Agathobaculum butyriciproducens Shows Neuroprotective Effects in a 6-OHDA-Induced Mouse Model of Parkinson's Disease |
Lee, Da Woon
(Laboratory Animal Resource Center, Korea Research Institute of Bioscience and Biotechnology (KRIBB))
Ryu, Young-Kyoung (Laboratory Animal Resource Center, Korea Research Institute of Bioscience and Biotechnology (KRIBB)) Chang, Dong-Ho (Microbiome Convergence Research Center, Korea Research Institute of Bioscience and Biotechnology (KRIBB)) Park, Hye-Yeon (Laboratory Animal Resource Center, Korea Research Institute of Bioscience and Biotechnology (KRIBB)) Go, Jun (Laboratory Animal Resource Center, Korea Research Institute of Bioscience and Biotechnology (KRIBB)) Maeng, So-Young (Laboratory Animal Resource Center, Korea Research Institute of Bioscience and Biotechnology (KRIBB)) Hwang, Dae Youn (Department of Biomaterials Science, College of Natural Resources and Life Science and Industry Convergence Research Institute, Pusan National University) Kim, Byoung-Chan (Microbiome Convergence Research Center, Korea Research Institute of Bioscience and Biotechnology (KRIBB)) Lee, Chul-Ho (Laboratory Animal Resource Center, Korea Research Institute of Bioscience and Biotechnology (KRIBB)) Kim, Kyoung-Shim (Laboratory Animal Resource Center, Korea Research Institute of Bioscience and Biotechnology (KRIBB)) |
1 | Zheng P, Zeng B, Zhou C, Liu M, Fang Z, Xu X, et al. 2016. Gut microbiome remodeling induces depressive-like behaviors through a pathway mediated by the host's metabolism. Mol. Psychiatry 21: 786-796. DOI |
2 | Ansari F, Pourjafar H, Tabrizi A, Homayouni A. 2020. The effects of probiotics and prebiotics on mental disorders: A review on depression, anxiety, alzheimer, and autism spectrum disorders. Curr. Pharm. Biotechnol. 21: 555-565. DOI |
3 | Huang H, Xu H, Luo Q, He J, Li M, Chen H, et al. 2019. Fecal microbiota transplantation to treat Parkinson's disease with constipation: A case report. Medicine (Baltimore) 98: e16163. DOI |
4 | Hsieh TH, Kuo CW, Hsieh KH, Shieh MJ, Peng CW, Chen YC, et al. 2020. Probiotics alleviate the progressive deterioration of motor functions in a mouse model of Parkinson's disease. Brain Sci. 10: 206. DOI |
5 | Srivastav S, Neupane S, Bhurtel S, Katila N, Maharjan S, Choi H, et al. 2019. Probiotics mixture increases butyrate, and subsequently rescues the nigral dopaminergic neurons from MPTP and rotenone-induced neurotoxicity. J. Nutr. Biochem. 69: 73-86. DOI |
6 | Bruce-Keller AJ, Salbaum JM, Luo M, Blanchard Et, Taylor CM, Welsh DA, et al. 2015. Obese-type gut microbiota induce neurobehavioral changes in the absence of obesity. Biol. Psychiatry 77: 607-615. DOI |
7 | Everard A, Belzer C, Geurts L, Ouwerkerk JP, Druart C, Bindels LB, et al. 2013. Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity. Proc. Natl. Acad. Sci. USA 110: 9066-9071. DOI |
8 | Keshavarzian A, Green SJ, Engen PA, Voigt RM, Naqib A, Forsyth CB, et al. 2015. Colonic bacterial composition in Parkinson's disease. Mov. Disord. 30: 1351-1360. DOI |
9 | Go J, Chang DH, Ryu YK, Park HY, Lee IB, Noh JR, et al. 2021. Human gut microbiota Agathobaculum butyriciproducens improves cognitive impairment in LPS-induced and APP/PS1 mouse models of Alzheimer's disease. Nutr Res. 86: 96-108. DOI |
