Adipose tissue derived bacteria are associated with inflammation in obesity and type 2 diabetes
ObjectiveBacterial translocation to various organs including human adipose tissue (AT) due to increased intestinal permeability remains poorly understood. We hypothesised that: (1) bacterial presence is highly tissue specific and (2) related in composition and quantity to immune inflammatory and met...
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| Veröffentlicht in: | Gut 2020-10, Vol.69 (10), p.1796-1806 |
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| creator | Massier, Lucas Chakaroun, Rima Tabei, Shirin Crane, Alyce Didt, Konrad David Fallmann, Jörg von Bergen, Martin Haange, Sven-Bastiaan Heyne, Henrike Stumvoll, Michael Gericke, Martin Dietrich, Arne Blüher, Matthias Musat, Niculina Kovacs, Peter |
| description | ObjectiveBacterial translocation to various organs including human adipose tissue (AT) due to increased intestinal permeability remains poorly understood. We hypothesised that: (1) bacterial presence is highly tissue specific and (2) related in composition and quantity to immune inflammatory and metabolic burden.DesignWe quantified and sequenced the bacterial 16S rRNA gene in blood and AT samples (omental, mesenteric and subcutaneous) of 75 subjects with obesity with or without type 2 diabetes (T2D) and used catalysed reporter deposition (CARD) – fluorescence in situ hybridisation (FISH) to detect bacteria in AT.ResultsUnder stringent experimental and bioinformatic control for contaminants, bacterial DNA was detected in blood and omental, subcutaneous and mesenteric AT samples in the range of 0.1 to 5 pg/µg DNA isolate. Moreover, CARD-FISH allowed the detection of living, AT-borne bacteria. Proteobacteria and Firmicutes were the predominant phyla, and bacterial quantity was associated with immune cell infiltration, inflammatory and metabolic parameters in a tissue-specific manner. Bacterial composition differed between subjects with and without T2D and was associated with related clinical measures, including systemic and tissues-specific inflammatory markers. Finally, treatment of adipocytes with bacterial DNA in vitro stimulated the expression of TNFA and IL6.ConclusionsOur study provides contaminant aware evidence for the presence of bacteria and bacterial DNA in several ATs in obesity and T2D and suggests an important role of bacteria in initiating and sustaining local AT subclinical inflammation and therefore impacting metabolic sequelae of obesity. |
| doi_str_mv | 10.1136/gutjnl-2019-320118 |
| format | Article |
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We hypothesised that: (1) bacterial presence is highly tissue specific and (2) related in composition and quantity to immune inflammatory and metabolic burden.DesignWe quantified and sequenced the bacterial 16S rRNA gene in blood and AT samples (omental, mesenteric and subcutaneous) of 75 subjects with obesity with or without type 2 diabetes (T2D) and used catalysed reporter deposition (CARD) – fluorescence in situ hybridisation (FISH) to detect bacteria in AT.ResultsUnder stringent experimental and bioinformatic control for contaminants, bacterial DNA was detected in blood and omental, subcutaneous and mesenteric AT samples in the range of 0.1 to 5 pg/µg DNA isolate. Moreover, CARD-FISH allowed the detection of living, AT-borne bacteria. Proteobacteria and Firmicutes were the predominant phyla, and bacterial quantity was associated with immune cell infiltration, inflammatory and metabolic parameters in a tissue-specific manner. Bacterial composition differed between subjects with and without T2D and was associated with related clinical measures, including systemic and tissues-specific inflammatory markers. Finally, treatment of adipocytes with bacterial DNA in vitro stimulated the expression of TNFA and IL6.ConclusionsOur study provides contaminant aware evidence for the presence of bacteria and bacterial DNA in several ATs in obesity and T2D and suggests an important role of bacteria in initiating and sustaining local AT subclinical inflammation and therefore impacting metabolic sequelae of obesity.