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Mode of delivery shapes gut colonization pattern and modulates regulatory immunity in mice
Delivery mode has been associated with long-term changes in gut microbiota composition and more recently also with changes in the immune system. This has further been suggested to link Cesarean section (C-section) with an increased risk for development of immune-mediated diseases such as type 1 diab...
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| Published in: | The Journal of immunology (1950) 2014-08, Vol.193 (3), p.1213-1222 |
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| container_end_page | 1222 |
| container_issue | 3 |
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| container_title | The Journal of immunology (1950) |
| container_volume | 193 |
| creator | Hansen, Camilla H F Andersen, Line S F Krych, Lukasz Metzdorff, Stine B Hasselby, Jane P Skov, Søren Nielsen, Dennis S Buschard, Karsten Hansen, Lars H Hansen, Axel K |
| description | Delivery mode has been associated with long-term changes in gut microbiota composition and more recently also with changes in the immune system. This has further been suggested to link Cesarean section (C-section) with an increased risk for development of immune-mediated diseases such as type 1 diabetes. In this study, we demonstrate that both C-section and cross-fostering with a genetically distinct strain influence the gut microbiota composition and immune key markers in mice. Gut microbiota profiling by denaturing gradient gel electrophoresis and 454/FLX-based 16S rRNA gene amplicon sequencing revealed that mice born by C-section had a distinct bacterial profile at weaning characterized by higher abundance of Bacteroides and Lachnospiraceae, and less Rikenellaceae and Ruminococcus. No clustering according to delivery method as determined by principal component analysis of denaturing gradient gel electrophoresis profiles was evident in adult mice. However, the adult C-section-born mice had lower proportions of Foxp3(+) regulatory T cells, tolerogenic CD103(+) dendritic cells, and less Il10 gene expression in mesenteric lymph nodes and spleens. This demonstrates long-term systemic effect on the regulatory immune system that was also evident in NOD mice, a model of type 1 diabetes, born by C-section. However, no effect of delivery mode was seen on diabetes incidence or insulitis development. In conclusion, the first exposure to microorganisms seems to be crucial for the early life gut microbiota and priming of regulatory immune system in mice, and mode of delivery strongly influences this. |
| doi_str_mv | 10.4049/jimmunol.1400085 |
| format | article |
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This has further been suggested to link Cesarean section (C-section) with an increased risk for development of immune-mediated diseases such as type 1 diabetes. In this study, we demonstrate that both C-section and cross-fostering with a genetically distinct strain influence the gut microbiota composition and immune key markers in mice. Gut microbiota profiling by denaturing gradient gel electrophoresis and 454/FLX-based 16S rRNA gene amplicon sequencing revealed that mice born by C-section had a distinct bacterial profile at weaning characterized by higher abundance of Bacteroides and Lachnospiraceae, and less Rikenellaceae and Ruminococcus. No clustering according to delivery method as determined by principal component analysis of denaturing gradient gel electrophoresis profiles was evident in adult mice. However, the adult C-section-born mice had lower proportions of Foxp3(+) regulatory T cells, tolerogenic CD103(+) dendritic cells, and less Il10 gene expression in mesenteric lymph nodes and spleens. This demonstrates long-term systemic effect on the regulatory immune system that was also evident in NOD mice, a model of type 1 diabetes, born by C-section. However, no effect of delivery mode was seen on diabetes incidence or insulitis development. In conclusion, the first exposure to microorganisms seems to be crucial for the early life gut microbiota and priming of regulatory immune system in mice, and mode of delivery strongly influences this.