10 | Hirsch EC, Hunot S. 2009. Neuroinflammation in Parkinson's disease: a target for neuroprotection? Lancet Neurol. 8: 382-397. DOI |
11 | Ryu YK, Park HY, Go J, Choi DH, Kim YH, Hwang JH, et al. 2018. Metformin inhibits the development of L-DOPA-induced dyskinesia in a murine model of Parkinson's disease. Mol. Neurobiol. 55: 5715-5726. DOI |
12 | Go J, Park TS, Han GH, Park HY, Ryu YK, Kim YH, et al. 2018. Piperlongumine decreases cognitive impairment and improves hippocampal function in aged mice. Int. J. Mol. Med. 42: 1875-1884. DOI |
13 | Ryu YK, Kang Y, Go J, Park HY, Noh JR, Kim YH, et al. 2017. Humulus japonicus prevents dopaminergic neuron death in 6-hydroxydopamine-induced models of Parkinson's disease. J. Med. Food 20: 116-123. DOI |
14 | Glinka Y, Gassen M, Youdim MB. 1997. Mechanism of 6-hydroxydopamine neurotoxicity. J. Neural. Transm. Suppl. 50: 55-66. DOI |
15 | Castelli V, d'Angelo M, Lombardi F, Alfonsetti M, Antonosante A, Catanesi M, et al. 2020. Effects of the probiotic formulation SLAB51 in in vitro and in vivo Parkinson's disease models. Aging (Albany NY) 12: 4641-4659. DOI |
16 | Park TS, Ryu YK, Park HY, Kim JY, Go J, Noh JR, et al. 2017. Humulus japonicus inhibits the progression of Alzheimer's disease in a APP/PS1 transgenic mouse model. Int. J. Mol. Med. 39: 21-30. DOI |
17 | Park HY, Kang YM, Kang Y, Park TS, Ryu YK, Hwang JH, et al. 2014. Inhibition of adenylyl cyclase type 5 prevents L-DOPA-induced dyskinesia in an animal model of Parkinson's disease. J. Neurosci. 34: 11744-11753. DOI |
18 | Keith BJ Fraklin GP. 2007. The mouse brain in stereotaxic coordinates, Third edition Ed. Elsevier, New York, USA. |
19 | Ryu YK, Go J, Park HY, Choi YK, Seo YJ, Choi JH, et al. 2020. Metformin regulates astrocyte reactivity in Parkinson's disease and normal aging. Neuropharmacology 175: 108173. DOI |
20 | Ahn S, Jin TE, Chang DH, Rhee MS, Kim HJ, Lee SJ, et al. 2016. Agathobaculum butyriciproducens gen. nov. sp. nov., a strict anaerobic, butyrate-producing gut bacterium isolated from human faeces and reclassification of Eubacterium desmolans as Agathobaculum desmolans comb. nov. Int. J. Syst. Evol. Microbiol. 66: 3656-3661. DOI |
21 | Beaulieu JM, Del'guidice T, Sotnikova TD, Lemasson M, Gainetdinov RR. 2011. Beyond cAMP: The regulation of Akt and GSK3 by dopamine receptors. Front. Mol. Neurosci. 4: 38. DOI |
22 | Doble BW, Woodgett JR. 2003. GSK-3: tricks of the trade for a multi-tasking kinase. J. Cell Sci. 116: 1175-1186. DOI |
23 | Percario S, da Silva Barbosa A, Varela ELP, Gomes ARQ, Ferreira MES, de Nazare Araujo Moreira T, et al. 2020. Oxidative stress in Parkinson's disease: Potential benefits of antioxidant supplementation. Oxid. Med. Cell Longev. 2020: 2360872. |
24 | de Oliveira MR, Ferreira GC, Schuck PF. 2016. Protective effect of carnosic acid against paraquat-induced redox impairment and mitochondrial dysfunction in SH-SY5Y cells: Role for PI3K/Akt/Nrf2 pathway. Toxicol. In Vitro 32: 41-54. DOI |
