Butyricicoccus pullicaecorum in inflammatory bowel disease
Objective Many species within the phylum Firmicutes are thought to exert anti-inflammatory effects. We quantified bacteria belonging to the genus Butyricicoccus in stools of patients with ulcerative colitis (UC) and Crohn's disease (CD). We evaluated the effect of Butyricicoccus pullicaecorum i...
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Veröffentlicht in: | Gut 2013-12, Vol.62 (12), p.1745-1752 |
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creator | Eeckhaut, Venessa Machiels, Kathleen Perrier, Clémentine Romero, Carlos Maes, Sofie Flahou, Bram Steppe, Marjan Haesebrouck, Freddy Sas, Benedikt Ducatelle, Richard Vermeire, Severine Van Immerseel, Filip |
description | Objective Many species within the phylum Firmicutes are thought to exert anti-inflammatory effects. We quantified bacteria belonging to the genus Butyricicoccus in stools of patients with ulcerative colitis (UC) and Crohn's disease (CD). We evaluated the effect of Butyricicoccus pullicaecorum in a rat colitis model and analysed the ability to prevent cytokine-induced increases in epithelial permeability. Design A genus-specific quantitative PCR was used for quantification of Butyricicoccus in stools from patients with UC or CD and healthy subjects. The effect of B pullicaecorum on trinitrobenzenesulfonic (TNBS)-induced colitis was assessed and the effect of B pullicaecorum culture supernatant on epithelial barrier function was investigated in vitro. Results The average number of Butyricicoccus in stools from patients with UC and CD in active (UC: 8.61 log10/g stool; CD: 6.58 log10/g stool) and remission phase (UC: 8.69 log10/g stool; CD: 8.38 log10/g stool) was significantly lower compared with healthy subjects (9.32 log10/g stool) and correlated with disease activity in CD. Oral administration of B pullicaecorum resulted in a significant protective effect based on macroscopic and histological criteria and decreased intestinal myeloperoxidase (MPO), tumour necrosis factor α (TNFα) and interleukin (IL)-12 levels. Supernatant of B pullicaecorum prevented the loss of transepithelial resistance (TER) and the increase in IL-8 secretion induced by TNFα and interferon γ (IFN gamma) in a Caco-2 cell model. Conclusions Patients with inflammatory bowel disease have lower numbers of Butyricicoccus bacteria in their stools. Administration of B pullicaecorum attenuates TNBS-induced colitis in rats and supernatant of B pullicaecorum cultures strengthens the epithelial barrier function by increasing the TER. |
doi_str_mv | 10.1136/gutjnl-2012-303611 |
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We quantified bacteria belonging to the genus Butyricicoccus in stools of patients with ulcerative colitis (UC) and Crohn's disease (CD). We evaluated the effect of Butyricicoccus pullicaecorum in a rat colitis model and analysed the ability to prevent cytokine-induced increases in epithelial permeability. Design A genus-specific quantitative PCR was used for quantification of Butyricicoccus in stools from patients with UC or CD and healthy subjects. The effect of B pullicaecorum on trinitrobenzenesulfonic (TNBS)-induced colitis was assessed and the effect of B pullicaecorum culture supernatant on epithelial barrier function was investigated in vitro. Results The average number of Butyricicoccus in stools from patients with UC and CD in active (UC: 8.61 log10/g stool; CD: 6.58 log10/g stool) and remission phase (UC: 8.69 log10/g stool; CD: 8.38 log10/g stool) was significantly lower compared with healthy subjects (9.32 log10/g stool) and correlated with disease activity in CD. Oral administration of B pullicaecorum resulted