Bacterial Butyrate in Parkinson's Disease Is Linked to Epigenetic Changes and Depressive Symptoms

Background The gut microbiome and its metabolites can impact brain health and are altered in Parkinson's disease (PD) patients. It has been recently demonstrated that PD patients have reduced fecal levels of the potent epigenetic modulator butyrate and its bacterial producers. Objectives Here,...

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Published inMovement disorders Vol. 37; no. 8; pp. 1644 - 1653
Main Authors Xie, Aoji, Ensink, Elizabeth, Li, Peipei, Gordevičius, Juozas, Marshall, Lee L., George, Sonia, Pospisilik, John Andrew, Aho, Velma T.E., Houser, Madelyn C., Pereira, Pedro A.B., Rudi, Knut, Paulin, Lars, Tansey, Malú G., Auvinen, Petri, Brundin, Patrik, Brundin, Lena, Labrie, Viviane, Scheperjans, Filip
Format Journal Article
LanguageEnglish
Published Hoboken, USA John Wiley & Sons, Inc 01.08.2022
Wiley Subscription Services, Inc
Subjects
Bisulfite
Butyrates
Depression - genetics
Digestive system
DNA methylation
Epidemiology
Epigenesis, Genetic
Epigenetics
Feces
Gastrointestinal Microbiome - genetics
Gastrointestinal tract
Genomes
Gut-brain axis
Humans
Intestinal microflora
Leukocytes (neutrophilic)
Mental depression
Mental disorders
Metabolites
microbiome
Microbiomes
Microbiota
Movement disorders
Neurodegenerative diseases
Neurons
Parkinson Disease - complications
Parkinson Disease - genetics
Parkinson Disease - microbiology
Parkinson's disease
Patients
Prefrontal cortex
DNA methylation
Parkinson's disease
gut brain axis
microbiome
epigenetics
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Abstract Background The gut microbiome and its metabolites can impact brain health and are altered in Parkinson's disease (PD) patients. It has been recently demonstrated that PD patients have reduced fecal levels of the potent epigenetic modulator butyrate and its bacterial producers. Objectives Here, we investigate whether the changes in the gut microbiome and associated metabolites are related to PD symptoms and epigenetic markers in leucocytes and neurons. Methods Stool, whole blood samples, and clinical data were collected from 55 PD patients and 55 controls. We performed DNA methylation analysis on whole blood samples and analyzed the results in relation to fecal short‐chain fatty acid concentrations and microbiota composition. In another cohort, prefrontal cortex neurons were isolated from control and PD brains. We identified genome‐wide DNA methylation by targeted bisulfite sequencing. Results We show that lower fecal butyrate and reduced counts of genera Roseburia, Romboutsia, and Prevotella are related to depressive symptoms in PD patients. Genes containing butyrate‐associated methylation sites include PD risk genes and significantly overlap with sites epigenetically altered in PD blood leucocytes, predominantly neutrophils, and in brain neurons, relative to controls. Moreover, butyrate‐associated methylated‐DNA regions in PD overlap with those altered in gastrointestinal (GI), autoimmune, and psychiatric diseases. Conclusions Decreased levels of bacterially produced butyrate are related to epigenetic changes in leucocytes and neurons from PD patients and to the severity of their depressive symptoms. PD shares common butyrate‐dependent epigenetic changes with certain GI and psychiatric disorders, which could be relevant for their epidemiological relation. © 2022 The Authors. Movement Disorders published by Wiley Periodicals LLC on behalf of International Parkinson and Movement Disorder Society
AbstractList The gut microbiome and its metabolites can impact brain health and are altered in Parkinson's disease (PD) patients. It has been recently demonstrated that PD patients have reduced fecal levels of the potent epigenetic modulator butyrate and its bacterial producers.BACKGROUNDThe gut microbiome and its metabolites can impact brain health and are altered in Parkinson's disease (PD) patients. It has been recently demonstrated that PD patients have reduced fecal levels of the potent epigenetic modulator butyrate and its bacterial producers.Here, we investigate whether the changes in the gut microbiome and associated metabolites are related to PD symptoms and epigenetic markers in leucocytes and neurons.OBJECTIVESHere, we investigate whether the changes in the gut microbiome and associated metabolites are related to PD symptoms and epigenetic markers in leucocytes and neurons.Stool, whole blood samples, and clinical data were collected from 55 PD patients and 55 controls. We performed DNA methylation analysis on whole blood samples and analyzed the results in relation to fecal short-chain fatty acid concentrations and microbiota composition. In another cohort, prefrontal cortex neurons were isolated from control and PD brains. We identified genome-wide DNA methylation by targeted bisulfite sequencing.METHODSStool, whole blood samples, and clinical data were collected from 55 PD patients and 55 controls. We performed DNA methylation analysis on whole blood samples and analyzed the results in relation to fecal short-chain fatty acid concentrations and microbiota composition. In another cohort, prefrontal cortex neurons were isolated from control and PD brains. We identified genome-wide DNA methylation by targeted bisulfite sequencing.We show that lower fecal butyrate and reduced counts of genera Roseburia, Romboutsia, and Prevotella are related to depressive symptoms in PD patients. Genes containing butyrate-associated methylation sites include PD risk genes and significantly overlap with