25 | Quesada A, Lee BY, Micevych PE. 2008. PI3 kinase/Akt activation mediates estrogen and IGF-1 nigral DA neuronal neuroprotection against a unilateral rat model of Parkinson's disease. Dev. Neurobiol. 68: 632-644. DOI |
26 | Xie CL, Lin JY, Wang MH, Zhang Y, Zhang SF, Wang XJ, et al. 2016. Inhibition of Glycogen Synthase Kinase-3beta (GSK-3beta) as potent therapeutic strategy to ameliorates L-dopa-induced dyskinesia in 6-OHDA parkinsonian rats. Sci. Rep. 6: 23527. DOI |
27 | Sun J, Xu J, Ling Y, Wang F, Gong T, Yang C, et al. 2019. Fecal microbiota transplantation alleviated Alzheimer's disease-like pathogenesis in APP/PS1 transgenic mice. Transl. Psychiatry 9: 189. DOI |
28 | Krishnankutty A, Kimura T, Saito T, Aoyagi K, Asada A, Takahashi SI, et al. 2017. In vivo regulation of glycogen synthase kinase 3beta activity in neurons and brains. Sci. Rep. 7: 8602. DOI |
29 | Reiter RJ. 1998. Oxidative damage in the central nervous system: protection by melatonin. Prog. Neurobiol. 56: 359-384. DOI |
30 | Miao L, St Clair DK. 2009. Regulation of superoxide dismutase genes: implications in disease. Free Radic. Biol. Med. 47: 344-356. DOI |
31 | Liddelow SA, Guttenplan KA, Clarke LE, Bennett FC, Bohlen CJ, Schirmer L, et al. 2017. Neurotoxic reactive astrocytes are induced by activated microglia. Nature 541: 481-487. DOI |
32 | Haavik J, Toska K. 1998. Tyrosine hydroxylase and Parkinson's disease. Mol. Neurobiol. 16: 285-309. DOI |
33 | Franke TF, Kaplan DR, Cantley LC. 1997. PI3K: downstream AKTion blocks apoptosis. Cell 88: 435-437. DOI |
34 | Albin RL, Young AB, Penney JB. 1989. The functional anatomy of basal ganglia disorders. Trends Neurosci. 12: 366-375. DOI |
35 | Zhao Z, Ning J, Bao XQ, Shang M, Ma J, Li G, et al. 2021. Fecal microbiota transplantation protects rotenone-induced Parkinson's disease mice via suppressing inflammation mediated by the lipopolysaccharide-TLR4 signaling pathway through the microbiota-gut-brain axis. Microbiome 9: 226. DOI |
36 | Stevens B, Allen NJ, Vazquez LE, Howell GR, Christopherson KS, Nouri N, et al. 2007. The classical complement cascade mediates CNS synapse elimination. Cell 131: 1164-1178. DOI |
37 | Nicholson JK, Holmes E, Kinross J, Burcelin R, Gibson G, Jia W, et al. 2012. Host-gut microbiota metabolic interactions. Science 336: 1262-1267. DOI |
38 | Holscher HD. 2017. Dietary fiber and prebiotics and the gastrointestinal microbiota. Gut Microbes 8: 172-184. DOI |
39 | Claesson MJ, Cusack S, O'Sullivan O, Greene-Diniz R, de Weerd H, Flannery E, et al. 2011. Composition, variability, and temporal stability of the intestinal microbiota of the elderly. Proc. Natl. Acad. Sci. USA 108 Suppl 1: 4586-4591. DOI |
40 | Unger MM, Spiegel J, Dillmann KU, Grundmann D, Philippeit H, Burmann J, et al. 2016. Short chain fatty acids and gut microbiota differ between patients with Parkinson's disease and age-matched controls. Parkinsonism Relat. Disord. 32: 66-72. DOI |
41 | Martinez-Martin P, Rodriguez-Blazquez C, Kurtis MM, Chaudhuri KR, Group NV. 2011. The impact of non-motor symptoms on health-related quality of life of patients with Parkinson's disease. Mov. Disord. 26: 399-406. DOI |
42 | Kalia LV, Lang AE. 2015. Parkinson's disease. Lancet 386: 896-912. DOI |