in a significant protective effect based on macroscopic and histological criteria and decreased intestinal myeloperoxidase (MPO), tumour necrosis factor α (TNFα) and interleukin (IL)-12 levels. Supernatant of B pullicaecorum prevented the loss of transepithelial resistance (TER) and the increase in IL-8 secretion induced by TNFα and interferon γ (IFN gamma) in a Caco-2 cell model. Conclusions Patients with inflammatory bowel disease have lower numbers of Butyricicoccus bacteria in their stools. Administration of B pullicaecorum attenuates TNBS-induced colitis in rats and supernatant of B pullicaecorum cultures strengthens the epithelial barrier function by increasing the TER.</description><identifier>ISSN: 0017-5749</identifier><identifier>EISSN: 1468-3288</identifier><identifier>DOI: 10.1136/gutjnl-2012-303611</identifier><identifier>PMID: 23263527</identifier><identifier>CODEN: GUTTAK</identifier><language>eng</language><publisher>England: BMJ Publishing Group Ltd and British Society of Gastroenterology</publisher><subject>Adult ; Animals ; Bacteria ; Bacterial Load ; Biopsy ; Butyrate ; Case-Control Studies ; Colitis, Ulcerative - microbiology ; Colitis, Ulcerative - prevention & control ; Crohn Disease - microbiology ; Crohn Disease - prevention & control ; Cytokines ; Disease Models, Animal ; Epithelial Barrier ; Feces - microbiology ; Female ; Firmicutes ; Gram-Positive Endospore-Forming Rods - genetics ; Gram-Positive Endospore-Forming Rods - physiology ; Humans ; IBD ; Inflammation ; Inflammatory bowel disease ; Intestinal Mucosa - metabolism ; Male ; Permeability ; Prevention ; Probiotics ; Probiotics - pharmacology ; Rats ; Rats, Wistar ; Real-Time Polymerase Chain Reaction ; RNA, Ribosomal, 16S - genetics ; Rodents ; Studies ; Womens health</subject><ispartof>Gut, 2013-12, Vol.62 (12), p.1745-1752</ispartof><rights>Published by the BMJ Publishing Group Limited. For permission to use (where not already granted under a licence) please go to http://group.bmj.com/group/rights-licensing/permissions</rights><rights>Copyright: 2013 Published by the BMJ Publishing Group Limited. For permission to use (where not already granted under a licence) please go to http://group.bmj.com/group/rights-licensing/permissions</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-b489t-5cf2816d847714854a654de7c86ca4a4b835fb1dc36192d768378726ba4f5e923</citedby><cites>FETCH-LOGICAL-b489t-5cf2816d847714854a654de7c86ca4a4b835fb1dc36192d768378726ba4f5e923</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttp://gut.bmj.com/content/62/12/1745.full.pdf$$EPDF$$P50$$Gbmj$$H</linktopdf><linktohtml>$$Uhttp://gut.bmj.com/content/62/12/1745.full$$EHTML$$P50$$Gbmj$$H</linktohtml><link.rule.ids>114,115,314,780,784,3196,23571,27924,27925,77472,77503</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/23263527$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Eeckhaut, Venessa</creatorcontrib><creatorcontrib>Machiels, Kathleen</creatorcontrib><creatorcontrib>Perrier, Clémentine</creatorcontrib><creatorcontrib>Romero, Carlos</creatorcontrib><creatorcontrib>Maes, Sofie</creatorcontrib><creatorcontrib>Flahou, Bram</creatorcontrib><creatorcontrib>Steppe, Marjan</creatorcontrib><creatorcontrib>Haesebrouck, Freddy</creatorcontrib><creatorcontrib>Sas, Benedikt</creatorcontrib><creatorcontrib>Ducatelle, Richard</creatorcontrib><creatorcontrib>Vermeire, Severine</creatorcontrib><creatorcontrib>Van Immerseel, Filip</creatorcontrib><title>Butyricicoccus pullicaecorum in inflammatory bowel disease</title><title>Gut</title><addtitle>Gut</addtitle><description>Objective Many species within the phylum Firmicutes are thought to exert anti-inflammatory effects. We quantified bacteria