</description><identifier>ISSN: 0017-5749</identifier><identifier>EISSN: 1468-3288</identifier><identifier>DOI: 10.1136/gutjnl-2019-320118</identifier><identifier>PMID: 32317332</identifier><language>eng</language><publisher>England: BMJ Publishing Group Ltd and British Society of Gastroenterology</publisher><subject>Adipocytes ; Adipose tissue ; Adipose Tissue - immunology ; Adipose Tissue - microbiology ; Antibiotics ; Bacteria ; bacterial translocation ; Bacterial Translocation - immunology ; Body fat ; Cells, Cultured ; Complications ; Contaminants ; Deoxyribonucleic acid ; Diabetes ; Diabetes mellitus (non-insulin dependent) ; Diabetes Mellitus, Type 2 - complications ; Diabetes Mellitus, Type 2 - immunology ; DNA ; DNA, Bacterial - isolation & purification ; Female ; Firmicutes - isolation & purification ; Fluorescence in situ hybridization ; Gastrointestinal surgery ; Gut microbiota ; Humans ; Inflammation ; Inflammation - immunology ; Insulin resistance ; Interleukin 6 ; Interleukin-6 - metabolism ; Intestinal Mucosa - metabolism ; intestinal permeability ; Intestine ; Male ; Metabolic disorders ; Microbiota ; Middle Aged ; Obesity ; Obesity - complications ; Obesity - immunology ; obesity surgery ; Permeability ; Proteobacteria - isolation & purification ; RNA, Ribosomal, 16S - blood ; rRNA 16S ; Tumor Necrosis Factor-alpha - metabolism ; Tumor necrosis factor-TNF</subject><ispartof>Gut, 2020-10, Vol.69 (10), p.1796-1806</ispartof><rights>Author(s) (or their employer(s)) 2020. No commercial re-use. See rights and permissions. Published by BMJ.</rights><rights>2020 Author(s) (or their employer(s)) 2020. No commercial re-use. See rights and permissions. Published by BMJ.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-b452t-82b200706ab84c736adbcae80da346e211d4a429529df3291cde30a6a844de483</citedby><cites>FETCH-LOGICAL-b452t-82b200706ab84c736adbcae80da346e211d4a429529df3291cde30a6a844de483</cites><orcidid>0000-0002-0290-5423 ; 0000-0003-2952-1152</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,776,780,27903,27904</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/32317332$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Massier, Lucas</creatorcontrib><creatorcontrib>Chakaroun, Rima</creatorcontrib><creatorcontrib>Tabei, Shirin</creatorcontrib><creatorcontrib>Crane, Alyce</creatorcontrib><creatorcontrib>Didt, Konrad David</creatorcontrib><creatorcontrib>Fallmann, Jörg</creatorcontrib><creatorcontrib>von Bergen, Martin</creatorcontrib><creatorcontrib>Haange, Sven-Bastiaan</creatorcontrib><creatorcontrib>Heyne, Henrike</creatorcontrib><creatorcontrib>Stumvoll, Michael</creatorcontrib><creatorcontrib>Gericke, Martin</creatorcontrib><creatorcontrib>Dietrich, Arne</creatorcontrib><creatorcontrib>Blüher, Matthias</creatorcontrib><creatorcontrib>Musat, Niculina</creatorcontrib><creatorcontrib>Kovacs, Peter</creatorcontrib><title>Adipose tissue derived bacteria are associated with inflammation in obesity and type 2 diabetes</title><title>Gut</title><addtitle>Gut</addtitle><addtitle>Gut</addtitle><description>ObjectiveBacterial translocation to various organs including human adipose tissue (AT) due to increased intestinal permeability remains poorly understood. We hypothesised that: (1) bacterial presence is highly tissue specific and (2) related in composition and quantity to immune inflammatory and metabolic burden.DesignWe quantified and sequenced the bacterial 16S rRNA gene in blood and AT samples (omental, mesenteric and subcutaneous) of 75 subjects with obesity with