</description><identifier>ISSN: 0022-1767</identifier><identifier>EISSN: 1550-6606</identifier><identifier>DOI: 10.4049/jimmunol.1400085</identifier><identifier>PMID: 24951818</identifier><language>eng</language><publisher>United States</publisher><subject>Adaptive Immunity ; Animals ; Bacteroides ; Bacteroides - immunology ; Bacteroides - isolation & purification ; Cesarean Section - methods ; Clostridium - immunology ; Clostridium - isolation & purification ; Diabetes Mellitus, Experimental - immunology ; Diabetes Mellitus, Experimental - microbiology ; Diabetes Mellitus, Experimental - pathology ; Female ; Intestines - cytology ; Intestines - immunology ; Intestines - microbiology ; Male ; Mice ; Mice, Inbred BALB C ; Mice, Inbred C57BL ; Mice, Inbred NOD ; Microbiota - immunology ; Mucous Membrane - cytology ; Mucous Membrane - immunology ; Mucous Membrane - microbiology ; Ruminococcus ; Ruminococcus - immunology ; Ruminococcus - isolation & purification ; T-Lymphocytes, Regulatory - cytology ; T-Lymphocytes, Regulatory - immunology ; T-Lymphocytes, Regulatory - microbiology</subject><ispartof>The Journal of immunology (1950), 2014-08, Vol.193 (3), p.1213-1222</ispartof><rights>Copyright © 2014 by The American Association of Immunologists, Inc.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c440t-88107fbe9811b9993dc3b8580e83abd46fd4d18b87745782b24c0da35153e0d23</citedby><cites>FETCH-LOGICAL-c440t-88107fbe9811b9993dc3b8580e83abd46fd4d18b87745782b24c0da35153e0d23</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>315,786,790,27957,27958</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/24951818$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Hansen, Camilla H F</creatorcontrib><creatorcontrib>Andersen, Line S F</creatorcontrib><creatorcontrib>Krych, Lukasz</creatorcontrib><creatorcontrib>Metzdorff, Stine B</creatorcontrib><creatorcontrib>Hasselby, Jane P</creatorcontrib><creatorcontrib>Skov, Søren</creatorcontrib><creatorcontrib>Nielsen, Dennis S</creatorcontrib><creatorcontrib>Buschard, Karsten</creatorcontrib><creatorcontrib>Hansen, Lars H</creatorcontrib><creatorcontrib>Hansen, Axel K</creatorcontrib><title>Mode of delivery shapes gut colonization pattern and modulates regulatory immunity in mice</title><title>The Journal of immunology (1950)</title><addtitle>J Immunol</addtitle><description>Delivery mode has been associated with long-term changes in gut microbiota composition and more recently also with changes in the immune system. This has further been suggested to link Cesarean section (C-section) with an increased risk for development of immune-mediated diseases such as type 1 diabetes. In this study, we demonstrate that both C-section and cross-fostering with a genetically distinct strain influence the gut microbiota composition and immune key markers in mice. Gut microbiota profiling by denaturing gradient gel electrophoresis and 454/FLX-based 16S rRNA gene amplicon sequencing revealed that mice born by C-section had a distinct bacterial profile at weaning characterized by higher abundance of Bacteroides and Lachnospiraceae, and less Rikenellaceae and Ruminococcus. No clustering according to delivery method as determined by principal component analysis of denaturing gradient gel electrophoresis profiles was evident in adult mice. However, the adult C-section-born mice had lower proportions of Foxp3(+) regulatory T cells, tolerogenic CD103(+) dendritic cells, and less Il10 gene expression in mesenteric lymph nodes and spleens. This demonstrates long-term systemic effect on the regulatory immune system that was also evident in NOD mice, a model of type 1 diabetes, born by C-section. However, no effect of delivery mode was seen on diabetes incidence or insulitis development. In conclusion, the first exposure to microorganisms seems to be crucial for the early life gut microbiota and priming of regulatory immune system in mice, and mode of delivery strongly influences this.