belonging to the genus Butyricicoccus in stools of patients with ulcerative colitis (UC) and Crohn's disease (CD). We evaluated the effect of Butyricicoccus pullicaecorum in a rat colitis model and analysed the ability to prevent cytokine-induced increases in epithelial permeability. Design A genus-specific quantitative PCR was used for quantification of Butyricicoccus in stools from patients with UC or CD and healthy subjects. The effect of B pullicaecorum on trinitrobenzenesulfonic (TNBS)-induced colitis was assessed and the effect of B pullicaecorum culture supernatant on epithelial barrier function was investigated in vitro. Results The average number of Butyricicoccus in stools from patients with UC and CD in active (UC: 8.61 log10/g stool; CD: 6.58 log10/g stool) and remission phase (UC: 8.69 log10/g stool; CD: 8.38 log10/g stool) was significantly lower compared with healthy subjects (9.32 log10/g stool) and correlated with disease activity in CD. Oral administration of B pullicaecorum resulted in a significant protective effect based on macroscopic and histological criteria and decreased intestinal myeloperoxidase (MPO), tumour necrosis factor α (TNFα) and interleukin (IL)-12 levels. Supernatant of B pullicaecorum prevented the loss of transepithelial resistance (TER) and the increase in IL-8 secretion induced by TNFα and interferon γ (IFN gamma) in a Caco-2 cell model. Conclusions Patients with inflammatory bowel disease have lower numbers of Butyricicoccus bacteria in their stools. Administration of B pullicaecorum attenuates TNBS-induced colitis in rats and supernatant of B pullicaecorum cultures strengthens the epithelial barrier function by increasing the TER.</description><subject>Adult</subject><subject>Animals</subject><subject>Bacteria</subject><subject>Bacterial Load</subject><subject>Biopsy</subject><subject>Butyrate</subject><subject>Case-Control Studies</subject><subject>Colitis, Ulcerative - microbiology</subject><subject>Colitis, Ulcerative - prevention & control</subject><subject>Crohn Disease - microbiology</subject><subject>Crohn Disease - prevention & control</subject><subject>Cytokines</subject><subject>Disease Models, Animal</subject><subject>Epithelial Barrier</subject><subject>Feces - microbiology</subject><subject>Female</subject><subject>Firmicutes</subject><subject>Gram-Positive Endospore-Forming Rods - genetics</subject><subject>Gram-Positive Endospore-Forming Rods - physiology</subject><subject>Humans</subject><subject>IBD</subject><subject>Inflammation</subject><subject>Inflammatory bowel disease</subject><subject>Intestinal Mucosa - metabolism</subject><subject>Male</subject><subject>Permeability</subject><subject>Prevention</subject><subject>Probiotics</subject><subject>Probiotics - pharmacology</subject><subject>Rats</subject><subject>Rats, Wistar</subject><subject>Real-Time Polymerase Chain Reaction</subject><subject>RNA, Ribosomal, 16S - genetics</subject><subject>Rodents</subject><subject>Studies</subject><subject>Womens health</subject><issn>0017-5749</issn><issn>1468-3288</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><recordid>eNqNkUtLw0AQxxdRtD6-gAcpePES3dl3vGmxPlEK1euy2WwkNWnqbhbttzclPsCLwsAc5jf_efwR2gd8DEDFyXNsZ_MqIRhIQjEVAGtoAEyohBKl1tEAY5AJlyzdQtshzDDGSqWwibYIJYJyIgfo9Dy2S1_a0jbWxjBcxKoqrXG28bEelvMuisrUtWkbvxxmzZurhnkZnAluF20Upgpu7zPvoMfxxXR0ldw9XF6Pzu6SjKm0TbgtiAKRKyYlMMWZEZzlTlolrGGGZYryIoPcdgekJJdCUakkEZlhBXcpoTvoqNdd-OY1utDqugzWVZWZuyYGDZJTxgVN5d8oY2m3BYDo0MNf6KyJft4d0gnKlAkQajWb9JT1TQjeFXrhy9r4pQasVybo3gS9MkH3JnRNB5_SMatd_t3y9fUOSHqgDK17_64b_6KFpJLr-6eRHt3cjCfTW6onP3xWz_6zwAd4Wp-X</recordid><startdate>20131201</startdate><enddate>20131201</enddate><creator>Eeckhaut, Venessa</creator><creator>Machiels, Kathleen</creator><creator>Perrier, Clémentine</creator><creator>Romero, Carlos</creator><creator>Maes, Sofie</creator><creator>Flahou, Bram</creator><creator>Steppe, Marjan</creator><creator>Haesebrouck, Freddy</creator><creator>Sas, Benedikt</creator><creator>Ducatelle, Richard</creator><creator>Vermeire, Severine</creator><creator>Van