sites epigenetically altered in PD blood leucocytes, predominantly neutrophils, and in brain neurons, relative to controls. Moreover, butyrate-associated methylated-DNA regions in PD overlap with those altered in gastrointestinal (GI), autoimmune, and psychiatric diseases.RESULTSWe show that lower fecal butyrate and reduced counts of genera Roseburia, Romboutsia, and Prevotella are related to depressive symptoms in PD patients. Genes containing butyrate-associated methylation sites include PD risk genes and significantly overlap with sites epigenetically altered in PD blood leucocytes, predominantly neutrophils, and in brain neurons, relative to controls. Moreover, butyrate-associated methylated-DNA regions in PD overlap with those altered in gastrointestinal (GI), autoimmune, and psychiatric diseases.Decreased levels of bacterially produced butyrate are related to epigenetic changes in leucocytes and neurons from PD patients and to the severity of their depressive symptoms. PD shares common butyrate-dependent epigenetic changes with certain GI and psychiatric disorders, which could be relevant for their epidemiological relation. © 2022 The Authors. Movement Disorders published by Wiley Periodicals LLC on behalf of International Parkinson and Movement Disorder Society.CONCLUSIONSDecreased levels of bacterially produced butyrate are related to epigenetic changes in leucocytes and neurons from PD patients and to the severity of their depressive symptoms. PD shares common butyrate-dependent epigenetic changes with certain GI and psychiatric disorders, which could be relevant for their epidemiological relation. © 2022 The Authors. Movement Disorders published by Wiley Periodicals LLC on behalf of International Parkinson and Movement Disorder Society.
The gut microbiome and its metabolites can impact brain health and are altered in Parkinson's disease (PD) patients. It has been recently demonstrated that PD patients have reduced fecal levels of the potent epigenetic modulator butyrate and its bacterial producers. Here, we investigate whether the changes in the gut microbiome and associated metabolites are related to PD symptoms and epigenetic markers in leucocytes and neurons. Stool, whole blood samples, and clinical data were collected from 55 PD patients and 55 controls. We performed DNA methylation analysis on whole blood samples and analyzed the results in relation to fecal short-chain fatty acid concentrations and microbiota composition. In another cohort, prefrontal cortex neurons were isolated from control and PD brains. We identified genome-wide DNA methylation by targeted bisulfite sequencing. We show that lower fecal butyrate and reduced counts of genera Roseburia, Romboutsia, and Prevotella are related to depressive symptoms in PD patients. Genes containing butyrate-associated methylation sites include PD risk genes and significantly overlap with sites epigenetically altered in PD blood leucocytes, predominantly neutrophils, and in brain neurons, relative to controls. Moreover, butyrate-associated methylated-DNA regions in PD overlap with those altered in gastrointestinal (GI), autoimmune, and psychiatric diseases. Decreased levels of bacterially produced butyrate are related to epigenetic changes in leucocytes and neurons from PD patients and to the severity of their depressive symptoms. PD shares common butyrate-dependent epigenetic changes with certain GI and psychiatric disorders, which could be relevant for their epidemiological relation. © 2022 The Authors. Movement Disorders published by Wiley Periodicals LLC on behalf of International Parkinson and Movement Disorder Society.
BackgroundThe gut microbiome and its metabolites can impact brain health and are altered in Parkinson's disease (PD) patients. It has been recently demonstrated that PD patients have reduced fecal levels of the potent epigenetic modulator butyrate and its bacterial producers.ObjectivesHere, we investigate whether the changes in the gut microbiome and associated metabolites are related to PD symptoms and epigenetic markers in leucocytes and neurons.MethodsStool, whole blood samples, and clinical data were collected from 55 PD patients and 55 controls. We performed DNA methylation analysis on whole blood samples and analyzed the results in relation to fecal short‐chain fatty acid concentrations and microbiota composition. In another cohort, prefrontal cortex neurons were isolated from control and PD brains. We identified genome‐wide DNA methylation by targeted bisulfite sequencing.ResultsWe show that lower fecal butyrate and reduced counts of genera Roseburia, Romboutsia, and Prevotella are related to depressive symptoms in PD patients. Genes containing butyrate‐associated methylation sites include PD risk genes and significantly overlap with sites epigenetically altered in PD blood leucocytes, predominantly neutrophils, and in brain neurons, relative to controls. Moreover, butyrate‐associated methylated‐DNA regions in PD overlap with those altered in gastrointestinal (GI), autoimmune, and psychiatric diseases.ConclusionsDecreased levels of bacterially produced butyrate are related to epigenetic changes in leucocytes and neurons from PD patients and to the severity of their depressive symptoms. PD shares common butyrate‐dependent epigenetic changes with certain GI and psychiatric disorders, which could be relevant for their epidemiological relation. © 2022 The Authors. Movement Disorders published by Wiley Periodicals LLC on behalf of International Parkinson and Movement Disorder Society