or without type 2 diabetes (T2D) and used catalysed reporter deposition (CARD) – fluorescence in situ hybridisation (FISH) to detect bacteria in AT.ResultsUnder stringent experimental and bioinformatic control for contaminants, bacterial DNA was detected in blood and omental, subcutaneous and mesenteric AT samples in the range of 0.1 to 5 pg/µg DNA isolate. Moreover, CARD-FISH allowed the detection of living, AT-borne bacteria. Proteobacteria and Firmicutes were the predominant phyla, and bacterial quantity was associated with immune cell infiltration, inflammatory and metabolic parameters in a tissue-specific manner. Bacterial composition differed between subjects with and without T2D and was associated with related clinical measures, including systemic and tissues-specific inflammatory markers. Finally, treatment of adipocytes with bacterial DNA in vitro stimulated the expression of TNFA and IL6.ConclusionsOur study provides contaminant aware evidence for the presence of bacteria and bacterial DNA in several ATs in obesity and T2D and suggests an important role of bacteria in initiating and sustaining local AT subclinical inflammation and therefore impacting metabolic sequelae of obesity.</description><subject>Adipocytes</subject><subject>Adipose tissue</subject><subject>Adipose Tissue - immunology</subject><subject>Adipose Tissue - microbiology</subject><subject>Antibiotics</subject><subject>Bacteria</subject><subject>bacterial translocation</subject><subject>Bacterial Translocation - immunology</subject><subject>Body fat</subject><subject>Cells, Cultured</subject><subject>Complications</subject><subject>Contaminants</subject><subject>Deoxyribonucleic acid</subject><subject>Diabetes</subject><subject>Diabetes mellitus (non-insulin dependent)</subject><subject>Diabetes Mellitus, Type 2 - complications</subject><subject>Diabetes Mellitus, Type 2 - immunology</subject><subject>DNA</subject><subject>DNA, Bacterial - isolation & purification</subject><subject>Female</subject><subject>Firmicutes - isolation & purification</subject><subject>Fluorescence in situ hybridization</subject><subject>Gastrointestinal surgery</subject><subject>Gut microbiota</subject><subject>Humans</subject><subject>Inflammation</subject><subject>Inflammation - immunology</subject><subject>Insulin resistance</subject><subject>Interleukin 6</subject><subject>Interleukin-6 - metabolism</subject><subject>Intestinal Mucosa - metabolism</subject><subject>intestinal permeability</subject><subject>Intestine</subject><subject>Male</subject><subject>Metabolic disorders</subject><subject>Microbiota</subject><subject>Middle Aged</subject><subject>Obesity</subject><subject>Obesity - complications</subject><subject>Obesity - immunology</subject><subject>obesity surgery</subject><subject>Permeability</subject><subject>Proteobacteria - isolation & purification</subject><subject>RNA, Ribosomal, 16S - blood</subject><subject>rRNA 16S</subject><subject>Tumor Necrosis Factor-alpha - metabolism</subject><subject>Tumor necrosis factor-TNF</subject><issn>0017-5749</issn><issn>1468-3288</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><recordid>eNqNkEtrGzEURkVJqF23fyCLIMimm0n08oy0NCZ9gCGbdC2uRteNzDyckSbB_74y4zqQRelG0hXn-7gcQq44u-Vclne_x7TrmkIwbgqZT64_kDlXpc6T1hdkzhivimWlzIx8inHHGNPa8I9kJoXklZRiTuzKh30fkaYQ44jU4xBe0FMHdcpPoDAghRj7OkDK_68hPdHQbRtoW0ih7_JAe4cxpAOFztN02CMV1AdwmDB-JpdbaCJ-Od0L8uvb_eP6R7F5-P5zvdoUTi1FKrRwgrGKleC0qitZgnc1oGYepCpRcO4VKGGWwvitFIbXHiWDErRSHpWWC_J16t0P_fOIMdk2xBqbBjrsx2iFNHJpNKtMRm_eobt-HLq8nRVKsZIpnuUsiJioeuhjHHBr90NoYThYzuxRv53026N-O-nPoetT9eha9OfIX98ZKCbAtbv_K7x9489r_iPwB-Dknps</recordid><startdate>20201001</startdate><enddate>20201001</enddate><creator>Massier, Lucas</creator><creator>Chakaroun, Rima</creator><creator>Tabei, Shirin</creator><creator>Crane, Alyce</creator><creator>Didt, Konrad