mice, Cognitive Dysfunction
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