Background The gut microbiome and its metabolites can impact brain health and are altered in Parkinson's disease (PD) patients. It has been recently demonstrated that PD patients have reduced fecal levels of the potent epigenetic modulator butyrate and its bacterial producers. Objectives Here, we investigate whether the changes in the gut microbiome and associated metabolites are related to PD symptoms and epigenetic markers in leucocytes and neurons. Methods Stool, whole blood samples, and clinical data were collected from 55 PD patients and 55 controls. We performed DNA methylation analysis on whole blood samples and analyzed the results in relation to fecal short‐chain fatty acid concentrations and microbiota composition. In another cohort, prefrontal cortex neurons were isolated from control and PD brains. We identified genome‐wide DNA methylation by targeted bisulfite sequencing. Results We show that lower fecal butyrate and reduced counts of genera Roseburia, Romboutsia, and Prevotella are related to depressive symptoms in PD patients. Genes containing butyrate‐associated methylation sites include PD risk genes and significantly overlap with sites epigenetically altered in PD blood leucocytes, predominantly neutrophils, and in brain neurons, relative to controls. Moreover, butyrate‐associated methylated‐DNA regions in PD overlap with those altered in gastrointestinal (GI), autoimmune, and psychiatric diseases. Conclusions Decreased levels of bacterially produced butyrate are related to epigenetic changes in leucocytes and neurons from PD patients and to the severity of their depressive symptoms. PD shares common butyrate‐dependent epigenetic changes with certain GI and psychiatric disorders, which could be relevant for their epidemiological relation. © 2022 The Authors. Movement Disorders published by Wiley Periodicals LLC on behalf of International Parkinson and Movement Disorder Society
Author Marshall, Lee L.
Scheperjans, Filip
Auvinen, Petri
Paulin, Lars
Labrie, Viviane
George, Sonia
Ensink, Elizabeth
Gordevičius, Juozas
Aho, Velma T.E.
Tansey, Malú G.
Li, Peipei
Pereira, Pedro A.B.
Brundin, Patrik
Rudi, Knut
Brundin, Lena
Xie, Aoji
Houser, Madelyn C.
Pospisilik, John Andrew
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/35723531$$D View this record in MEDLINE/PubMed
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ContentType Journal Article
Copyright 2022 The Authors. published by Wiley Periodicals LLC on behalf of International Parkinson and Movement Disorder Society
2022 The Authors. Movement Disorders published by Wiley Periodicals LLC on behalf of International Parkinson and Movement Disorder Society.
2022. This article is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
Copyright_xml – notice: 2022 The Authors. published by Wiley Periodicals LLC on behalf of International Parkinson and Movement Disorder Society
– notice: 2022 The Authors. Movement Disorders published by Wiley Periodicals LLC on behalf of International Parkinson and Movement Disorder Society.
– notice: 2022. This article is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
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Issue 8
Keywords DNA methylation
Parkinson's disease
gut brain axis
microbiome
epigenetics
Language English
License Attribution
2022 The Authors. Movement Disorders published by Wiley Periodicals LLC on behalf of International Parkinson and Movement Disorder Society.
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MergedId FETCHMERGED-LOGICAL-c3888-2bc3048b1bb3ffe832c986a865f0768d8f9af8787b4cc2a491c02b6b416cc13b3
Notes Funding agencies
This work was supported by a Farmer Family Foundation grant award and a Gibby & Friends versus Parky Award to P.B., with L.B., J.A.P., and V.L. F.S. received funding from The Michael J. Fox Foundation for Parkinson's Research, the Academy of Finland (295724 and 310835), the Hospital District of Helsinki and Uusimaa (UAK1014004, UAK1014005, and TYH2018224), the Finnish Medical Foundation, and the Finnish Parkinson Foundation.
Viviane Labrie and Filip Scheperjans should be considered joint senior authors.
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Snippet Background The gut microbiome and its metabolites can impact brain health and are altered in Parkinson's disease (PD) patients. It has been recently...
The gut microbiome and its metabolites can impact brain health and are altered in Parkinson's disease (PD) patients. It has been recently demonstrated that PD...
BackgroundThe gut microbiome and its metabolites can impact brain health and are altered in Parkinson's disease (PD) patients. It has been recently...
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SubjectTerms Bisulfite
Butyrates
Depression - genetics
Digestive system
DNA methylation
Epidemiology
Epigenesis, Genetic
Epigenetics
Feces
Gastrointestinal Microbiome - genetics
Gastrointestinal tract
Genomes
Gut-brain axis
Humans
Intestinal microflora
Leukocytes (neutrophilic)
Mental depression
Mental disorders
Metabolites
microbiome
Microbiomes
Microbiota
Movement disorders
Neurodegenerative diseases
Neurons
Parkinson Disease - complications
Parkinson Disease - genetics
Parkinson Disease - microbiology
Parkinson's disease
Patients
Prefrontal cortex
Title Bacterial Butyrate in Parkinson's Disease Is Linked to Epigenetic Changes and Depressive Symptoms
URI https://onlinelibrary.wiley.com/doi/abs/10.1002%2Fmds.29128
https://www.ncbi.nlm.nih.gov/pubmed/35723531
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https://www.proquest.com/docview/2678739254
Volume 37
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