43 | Rana AQ, Ahmed US, Chaudry ZM, Vasan S. 2015. Parkinson's disease: a review of non-motor symptoms. Expert Rev. Neurother. 15: 549-562. DOI |
44 | Schapira AHV, Chaudhuri KR, Jenner P. 2017. Non-motor features of Parkinson disease. Nat. Rev. Neurosci. 18: 435-450. DOI |
45 | Neufeld KM, Kang N, Bienenstock J, Foster JA. 2011. Reduced anxiety-like behavior and central neurochemical change in germ-free mice. Neurogastroenterol. Motil. 23: 255-264, e119. DOI |
46 | Rani L, Mondal AC. 2021. Unravelling the role of gut microbiota in Parkinson's disease progression: Pathogenic and therapeutic implications. Neurosci. Res. 168: 100-112. DOI |
47 | Xu R, Zhang Y, Chen S, Zeng Y, Fu X, Chen T, et al. 2022. The role of the probiotic Akkermansia muciniphila in brain functions: insights underpinning therapeutic potential. Crit. Rev. Microbiol. 11: 1-26. |
48 | Thiruvengadam M, Venkidasamy B, Subramanian U, Samynathan R, Ali Shariati M, Rebezov M, et al. 2021. Bioactive compounds in oxidative stress-mediated diseases: Targeting the NRF2/ARE signaling pathway and epigenetic regulation. Antioxidants (Basel). 10: 1859. DOI |
49 | Kramer BC, Mytilineou C. 2004. Alterations in the cellular distribution of bcl-2, bcl-x and bax in the adult rat substantia nigra following striatal 6-hydroxydopamine lesions. J. Neurocytol. 33: 213-223. DOI |
50 | Hayashi A, Sato T, Kamada N, Mikami Y, Matsuoka K, Hisamatsu T, et al. 2013. A single strain of Clostridium butyricum induces intestinal IL-10-producing macrophages to suppress acute experimental colitis in mice. Cell Host Microbe. 13: 711-722. DOI |
51 | Zhu Y, Zhang J, Zeng Y. 2012. Overview of tyrosine hydroxylase in Parkinson's disease. CNS Neurol. Disord. Drug Targets 11: 350-358. DOI |
52 | Yang L, Wang H, Liu L, Xie A. 2018. The role of insulin/IGF-1/PI3K/Akt/GSK3beta signaling in Parkinson's disease dementia. Front. Neurosci. 12: 73. DOI |
53 | Chung CY, Koprich JB, Endo S, Isacson O. 2007. An endogenous serine/threonine protein phosphatase inhibitor, G-substrate, reduces vulnerability in models of Parkinson's disease. J. Neurosci. 27: 8314-8323. DOI |
54 | Cersosimo MG, Raina GB, Pecci C, Pellene A, Calandra CR, Gutierrez C, et al. 2013. Gastrointestinal manifestations in Parkinson's disease: prevalence and occurrence before motor symptoms. J. Neurol. 260: 1332-1338. DOI |
55 | Hughes AJ, Daniel SE, Kilford L, Lees AJ. 1992. Accuracy of clinical diagnosis of idiopathic Parkinson's disease: a clinico-pathological study of 100 cases. J. Neurol. Neurosurg. Psychiatry 55: 181-184. DOI |
56 | Fasano A, Visanji NP, Liu LW, Lang AE, Pfeiffer RF. 2015. Gastrointestinal dysfunction in Parkinson's disease. Lancet Neurol. 14: 625-639. DOI |
57 | Santos SF, de Oliveira HL, Yamada ES, Neves BC, Pereira A, Jr. 2019. The gut and Parkinson's disease-A bidirectional pathway. Front. Neurol. 10: 574. DOI |
58 | Cryan JF, O'Riordan KJ, Cowan CSM, Sandhu KV, Bastiaanssen TFS, Boehme M, et al. 2019. The microbiota-gut-brain Axis. Physiol. Rev. 99: 1877-2013. DOI |
59 | Fulling C, Dinan TG, Cryan JF. 2019. Gut microbe to brain signaling: What happens in vagus. Neuron 101: 998-1002. DOI |