</description><subject>Adaptive Immunity</subject><subject>Animals</subject><subject>Bacteroides</subject><subject>Bacteroides - immunology</subject><subject>Bacteroides - isolation & purification</subject><subject>Cesarean Section - methods</subject><subject>Clostridium - immunology</subject><subject>Clostridium - isolation & purification</subject><subject>Diabetes Mellitus, Experimental - immunology</subject><subject>Diabetes Mellitus, Experimental - microbiology</subject><subject>Diabetes Mellitus, Experimental - pathology</subject><subject>Female</subject><subject>Intestines - cytology</subject><subject>Intestines - immunology</subject><subject>Intestines - microbiology</subject><subject>Male</subject><subject>Mice</subject><subject>Mice, Inbred BALB C</subject><subject>Mice, Inbred C57BL</subject><subject>Mice, Inbred NOD</subject><subject>Microbiota - immunology</subject><subject>Mucous Membrane - cytology</subject><subject>Mucous Membrane - immunology</subject><subject>Mucous Membrane - microbiology</subject><subject>Ruminococcus</subject><subject>Ruminococcus - immunology</subject><subject>Ruminococcus - isolation & purification</subject><subject>T-Lymphocytes, Regulatory - cytology</subject><subject>T-Lymphocytes, Regulatory - immunology</subject><subject>T-Lymphocytes, Regulatory - microbiology</subject><issn>0022-1767</issn><issn>1550-6606</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2014</creationdate><recordtype>article</recordtype><recordid>eNqNkDtPwzAUhS0EoqWwMyGPLCnXr9gZUcVLKmKBhSVyYqe4SuIQO0jl15PSlpnpnuE7R1cfQpcE5hx4drN2TTO0vp4TDgBKHKEpEQKSNIX0GE0BKE2ITOUEnYWwHpEUKD9FE8ozQRRRU_T-7I3FvsLG1u7L9hscPnRnA14NEZe-9q371tH5Fnc6Rtu3WLcGN94MtY4j1tvVNvmx-PuLi2NoceNKe45OKl0He7G_M_R2f_e6eEyWLw9Pi9tlUnIOMVGKgKwKmylCiizLmClZoYQCq5guDE8rww1RhZKSC6loQXkJRjNBBLNgKJuh691u1_vPwYaYNy6Utq51a_0QcqJApRIY_QcquFSMAIERhR1a9j6E3lZ517tG95ucQL6Vnx_k53v5Y-Vqvz4UjTV_hYNt9gOIQ4I9</recordid><startdate>20140801</startdate><enddate>20140801</enddate><creator>Hansen, Camilla H F</creator><creator>Andersen, Line S F</creator><creator>Krych, Lukasz</creator><creator>Metzdorff, Stine B</creator><creator>Hasselby, Jane P</creator><creator>Skov, Søren</creator><creator>Nielsen, Dennis S</creator><creator>Buschard, Karsten</creator><creator>Hansen, Lars H</creator><creator>Hansen, Axel K</creator><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>7X8</scope><scope>7T5</scope><scope>H94</scope></search><sort><creationdate>20140801</creationdate><title>Mode of delivery shapes gut colonization pattern and modulates regulatory immunity in mice</title><author>Hansen, Camilla H F ; Andersen, Line S F ; Krych, Lukasz ; Metzdorff, Stine B ; Hasselby, Jane P ; Skov, Søren ; Nielsen, Dennis S ; Buschard, Karsten ; Hansen, Lars H ; Hansen, Axel K</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c440t-88107fbe9811b9993dc3b8580e83abd46fd4d18b87745782b24c0da35153e0d23</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2014</creationdate><topic>Adaptive Immunity</topic><topic>Animals</topic><topic>Bacteroides</topic><topic>Bacteroides - immunology</topic><topic>Bacteroides - isolation & purification</topic><topic>Cesarean Section - methods</topic><topic>Clostridium - immunology</topic><topic>Clostridium - isolation & purification</topic><topic>Diabetes Mellitus, Experimental - immunology</topic><topic>Diabetes Mellitus, Experimental - microbiology</topic><topic>Diabetes Mellitus, Experimental - pathology</topic><topic>Female</topic><topic>Intestines - cytology</topic><topic>Intestines - immunology</topic><topic>Intestines - microbiology</topic><topic>Male</topic><topic>Mice</topic><topic>Mice, Inbred BALB C</topic><topic>Mice, Inbred C57BL</topic><topic>Mice, Inbred NOD</topic><topic>Microbiota - immunology</topic><topic>Mucous Membrane - cytology</topic><topic>Mucous Membrane - immunology</topic><topic>Mucous Membrane - microbiology</topic><topic>Ruminococcus</topic><topic>Ruminococcus - immunology</topic><topic>Ruminococcus - isolation & purification</topic><topic>T-Lymphocytes, Regulatory - cytology</topic><topic>T-Lymphocytes, Regulatory - immunology</topic><topic>T-Lymphocytes, Regulatory - microbiology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Hansen, Camilla H F</creatorcontrib><creatorcontrib>Andersen, Line S F</creatorcontrib><creatorcontrib>Krych, Lukasz</creatorcontrib><creatorcontrib>Metzdorff, Stine B</creatorcontrib><creatorcontrib>Hasselby, Jane