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Translational Neurodegeneration
Published in: Translational Neurodegeneration 1/2019

Open Access 01-12-2019 | Chronic Inflammatory Bowel Disease | Review

Microbiome changes: an indicator of Parkinson’s disease?

Authors: Caroline Haikal, Qian-Qian Chen, Jia-Yi Li

Published in: Translational Neurodegeneration | Issue 1/2019

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Abstract

Parkinson’s disease is characterized by dopaminergic neuron loss and intracellular inclusions composed mainly of alpha synuclein (α-syn), but the mechanism of pathogenesis is still obscure. In recent years, more attention has been given to the gut as a key player in the initiation and progression of PD pathology. Several studies characterizing changes in the microbiome, particularly the gut microbiome, have been conducted. Although many studies found a decrease in the bacterial family Prevotellaceae and in butyrate-producing bacterial genera such as Roseburia and Faecalibacteria, and an increase in the genera Akkermansia many of the studies reported contradictory findings. In this review, we highlight the findings from the different studies and reflect on the future of microbiome studies in PD research.
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Literature
1.
Braak H, Rub U, Gai WP, Del Tredici K. Idiopathic Parkinson's disease: possible routes by which vulnerable neuronal types may be subject to neuroinvasion by an unknown pathogen. J Neural Transm (Vienna). 2003;110:517–36.
2.
Hawkes CH, Del Tredici K, Braak H. Parkinson's disease: a dual-hit hypothesis. Neuropathol Appl Neurobiol. 2007;33:599–614.PubMed
3.
Holmqvist S, et al. Direct evidence of Parkinson pathology spread from the gastrointestinal tract to the brain in rats. Acta Neuropathol. 2014;128:805–20.PubMed
4.
Kim S, et al. Transneuronal propagation of pathologic alpha-Synuclein from the gut to the brain models Parkinson's disease. Neuron. 2019;103:627–41.PubMed
5.
Svensson E, et al. Vagotomy and subsequent risk of Parkinson's disease. Ann Neurol. 2015;78:522–9.PubMed
6.
Klingelhoefer L, Reichmann H. Pathogenesis of Parkinson disease--the gut-brain axis and environmental factors. Nat Rev Neurol. 2015;11:625–36.PubMed
7.
8.
9.
Villumsen M, Aznar S, Pakkenberg B, Jess T, Brudek T. Inflammatory bowel disease increases the risk of Parkinson's disease: a Danish nationwide cohort study 1977-2014. Gut. 2019;68:18–24.PubMed
10.
Weimers P, et al. Inflammatory bowel disease and Parkinson's disease: a Nationwide Swedish cohort study. Inflamm Bowel Dis. 2019;25:111–23.PubMed
11.
Zhu F, et al. The risk of Parkinson's disease in inflammatory bowel disease: a systematic review and meta-analysis. Dig Liver Dis. 2019;51:38–42.PubMed
12.
Matheoud D, et al. Intestinal infection triggers Parkinson's disease-like symptoms in Pink1(−/−) mice. Nature. 2019;571:565–9.PubMed
13.
Shannon KM, Keshavarzian A, Dodiya HB, Jakate S, Kordower JH. Is alpha-synuclein in the colon a biomarker for premotor Parkinson's disease? Evidence from 3 cases. Mov Disord. 2012;27:716–9.PubMed
14.
Bhattacharyya D, et al. Lipopolysaccharide from gut microbiota modulates alpha-Synuclein aggregation and alters its biological function. ACS Chem Neurosci. 2019;10:2229–36.PubMed
15.
Kim C, et al. Exposure to bacterial endotoxin generates a distinct strain of alpha-synuclein fibril. Sci Rep. 2016;6:30891.PubMedPubMedCentral
16.
Chen SG, et al. Exposure to the functional bacterial amyloid protein Curli enhances alpha-Synuclein aggregation in aged Fischer 344 rats and Caenorhabditis elegans. Sci Rep. 2016;6:34477.PubMedPubMedCentral