David</creator><creator>Fallmann, Jörg</creator><creator>von Bergen, Martin</creator><creator>Haange, Sven-Bastiaan</creator><creator>Heyne, Henrike</creator><creator>Stumvoll, Michael</creator><creator>Gericke, Martin</creator><creator>Dietrich, Arne</creator><creator>Blüher, Matthias</creator><creator>Musat, Niculina</creator><creator>Kovacs, Peter</creator><general>BMJ Publishing Group Ltd and British Society of Gastroenterology</general><general>BMJ Publishing Group LTD</general><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><orcidid>https://orcid.org/0000-0002-0290-5423</orcidid><orcidid>https://orcid.org/0000-0003-2952-1152</orcidid></search><sort><creationdate>20201001</creationdate><title>Adipose tissue derived bacteria are associated with inflammation in obesity and type 2 diabetes</title><author>Massier, Lucas ; Chakaroun, Rima ; Tabei, Shirin ; Crane, Alyce ; Didt, Konrad David ; Fallmann, Jörg ; von Bergen, Martin ; Haange, Sven-Bastiaan ; Heyne, Henrike ; Stumvoll, Michael ; Gericke, Martin ; Dietrich, Arne ; Blüher, Matthias ; Musat, Niculina ; Kovacs, Peter</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-b452t-82b200706ab84c736adbcae80da346e211d4a429529df3291cde30a6a844de483</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Adipocytes</topic><topic>Adipose tissue</topic><topic>Adipose Tissue - immunology</topic><topic>Adipose Tissue - microbiology</topic><topic>Antibiotics</topic><topic>Bacteria</topic><topic>bacterial translocation</topic><topic>Bacterial Translocation - immunology</topic><topic>Body fat</topic><topic>Cells, Cultured</topic><topic>Complications</topic><topic>Contaminants</topic><topic>Deoxyribonucleic acid</topic><topic>Diabetes</topic><topic>Diabetes mellitus (non-insulin dependent)</topic><topic>Diabetes Mellitus, Type 2 - complications</topic><topic>Diabetes Mellitus, Type 2 - immunology</topic><topic>DNA</topic><topic>DNA, Bacterial - isolation & purification</topic><topic>Female</topic><topic>Firmicutes - isolation & purification</topic><topic>Fluorescence in situ hybridization</topic><topic>Gastrointestinal surgery</topic><topic>Gut microbiota</topic><topic>Humans</topic><topic>Inflammation</topic><topic>Inflammation - immunology</topic><topic>Insulin resistance</topic><topic>Interleukin 6</topic><topic>Interleukin-6 - metabolism</topic><topic>Intestinal Mucosa - metabolism</topic><topic>intestinal permeability</topic><topic>Intestine</topic><topic>Male</topic><topic>Metabolic disorders</topic><topic>Microbiota</topic><topic>Middle Aged</topic><topic>Obesity</topic><topic>Obesity - complications</topic><topic>Obesity - immunology</topic><topic>obesity surgery</topic><topic>Permeability</topic><topic>Proteobacteria - isolation & purification</topic><topic>RNA, Ribosomal, 16S - blood</topic><topic>rRNA 16S</topic><topic>Tumor Necrosis Factor-alpha - metabolism</topic><topic>Tumor necrosis factor-TNF</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Massier, Lucas</creatorcontrib><creatorcontrib>Chakaroun, Rima</creatorcontrib><creatorcontrib>Tabei, Shirin</creatorcontrib><creatorcontrib>Crane, Alyce</creatorcontrib><creatorcontrib>Didt, Konrad David</creatorcontrib><creatorcontrib>Fallmann, Jörg</creatorcontrib><creatorcontrib>von Bergen, Martin</creatorcontrib><creatorcontrib>Haange, Sven-Bastiaan</creatorcontrib><creatorcontrib>Heyne, Henrike</creatorcontrib><creatorcontrib>Stumvoll, Michael</creatorcontrib><creatorcontrib>Gericke, Martin</creatorcontrib><creatorcontrib>Dietrich, Arne</creatorcontrib><creatorcontrib>Blüher, Matthias</creatorcontrib><creatorcontrib>Musat, Niculina</creatorcontrib><creatorcontrib>Kovacs, Peter</creatorcontrib><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><jtitle>Gut</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Massier, Lucas</au><au>Chakaroun, Rima</au><au>Tabei, Shirin</au><au>Crane, Alyce</au><au>Didt, Konrad