Probiotic Enhancement of Antioxidant Capacity and Alterations of Gut Microbiota Composition in 6-Hydroxydopamin-Induced Parkinson’s Disease Rats
Abstract
:1. Introduction
2. Materials and Methods
2.1. Supplements
2.2. Animals and Study Design
2.3. Unilateral 6-OHDA Lesions
2.4. Evaluation of Neuroprotective Effects
2.4.1. Immunohistochemical Staining and Image Analysis
2.4.2. Behavioral Tests
2.5. Evaluation of Oxidative Stress and Inflammation Markers in Serum
2.5.1. ROS Assay
2.5.2. Quantification of Antioxidant Enzyme Activity
2.5.3. Quantification of Inflammatory Cytokines
2.6. Evaluation of Microbiota Composition and Microbial Metabolites
2.6.1. Bacterial Genomic DNA Isolation
2.6.2. 16S rRNA Amplicon Sequencing and Data Analysis
2.6.3. High-Performance Liquid Chromatography (HPLC)
2.7. Statistical Analyses
3. Results
3.1. Long-Term Probiotic and Prebiotic Supplementation Ameliorated General Motor Symptoms and Confered Neuroprotective Effects in Rats with 6-OHDA-Induced PD
3.2. Probiotic and Prebiotic Supplementation Reduced Inflammation, Promoted Antioxidant Activity, and Increased SCFA Production
3.3. Long-Term Probiotic and Prebiotic Supplementation Alter 6-OHDA-Induced Gut Dysbiosis by Remodeling the Composition of the Fecal Microbiota
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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ND | PD | LD | 1X | MR | 1XMR | |
---|---|---|---|---|---|---|
ROS (% normal control) | 100.0 ± 5.8 | 187.5 ± 11.0 a | 172.4 ± 19.0 | 105.0 ± 21.3 b | 113.7 ± 10.3 b | 107.4 ± 12.1 b |
TNF-α (pg/mL) | 43.9 ± 1.5 | 64.9 ± 1.6 a | 59.9 ± 2.4 ab | 51.2 ± 1.7 ab | 53.7 ± 2.9 ab | 52.0 ± 2.3 ab |
SOD activity (mU/mL) | 68.7 ± 8.3 | 43.7 ± 1.6 a | 47.0 ± 1.6 ab | 51.6 ± 2.8 ab | 49.8 ± 1.6 ab | 50.6 ± 1.1 ab |
GPx activity (mU/mL) | 65.3 ± 4.4 | 53.9 ± 2.1 a | 58.5 ± 1.4 b | 60.5 ± 1.1 b | 58.6 ± 1.0 b | 59.3 ± 1.2 b |
Catalase activity (mU/mL) | 4.8 ± 0.1 | 3.4 ± 0.3 a | 3.6 ± 0.5 a | 4.4 ± 0.6 b | 3.8 ± 0.3 a | 3.8 ± 0.1 ab |
Progression Parameters | Correlation | Bacterial Taxa |
---|---|---|
Time on the rod(s) | + | Synergistes (r = 0.353; p = 0.040) |
SOD 1 activity (mU/mL) | + | Eggerthella (r = 0.497; p = 0.003) |
GPx activity (mU/mL) | + | Eggerthella (r = 0.402; p = 0.018) |
Catalase activity (mU/mL) | + | Bacteroides (r = 0.404; p = 0.017), Anaerostipes (r = 0.473; p = 0.004), Prevotella (r = 0.391; p = 0.022), Sutterella (r = 0.392; p = 0.021), Catenibacterium (r = 0.503; p = 0.002), Megamonas (r = 0.489; p = 0.003), Citrobacter (r = 0.517; p = 0.001), Synergistes (r = 0.450; p = 0.007), Eggerthella (r = 0.372; p = 0.030) |
− | Lactobacillus (r = −0.372; p = 0.030) |
Progression Parameters | Correlation | Bacterial Taxa |
---|---|---|
Contralateral rotation (rotations/minute) | + | Lactobacillus reuteri (r = 0.343; p = 0.046), Lactobacillus apis (r = 0.380; p = 0.026) |