17.
Chorell E, et al. Bacterial chaperones CsgE and CsgC differentially modulate human alpha-Synuclein amyloid formation via transient contacts. PLoS One. 2015;10:e0140194.PubMedPubMedCentral
18.
Evans ML, et al. The bacterial curli system possesses a potent and selective inhibitor of amyloid formation. Mol Cell. 2015;57:445–55.PubMedPubMedCentral
19.
Sampson TR, et al. Gut Microbiota Regulate Motor Deficits and Neuroinflammation in a Model of Parkinson's Disease. Cell. 2016;167:1469–1480 e1412.PubMedPubMedCentral
20.
Tamburrino A, et al. Cyclosporin promotes neurorestoration and cell replacement therapy in pre-clinical models of Parkinson's disease. Acta Neuropathol Commun. 2015;3:84.PubMedPubMedCentral
21.
Brochard V, et al. Infiltration of CD4+ lymphocytes into the brain contributes to neurodegeneration in a mouse model of Parkinson disease. J Clin Invest. 2009;119:182–92.PubMed
22.
Gilbert JA, et al. Current understanding of the human microbiome. Nat Med. 2018;24:392–400.PubMed
23.
Dunn AB, Jordan S, Baker BJ, Carlson NS. The maternal infant microbiome: considerations for labor and birth. MCN Am J Matern Child Nurs. 2017;42:318–25.PubMedPubMedCentral
24.
Goedert JJ, Hua X, Yu G, Shi J. Diversity and composition of the adult fecal microbiome associated with history of cesarean birth or appendectomy: analysis of the American gut project. EBioMedicine. 2014;1:167–72.PubMedPubMedCentral
25.
Adlerberth I, et al. Reduced enterobacterial and increased staphylococcal colonization of the infantile bowel: an effect of hygienic lifestyle? Pediatr Res. 2006;59:96–101.PubMed
26.
Gronlund MM, Lehtonen OP, Eerola E, Kero P. Fecal microflora in healthy infants born by different methods of delivery: permanent changes in intestinal flora after cesarean delivery. J Pediatr Gastroenterol Nutr. 1999;28:19–25.PubMed
27.
Dominguez-Bello MG, et al. Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc Natl Acad Sci U S A. 2010;107:11971–5.PubMedPubMedCentral
28.
29.
Dethlefsen L, Relman DA. Incomplete recovery and individualized responses of the human distal gut microbiota to repeated antibiotic perturbation. Proc Natl Acad Sci U S A. 2011;108(Suppl 1):4554–61.PubMed
30.
31.
Ward NL, et al. Antibiotic treatment induces long-lasting changes in the fecal microbiota that protect against colitis. Inflamm Bowel Dis. 2016;22:2328–40.PubMedPubMedCentral
32.
Antharam VC, et al. Intestinal dysbiosis and depletion of butyrogenic bacteria in Clostridium difficile infection and nosocomial diarrhea. J Clin Microbiol. 2013;51:2884–92.PubMedPubMedCentral
33.
An R, et al. Age-dependent changes in GI physiology and microbiota: time to reconsider? Gut. 2018;67:2213–22.PubMed
34.
Odamaki T, et al. Age-related changes in gut microbiota composition from newborn to centenarian: a cross-sectional study. BMC Microbiol. 2016;16:90.PubMedPubMedCentral
35.
36.
Vandeputte D, et al. Stool consistency is strongly associated with gut microbiota richness and composition, enterotypes and bacterial growth rates. Gut. 2016;65:57–62.PubMed
37.
Vandeputte D, et al. Quantitative microbiome profiling links gut community variation to microbial load. Nature. 2017;551:507–11.PubMed
38.
Roager HM, et al. Colonic transit time is related to bacterial metabolism and mucosal turnover in the gut. Nat Microbiol. 2016;1:16093.PubMed
39.
Keshavarzian A, et al. Colonic bacterial composition in Parkinson's disease. Mov Disord. 2015;30:1351–60.PubMed
40.
Heintz-Buschart A, et al. The nasal and gut microbiome in Parkinson's disease and idiopathic rapid eye movement sleep behavior disorder. Mov Disord. 2018;33:88–98.PubMed