P</creatorcontrib><creatorcontrib>Skov, Søren</creatorcontrib><creatorcontrib>Nielsen, Dennis S</creatorcontrib><creatorcontrib>Buschard, Karsten</creatorcontrib><creatorcontrib>Hansen, Lars H</creatorcontrib><creatorcontrib>Hansen, Axel K</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>Immunology Abstracts</collection><collection>AIDS and Cancer Research Abstracts</collection><jtitle>The Journal of immunology (1950)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Hansen, Camilla H F</au><au>Andersen, Line S F</au><au>Krych, Lukasz</au><au>Metzdorff, Stine B</au><au>Hasselby, Jane P</au><au>Skov, Søren</au><au>Nielsen, Dennis S</au><au>Buschard, Karsten</au><au>Hansen, Lars H</au><au>Hansen, Axel K</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Mode of delivery shapes gut colonization pattern and modulates regulatory immunity in mice</atitle><jtitle>The Journal of immunology (1950)</jtitle><addtitle>J Immunol</addtitle><date>2014-08-01</date><risdate>2014</risdate><volume>193</volume><issue>3</issue><spage>1213</spage><epage>1222</epage><pages>1213-1222</pages><issn>0022-1767</issn><eissn>1550-6606</eissn><notes>ObjectType-Article-1</notes><notes>SourceType-Scholarly Journals-1</notes><notes>ObjectType-Feature-2</notes><notes>content type line 23</notes><abstract>Delivery mode has been associated with long-term changes in gut microbiota composition and more recently also with changes in the immune system. This has further been suggested to link Cesarean section (C-section) with an increased risk for development of immune-mediated diseases such as type 1 diabetes. In this study, we demonstrate that both C-section and cross-fostering with a genetically distinct strain influence the gut microbiota composition and immune key markers in mice. Gut microbiota profiling by denaturing gradient gel electrophoresis and 454/FLX-based 16S rRNA gene amplicon sequencing revealed that mice born by C-section had a distinct bacterial profile at weaning characterized by higher abundance of Bacteroides and Lachnospiraceae, and less Rikenellaceae and Ruminococcus. No clustering according to delivery method as determined by principal component analysis of denaturing gradient gel electrophoresis profiles was evident in adult mice. However, the adult C-section-born mice had lower proportions of Foxp3(+) regulatory T cells, tolerogenic CD103(+) dendritic cells, and less Il10 gene expression in mesenteric lymph nodes and spleens. This demonstrates long-term systemic effect on the regulatory immune system that was also evident in NOD mice, a model of type 1 diabetes, born by C-section. However, no effect of delivery mode was seen on diabetes incidence or insulitis development. In conclusion, the first exposure to microorganisms seems to be crucial for the early life gut microbiota and priming of regulatory immune system in mice, and mode of delivery strongly influences this.</abstract><cop>United States</cop><pmid>24951818</pmid><doi>10.4049/jimmunol.1400085</doi><tpages>10</tpages><oa>free_for_read</oa></addata></record> |
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| ispartof | The Journal of immunology (1950), 2014-08, Vol.193 (3), p.1213-1222 |
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| source | EZB-FREE-00999 freely available EZB journals |
| subjects | Adaptive Immunity Animals Bacteroides Bacteroides - immunology Bacteroides - isolation & purification Cesarean Section - methods Clostridium - immunology Clostridium - isolation & purification Diabetes Mellitus, Experimental - immunology Diabetes Mellitus, Experimental - microbiology Diabetes Mellitus, Experimental - pathology Female Intestines - cytology Intestines - immunology Intestines - microbiology Male Mice Mice, Inbred BALB C Mice, Inbred C57BL Mice, Inbred NOD Microbiota - immunology Mucous Membrane - cytology Mucous Membrane - immunology Mucous Membrane - microbiology Ruminococcus Ruminococcus - immunology Ruminococcus - isolation & purification T-Lymphocytes, Regulatory - cytology T-Lymphocytes, Regulatory - immunology T-Lymphocytes, Regulatory - microbiology |
| title | Mode of delivery shapes gut colonization pattern and modulates regulatory immunity in mice |
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