David</au><au>Fallmann, Jörg</au><au>von Bergen, Martin</au><au>Haange, Sven-Bastiaan</au><au>Heyne, Henrike</au><au>Stumvoll, Michael</au><au>Gericke, Martin</au><au>Dietrich, Arne</au><au>Blüher, Matthias</au><au>Musat, Niculina</au><au>Kovacs, Peter</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Adipose tissue derived bacteria are associated with inflammation in obesity and type 2 diabetes</atitle><jtitle>Gut</jtitle><stitle>Gut</stitle><addtitle>Gut</addtitle><date>2020-10-01</date><risdate>2020</risdate><volume>69</volume><issue>10</issue><spage>1796</spage><epage>1806</epage><pages>1796-1806</pages><issn>0017-5749</issn><eissn>1468-3288</eissn><abstract>ObjectiveBacterial translocation to various organs including human adipose tissue (AT) due to increased intestinal permeability remains poorly understood. We hypothesised that: (1) bacterial presence is highly tissue specific and (2) related in composition and quantity to immune inflammatory and metabolic burden.DesignWe quantified and sequenced the bacterial 16S rRNA gene in blood and AT samples (omental, mesenteric and subcutaneous) of 75 subjects with obesity with or without type 2 diabetes (T2D) and used catalysed reporter deposition (CARD) – fluorescence in situ hybridisation (FISH) to detect bacteria in AT.ResultsUnder stringent experimental and bioinformatic control for contaminants, bacterial DNA was detected in blood and omental, subcutaneous and mesenteric AT samples in the range of 0.1 to 5 pg/µg DNA isolate. Moreover, CARD-FISH allowed the detection of living, AT-borne bacteria. Proteobacteria and Firmicutes were the predominant phyla, and bacterial quantity was associated with immune cell infiltration, inflammatory and metabolic parameters in a tissue-specific manner. Bacterial composition differed between subjects with and without T2D and was associated with related clinical measures, including systemic and tissues-specific inflammatory markers. Finally, treatment of adipocytes with bacterial DNA in vitro stimulated the expression of TNFA and IL6.ConclusionsOur study provides contaminant aware evidence for the presence of bacteria and bacterial DNA in several ATs in obesity and T2D and suggests an important role of bacteria in initiating and sustaining local AT subclinical inflammation and therefore impacting metabolic sequelae of obesity.</abstract><cop>England</cop><pub>BMJ Publishing Group Ltd and British Society of Gastroenterology</pub><pmid>32317332</pmid><doi>10.1136/gutjnl-2019-320118</doi><tpages>11</tpages><orcidid>https://orcid.org/0000-0002-0290-5423</orcidid><orcidid>https://orcid.org/0000-0003-2952-1152</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Adipocytes Adipose tissue Adipose Tissue - immunology Adipose Tissue - microbiology Antibiotics Bacteria bacterial translocation Bacterial Translocation - immunology Body fat Cells, Cultured Complications Contaminants Deoxyribonucleic acid Diabetes Diabetes mellitus (non-insulin dependent) Diabetes Mellitus, Type 2 - complications Diabetes Mellitus, Type 2 - immunology DNA DNA, Bacterial - isolation & purification Female Firmicutes - isolation & purification Fluorescence in situ hybridization Gastrointestinal surgery Gut microbiota Humans Inflammation Inflammation - immunology Insulin resistance Interleukin 6 Interleukin-6 - metabolism Intestinal Mucosa - metabolism intestinal permeability Intestine Male Metabolic disorders Microbiota Middle Aged Obesity Obesity - complications Obesity - immunology obesity surgery Permeability Proteobacteria - isolation & purification RNA, Ribosomal, 16S - blood rRNA 16S Tumor Necrosis Factor-alpha - metabolism Tumor necrosis factor-TNF |
| title | Adipose tissue derived bacteria are associated with inflammation in obesity and type 2 diabetes |
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