41.
Pereira PAB, et al. Oral and nasal microbiota in Parkinson's disease. Parkinsonism Relat Disord. 2017;38:61–7.PubMed
42.
Qian Y, et al. Alteration of the fecal microbiota in Chinese patients with Parkinson's disease. Brain Behav Immun. 2018;70:194–202.PubMed
43.
Lin CH, et al. Altered gut microbiota and inflammatory cytokine responses in patients with Parkinson's disease. J Neuroinflammation. 2019;16:129.PubMedPubMedCentral
44.
Bedarf JR, et al. Functional implications of microbial and viral gut metagenome changes in early stage L-DOPA-naive Parkinson's disease patients. Genome Med. 2017;9:39.PubMedPubMedCentral
45.
Petrov VA, et al. Analysis of gut microbiota in patients with Parkinson's disease. Bull Exp Biol Med. 2017;162:734–7.PubMed
46.
Scheperjans F, et al. Gut microbiota are related to Parkinson's disease and clinical phenotype. Mov Disord. 2015;30:350–8.PubMed
47.
Hopfner F, et al. Gut microbiota in Parkinson disease in a northern German cohort. Brain Res. 1667;2017:41–5.
48.
Hasegawa S, et al. Intestinal Dysbiosis and lowered serum lipopolysaccharide-binding protein in Parkinson's disease. PLoS One. 2015;10:e0142164.PubMedPubMedCentral
49.
Li W, et al. Structural changes of gut microbiota in Parkinson's disease and its correlation with clinical features. Sci China Life Sci. 2017;60:1223–33.PubMed
50.
Hill-Burns EM, et al. Parkinson's disease and Parkinson's disease medications have distinct signatures of the gut microbiome. Mov Disord. 2017;32:739–49.PubMedPubMedCentral
51.
Unger MM, et al. Short chain fatty acids and gut microbiota differ between patients with Parkinson's disease and age-matched controls. Parkinsonism Relat Disord. 2016;32:66–72.PubMed
52.
Li F, et al. Alteration of the fecal microbiota in north-eastern Han Chinese population with sporadic Parkinson's disease. Neurosci Lett. 2019;707:134297.PubMed
53.
Pietrucci D, et al. Dysbiosis of gut microbiota in a selected population of Parkinson's patients. Parkinsonism Relat Disord. 2019;65:124–30.PubMed
54.
Lin A, et al. Gut microbiota in patients with Parkinson's disease in southern China. Parkinsonism Relat Disord. 2018;53:82–8.PubMed
55.
Aho VTE, et al. Gut microbiota in Parkinson's disease: temporal stability and relations to disease progression. EBioMedicine. 2019;44:691–707.PubMedPubMedCentral
56.
Palm NW, et al. Immunoglobulin a coating identifies colitogenic bacteria in inflammatory bowel disease. Cell. 2014;158:1000–10.PubMedPubMedCentral
57.
Minato T, et al. Progression of Parkinson's disease is associated with gut dysbiosis: two-year follow-up study. PLoS One. 2017;12:e0187307.PubMedPubMedCentral
58.
Tan AH, et al. Altered gut microbiome and metabolome in patients with multiple system atrophy. Mov Disord. 2018;33:174–6.PubMed
59.
Yang X, Qian Y, Xu S, Song Y, Xiao Q. Longitudinal analysis of fecal microbiome and pathologic processes in a rotenone induced mice model of Parkinson's disease. Front Aging Neurosci. 2017;9:441.PubMed
60.
Mihaila D, et al. The oral microbiome of early stage Parkinson's disease and its relationship with functional measures of motor and non-motor function. PLoS One. 2019;14:e0218252.PubMedPubMedCentral
61.
Perez-Pardo P, et al. Gut bacterial composition in a mouse model of Parkinson's disease. Benefic Microbes. 2018;9:799–814.
62.
Greer RL, et al. Akkermansia muciniphila mediates negative effects of IFNgamma on glucose metabolism. Nat Commun. 2016;7:13329.PubMedPubMedCentral
63.
Demirci M, et al. Reduced Akkermansia muciniphila and Faecalibacterium prausnitzii levels in the gut microbiota of children with allergic asthma. Allergol Immunopathol (Madr). 2019;47:365–71.