60 | Deumens R, Blokland A, Prickaerts J. 2002. Modeling Parkinson's disease in rats: an evaluation of 6-OHDA lesions of the nigrostriatal pathway. Exp. Neurol. 175: 303-317. DOI |
61 | Whitton PS. 2010. Neuroinflammation and the prospects for anti-inflammatory treatment of Parkinson's disease. Curr. Opin. Investig. Drugs. 11: 788-794. |
62 | Yan J, Fu Q, Cheng L, Zhai M, Wu W, Huang L, et al. 2014. Inflammatory response in Parkinson's disease (Review). Mol. Med. Rep. 10: 2223-2233. DOI |
63 | Troncoso-Escudero P, Parra A, Nassif M, Vidal RL. 2018. Outside in: Unraveling the role of neuroinflammation in the progression of Parkinson's disease. Front. Neurol. 9: 860. DOI |
64 | Gagne JJ, Power MC. 2010. Anti-inflammatory drugs and risk of Parkinson disease: a meta-analysis. Neurology 74: 995-1002. DOI |
65 | Park HY, Ryu YK, Kim YH, Park TS, Go J, Hwang JH, et al. 2016. Gadd45beta ameliorates L-DOPA-induced dyskinesia in a Parkinson's disease mouse model. Neurobiol. Dis. 89: 169-179. DOI |
66 | Oh YJ, Wong SC, Moffat M, O'Malley KL. 1995. Overexpression of Bcl-2 attenuates MPP+, but not 6-ODHA, induced cell death in a dopaminergic neuronal cell line. Neurobiol. Dis. 2: 157-167. DOI |
67 | Chen G, Bower KA, Ma C, Fang S, Thiele CJ, Luo J. 2004. Glycogen synthase kinase 3beta (GSK3beta) mediates 6-hydroxydopamine-induced neuronal death. FASEB J. 18: 1162-1164. DOI |
68 | Jope RS, Johnson GV. 2004. The glamour and gloom of glycogen synthase kinase-3. Trends Biochem. Sci. 29: 95-102. DOI |
69 | Aleyasin H, Rousseaux MW, Marcogliese PC, Hewitt SJ, Irrcher I, Joselin AP, et al. 2010. DJ-1 protects the nigrostriatal axis from the neurotoxin MPTP by modulation of the AKT pathway. Proc. Natl. Acad. Sci. USA 107: 3186-3191. DOI |
70 | Li L, Dong H, Song E, Xu X, Liu L, Song Y. 2014. Nrf2/ARE pathway activation, HO-1 and NQO1 induction by polychlorinated biphenyl quinone is associated with reactive oxygen species and PI3K/AKT signaling. Chem. Biol. Interact. 209: 56-67. DOI |
71 | Liddelow SA, Barres BA. 2017. Reactive astrocytes: Production, function, and therapeutic potential. Immunity 46: 957-967. DOI |
72 | Gorshkov K, Aguisanda F, Thorne N, Zheng W. 2018. Astrocytes as targets for drug discovery. Drug Discov. Today 23: 673-680. DOI |
73 | Aaseth J, Dusek P, Roos PM. 2018. Prevention of progression in Parkinson's disease. Biometals 31: 737-747. DOI |
74 | Liu J, Wang F, Liu S, Du J, Hu X, Xiong J, et al. 2017. Sodium butyrate exerts protective effect against Parkinson's disease in mice via stimulation of glucagon like peptide-1. J. Neurol. Sci. 381: 176-181. |
75 | Braak H, Rub U, Gai WP, Del Tredici K. 2003. Idiopathic Parkinson's disease: possible routes by which vulnerable neuronal types may be subject to neuroinvasion by an unknown pathogen. J. Neural. Transm (Vienna) 110: 517-536. DOI |
76 | Kawase T, Nagasawa M, Ikeda H, Yasuo S, Koga Y, Furuse M. 2017. Gut microbiota of mice putatively modifies amino acid metabolism in the host brain. Br. J. Nutr. 117: 775-783. DOI |
77 | Cantu-Jungles TM, Rasmussen HE, Hamaker BR. 2019. Potential of prebiotic butyrogenic fibers in Parkinson's disease. Front. Neurol. 10: 663. DOI |
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