Time on the rod(s) | − | Lactobacillus apis (r = −0.343; p = 0.046), Lactobacillus amylolyticus (r = −0.365; p = 0.033), |
SOD 1 activity (mU/mL) | − | Lactobacillus reuteri (r = −0.383; p = 0.025), Lactobacillus antri (r = −0.393; p = 0.035), Lactobacillus frumenti (r = −0.343; p = 0.046), Lactobacillus camelliae (r = −0.385; p = 0.024), Lactobacillus senmaizukei (r = −0.366; p = 0.032), Lactobacillus panis (r = −0.378; p = 0.027), Lactobacillus amylolyticus (r = −0.421; p = 0.013) |
GPx activity (mU/mL) | − | Lactobacillus reuteri (r = −0.360; p = 0.036), Lactobacillus apis (r = −0.351; p = 0.041), Lactobacillus camelliae (r = −0.376; p = 0.028) |
Catalase activity (mU/mL) | + | Bifidobacterium adolescentis (r = 0.411; p = 0.015), Bifidobacterium longum (r = 0.341; p = 0.048), Lactobacillus plantarum (r = 0.483; p = 0.030), Lactobacillus pentosus (r = 0.395; p = 0.020), Lactobacillus japonicus (r = 0.381; p = 0.026) |
− | Lactobacillus taiwanensis (r = −0.371; p = 0.030), Lactobacillus siliginis (r = −0.387; p = 0.023), Lactobacillus intermedius (r = −0.429; p = 0.011), Lactobacillus salivarius (r = −0.399; p = 0.019), Lactobacillus tucceti (r = −0.400; p = 0.018), Lactobacillus panis (r = −0.362; p = 0.035) |
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Tsao, S.-P.; Nurrahma, B.A.; Kumar, R.; Wu, C.-H.; Yeh, T.-H.; Chiu, C.-C.; Lee, Y.-P.; Liao, Y.-C.; Huang, C.-H.; Yeh, Y.-T.; et al. Probiotic Enhancement of Antioxidant Capacity and Alterations of Gut Microbiota Composition in 6-Hydroxydopamin-Induced Parkinson’s Disease Rats. Antioxidants 2021, 10, 1823. https://doi.org/10.3390/antiox10111823
Tsao S-P, Nurrahma BA, Kumar R, Wu C-H, Yeh T-H, Chiu C-C, Lee Y-P, Liao Y-C, Huang C-H, Yeh Y-T, et al. Probiotic Enhancement of Antioxidant Capacity and Alterations of Gut Microbiota Composition in 6-Hydroxydopamin-Induced Parkinson’s Disease Rats. Antioxidants. 2021; 10(11):1823. https://doi.org/10.3390/antiox10111823
Chicago/Turabian StyleTsao, Shu-Ping, Bira Arumndari Nurrahma, Ravi Kumar, Chieh-Hsi Wu, Tu-Hsueh Yeh, Ching-Chi Chiu, Yen-Peng Lee, Yi-Chi Liao, Cheng-Hsieh Huang, Yao-Tsung Yeh, and et al. 2021. "Probiotic Enhancement of Antioxidant Capacity and Alterations of Gut Microbiota Composition in 6-Hydroxydopamin-Induced Parkinson’s Disease Rats" Antioxidants 10, no. 11: 1823. https://doi.org/10.3390/antiox10111823
APA StyleTsao, S.-P., Nurrahma, B. A., Kumar, R., Wu, C.-H., Yeh, T.-H., Chiu, C.-C., Lee, Y.-P., Liao, Y.-C., Huang, C.-H., Yeh, Y.-T., & Huang, H.-Y. (2021). Probiotic Enhancement of Antioxidant Capacity and Alterations of Gut Microbiota Composition in 6-Hydroxydopamin-Induced Parkinson’s Disease Rats. Antioxidants, 10(11), 1823. https://doi.org/10.3390/antiox10111823