Immerseel, Filip</creator><general>BMJ Publishing Group Ltd and British Society of Gastroenterology</general><general>BMJ Publishing Group LTD</general><scope>BSCLL</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>3V.</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>88I</scope><scope>8AF</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>BTHHO</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M2P</scope><scope>M7P</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>Q9U</scope><scope>7X8</scope><scope>7T5</scope><scope>H94</scope></search><sort><creationdate>20131201</creationdate><title>Butyricicoccus pullicaecorum in inflammatory bowel disease</title><author>Eeckhaut, Venessa ; Machiels, Kathleen ; Perrier, Clémentine ; Romero, Carlos ; Maes, Sofie ; Flahou, Bram ; Steppe, Marjan ; Haesebrouck, Freddy ; Sas, Benedikt ; Ducatelle, Richard ; Vermeire, Severine ; Van Immerseel, Filip</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-b489t-5cf2816d847714854a654de7c86ca4a4b835fb1dc36192d768378726ba4f5e923</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>Adult</topic><topic>Animals</topic><topic>Bacteria</topic><topic>Bacterial Load</topic><topic>Biopsy</topic><topic>Butyrate</topic><topic>Case-Control Studies</topic><topic>Colitis, Ulcerative - microbiology</topic><topic>Colitis, Ulcerative - prevention & control</topic><topic>Crohn Disease - microbiology</topic><topic>Crohn Disease - prevention & control</topic><topic>Cytokines</topic><topic>Disease Models, Animal</topic><topic>Epithelial Barrier</topic><topic>Feces - microbiology</topic><topic>Female</topic><topic>Firmicutes</topic><topic>Gram-Positive Endospore-Forming Rods - genetics</topic><topic>Gram-Positive Endospore-Forming Rods - physiology</topic><topic>Humans</topic><topic>IBD</topic><topic>Inflammation</topic><topic>Inflammatory bowel disease</topic><topic>Intestinal Mucosa - metabolism</topic><topic>Male</topic><topic>Permeability</topic><topic>Prevention</topic><topic>Probiotics</topic><topic>Probiotics - pharmacology</topic><topic>Rats</topic><topic>Rats, Wistar</topic><topic>Real-Time Polymerase Chain Reaction</topic><topic>RNA, Ribosomal, 16S - genetics</topic><topic>Rodents</topic><topic>Studies</topic><topic>Womens health</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Eeckhaut, Venessa</creatorcontrib><creatorcontrib>Machiels, Kathleen</creatorcontrib><creatorcontrib>Perrier, Clémentine</creatorcontrib><creatorcontrib>Romero, Carlos</creatorcontrib><creatorcontrib>Maes, Sofie</creatorcontrib><creatorcontrib>Flahou, Bram</creatorcontrib><creatorcontrib>Steppe, Marjan</creatorcontrib><creatorcontrib>Haesebrouck, Freddy</creatorcontrib><creatorcontrib>Sas, Benedikt</creatorcontrib><creatorcontrib>Ducatelle, Richard</creatorcontrib><creatorcontrib>Vermeire, Severine</creatorcontrib><creatorcontrib>Van Immerseel, Filip</creatorcontrib><collection>Istex</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Science Database (Alumni Edition)</collection><collection>STEM Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>BMJ Journals</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Science Database</collection><collection>Biological Science Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>ProQuest Central Basic</collection><collection>MEDLINE - Academic</collection><collection>Immunology