64.
Ansaldo E, et al. Akkermansia muciniphila induces intestinal adaptive immune responses during homeostasis. Science. 2019;364:1179–84.PubMedPubMedCentral
65.
Poretsky R, Rodriguez RL, Luo C, Tsementzi D, Konstantinidis KT. Strengths and limitations of 16S rRNA gene amplicon sequencing in revealing temporal microbial community dynamics. PLoS One. 2014;9:e93827.PubMedPubMedCentral
66.
Jo JH, Kennedy EA, Kong HH. Research techniques made simple: bacterial 16S ribosomal RNA gene sequencing in cutaneous research. J Invest Dermatol. 2016;136:e23–7.PubMedPubMedCentral
67.
Bauer MA, Kainz K, Carmona-Gutierrez D, Madeo F. Microbial wars: competition in ecological niches and within the microbiome. Microb Cell. 2018;5:215–9.PubMedPubMedCentral
68.
Donaldson GP, Lee SM, Mazmanian SK. Gut biogeography of the bacterial microbiota. Nat Rev Microbiol. 2016;14:20–32.PubMed
69.
Blander JM, Longman RS, Iliev ID, Sonnenberg GF, Artis D. Regulation of inflammation by microbiota interactions with the host. Nat Immunol. 2017;18:851–60.PubMedPubMedCentral
70.
Nell S, Suerbaum S, Josenhans C. The impact of the microbiota on the pathogenesis of IBD: lessons from mouse infection models. Nat Rev Microbiol. 2010;8:564–77.PubMed
71.
Zuo T, Ng SC. The gut microbiota in the pathogenesis and therapeutics of inflammatory bowel disease. Front Microbiol. 2018;9:2247.PubMedPubMedCentral
72.
Qiang Y, et al. Butyrate and retinoic acid imprint mucosal-like dendritic cell development synergistically from bone marrow cells. Clin Exp Immunol. 2017;189:290–7.PubMedPubMedCentral
73.
Sun MF, et al. Neuroprotective effects of fecal microbiota transplantation on MPTP-induced Parkinson's disease mice: gut microbiota, glial reaction and TLR4/TNF-alpha signaling pathway. Brain Behav Immun. 2018;70:48–60.PubMed
74.
75.
Hewel C, et al. Common miRNA patterns of Alzheimer's disease and Parkinson's disease and their putative impact on commensal gut microbiota. Front Neurosci. 2019;13:113.PubMedPubMedCentral
76.
Raisch J, Darfeuille-Michaud A, Nguyen HT. Role of microRNAs in the immune system, inflammation and cancer. World J Gastroenterol. 2013;19:2985–96.PubMedPubMedCentral
77.
Hibbing ME, Fuqua C, Parsek MR, Peterson SB. Bacterial competition: surviving and thriving in the microbial jungle. Nat Rev Microbiol. 2010;8:15–25.PubMedPubMedCentral
78.
Morales DK, Hogan DA. Candida albicans interactions with bacteria in the context of human health and disease. PLoS Pathog. 2010;6:e1000886.PubMedPubMedCentral
79.
Shirtliff ME, Peters BM, Jabra-Rizk MA. Cross-kingdom interactions: Candida albicans and bacteria. FEMS Microbiol Lett. 2009;299:1–8.PubMedPubMedCentral
80.
Hsu BB, et al. Dynamic Modulation of the Gut Microbiota and Metabolome by Bacteriophages in a Mouse Model. Cell Host Microbe. 2019;25:803–814 e805.PubMedPubMedCentral
81.
Knights D, Parfrey LW, Zaneveld J, Lozupone C, Knight R. Human-associated microbial signatures: examining their predictive value. Cell Host Microbe. 2011;10:292–6.PubMed
82.
Walters WA, Xu Z, Knight R. Meta-analyses of human gut microbes associated with obesity and IBD. FEBS Lett. 2014;588:4223–33.PubMedPubMedCentral
Metadata
Title
Microbiome changes: an indicator of Parkinson’s disease?
Authors
Caroline Haikal
Qian-Qian Chen
Jia-Yi Li
Publication date
01-12-2019
Publisher
BioMed Central
Published in
Translational Neurodegeneration / Issue 1/2019
Electronic ISSN: 2047-9158
DOI
https://doi.org/10.1186/s40035-019-0175-7

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