Abstracts</collection><collection>AIDS and Cancer Research Abstracts</collection><jtitle>Gut</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Eeckhaut, Venessa</au><au>Machiels, Kathleen</au><au>Perrier, Clémentine</au><au>Romero, Carlos</au><au>Maes, Sofie</au><au>Flahou, Bram</au><au>Steppe, Marjan</au><au>Haesebrouck, Freddy</au><au>Sas, Benedikt</au><au>Ducatelle, Richard</au><au>Vermeire, Severine</au><au>Van Immerseel, Filip</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Butyricicoccus pullicaecorum in inflammatory bowel disease</atitle><jtitle>Gut</jtitle><addtitle>Gut</addtitle><date>2013-12-01</date><risdate>2013</risdate><volume>62</volume><issue>12</issue><spage>1745</spage><epage>1752</epage><pages>1745-1752</pages><issn>0017-5749</issn><eissn>1468-3288</eissn><coden>GUTTAK</coden><abstract>Objective Many species within the phylum Firmicutes are thought to exert anti-inflammatory effects. We quantified bacteria belonging to the genus Butyricicoccus in stools of patients with ulcerative colitis (UC) and Crohn's disease (CD). We evaluated the effect of Butyricicoccus pullicaecorum in a rat colitis model and analysed the ability to prevent cytokine-induced increases in epithelial permeability. Design A genus-specific quantitative PCR was used for quantification of Butyricicoccus in stools from patients with UC or CD and healthy subjects. The effect of B pullicaecorum on trinitrobenzenesulfonic (TNBS)-induced colitis was assessed and the effect of B pullicaecorum culture supernatant on epithelial barrier function was investigated in vitro. Results The average number of Butyricicoccus in stools from patients with UC and CD in active (UC: 8.61 log10/g stool; CD: 6.58 log10/g stool) and remission phase (UC: 8.69 log10/g stool; CD: 8.38 log10/g stool) was significantly lower compared with healthy subjects (9.32 log10/g stool) and correlated with disease activity in CD. Oral administration of B pullicaecorum resulted in a significant protective effect based on macroscopic and histological criteria and decreased intestinal myeloperoxidase (MPO), tumour necrosis factor α (TNFα) and interleukin (IL)-12 levels. Supernatant of B pullicaecorum prevented the loss of transepithelial resistance (TER) and the increase in IL-8 secretion induced by TNFα and interferon γ (IFN gamma) in a Caco-2 cell model. Conclusions Patients with inflammatory bowel disease have lower numbers of Butyricicoccus bacteria in their stools. Administration of B pullicaecorum attenuates TNBS-induced colitis in rats and supernatant of B pullicaecorum cultures strengthens the epithelial barrier function by increasing the TER.</abstract><cop>England</cop><pub>BMJ Publishing Group Ltd and British Society of Gastroenterology</pub><pmid>23263527</pmid><doi>10.1136/gutjnl-2012-303611</doi><tpages>8</tpages></addata></record> |
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subjects | Adult Animals Bacteria Bacterial Load Biopsy Butyrate Case-Control Studies Colitis, Ulcerative - microbiology Colitis, Ulcerative - prevention & control Crohn Disease - microbiology Crohn Disease - prevention & control Cytokines Disease Models, Animal Epithelial Barrier Feces - microbiology Female Firmicutes Gram-Positive Endospore-Forming Rods - genetics Gram-Positive Endospore-Forming Rods - physiology Humans IBD Inflammation Inflammatory bowel disease Intestinal Mucosa - metabolism Male Permeability Prevention Probiotics Probiotics - pharmacology Rats Rats, Wistar Real-Time Polymerase Chain Reaction RNA, Ribosomal, 16S - genetics Rodents Studies Womens health |
title | Butyricicoccus pullicaecorum in inflammatory bowel disease |
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