Differential Susceptibility to T Cell-Induced Colitis in Mice: Role of the Intestinal Microbiota

Abstract One of the best characterized mouse models of the inflammatory bowel diseases (IBD; Crohn's disease, ulcerative colitis) is the CD4+CD45RBhigh T cell transfer model of chronic colitis. Following our relocation to Texas Tech University Health Sciences Center (TTUHSC), we observed a dram...

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Veröffentlicht in:Inflammatory bowel diseases 2018-01, Vol.24 (2), p.361-379
Hauptverfasser: Reinoso Webb, Cynthia, den Bakker, Hendrik, Koboziev, Iurii, Jones-Hall, Yava, Rao Kottapalli, Kameswara, Ostanin, Dmitry, Furr, Kathryn L, Mu, Qinghui, Luo, Xin M, Grisham, Matthew B
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container_end_page 379
container_issue 2
container_start_page 361
container_title Inflammatory bowel diseases
container_volume 24
creator Reinoso Webb, Cynthia
den Bakker, Hendrik
Koboziev, Iurii
Jones-Hall, Yava
Rao Kottapalli, Kameswara
Ostanin, Dmitry
Furr, Kathryn L
Mu, Qinghui
Luo, Xin M
Grisham, Matthew B
description Abstract One of the best characterized mouse models of the inflammatory bowel diseases (IBD; Crohn's disease, ulcerative colitis) is the CD4+CD45RBhigh T cell transfer model of chronic colitis. Following our relocation to Texas Tech University Health Sciences Center (TTUHSC), we observed a dramatic reduction in the incidence of moderate-to-severe colitis from a 16-year historical average of 90% at Louisiana State University Health Sciences Center (LSUHSC) to
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Following our relocation to Texas Tech University Health Sciences Center (TTUHSC), we observed a dramatic reduction in the incidence of moderate-to-severe colitis from a 16-year historical average of 90% at Louisiana State University Health Sciences Center (LSUHSC) to &lt;30% at TTUHSC. We hypothesized that differences in the commensal microbiota at the 2 institutions may account for the differences in susceptibility to T cell-induced colitis. Using bioinformatic analyses of 16S rRNA amplicon sequence data, we quantified and compared the major microbial populations in feces from healthy and colitic mice housed at the 2 institutions. We found that the bacterial composition differed greatly between mice housed at LSUHSC vs TTUHSC. We identified several genera strongly associated with, and signficantly overrepresented in high responding RAG-/- mice housed at LSUHSC. In addition, we found that colonization of healthy TTUHSC RAG-/- mice with feces obtained from healthy or colitic RAG-/- mice housed at LSUHSC transferred susceptibility to T cell-induced colitis such that the recipients developed chronic colitis with incidence and severity similar to mice generated at LSUHSC. Finally, we found that the treatment of mice with preexisting colitis with antibiotics remarkably attenuated disease. Taken together, our data demonstrate that specific microbial communities determine disease susceptibility and that manipulation of the intestinal microbiota alters the induction and/or perpetuation of chronic colitis.</description><identifier>ISSN: 1078-0998</identifier><identifier>EISSN: 1536-4844</identifier><identifier>DOI: 10.1093/ibd/izx014</identifier><identifier>PMID: 29361089</identifier><language>eng</language><publisher>US: Oxford University Press</publisher><subject>Adoptive Transfer ; Animals ; Anti-Bacterial Agents - pharmacology ; Bacteria - classification ; Basic Science Research ; Colitis - immunology ; Colitis - microbiology ; Colon - drug effects ; Colon - pathology ; Disease Models, Animal ; Feces - microbiology ; Gastrointestinal Microbiome - drug effects ; Gastrointestinal Microbiome - immunology ; Male ; Mice ; Mice, Inbred C57BL ; Mice, Knockout ; RNA, Ribosomal, 16S - genetics ; T-Lymphocytes - immunology</subject><ispartof>Inflammatory bowel diseases, 2018-01, Vol.24 (2), p.361-379</ispartof><rights>2018 Crohn's &amp; Colitis Foundation. Published by Oxford University Press. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com. 2018</rights><rights>2018 Crohn’s &amp; Colitis Foundation of America. Published by Oxford University Press. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.</rights><rights>2018 Crohn’s &amp; Colitis Foundation. Published by Oxford University Press. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com. 2018</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c408t-1e522f1306690f3ec364243e1abd78e39a6844ffae4df974567e06c0aef853f63</citedby><cites>FETCH-LOGICAL-c408t-1e522f1306690f3ec364243e1abd78e39a6844ffae4df974567e06c0aef853f63</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,776,780,881,1578,27901,27902</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/29361089$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Reinoso Webb, Cynthia</creatorcontrib><creatorcontrib>den Bakker, Hendrik</creatorcontrib><creatorcontrib>Koboziev, Iurii</creatorcontrib><creatorcontrib>Jones-Hall, Yava</creatorcontrib><creatorcontrib>Rao Kottapalli, Kameswara</creatorcontrib><creatorcontrib>Ostanin, Dmitry</creatorcontrib><creatorcontrib>Furr, Kathryn L</creatorcontrib><creatorcontrib>Mu, Qinghui</creatorcontrib><creatorcontrib>Luo, Xin M</creatorcontrib><creatorcontrib>Grisham, Matthew B</creatorcontrib><title>Differential Susceptibility to T Cell-Induced Colitis in Mice: Role of the Intestinal Microbiota</title><title>Inflammatory bowel diseases</title><addtitle>Inflamm Bowel Dis</addtitle><description>Abstract One of the best characterized mouse models of the inflammatory bowel diseases (IBD; Crohn's disease, ulcerative colitis) is the CD4+CD45RBhigh T cell transfer model of chronic colitis. Following our relocation to Texas Tech University Health Sciences Center (TTUHSC), we observed a dramatic reduction in the incidence of moderate-to-severe colitis from a 16-year historical average of 90% at Louisiana State University Health Sciences Center (LSUHSC) to &lt;30% at TTUHSC. We hypothesized that differences in the commensal microbiota at the 2 institutions may account for the differences in susceptibility to T cell-induced colitis. Using bioinformatic analyses of 16S rRNA amplicon sequence data, we quantified and compared the major microbial populations in feces from healthy and colitic mice housed at the 2 institutions. We found that the bacterial composition differed greatly between mice housed at LSUHSC vs TTUHSC. We identified several genera strongly associated with, and signficantly overrepresented in high responding RAG-/- mice housed at LSUHSC. In addition, we found that colonization of healthy TTUHSC RAG-/- mice with feces obtained from healthy or colitic RAG-/- mice housed at LSUHSC transferred susceptibility to T cell-induced colitis such that the recipients developed chronic colitis with incidence and severity similar to mice generated at LSUHSC. Finally, we found that the treatment of mice with preexisting colitis with antibiotics remarkably attenuated disease. Taken together, our data demonstrate that specific microbial communities determine disease susceptibility and that manipulation of the intestinal microbiota alters the induction and/or perpetuation of chronic colitis.</description><subject>Adoptive Transfer</subject><subject>Animals</subject><subject>Anti-Bacterial Agents - pharmacology</subject><subject>Bacteria - classification</subject><subject>Basic Science Research</subject><subject>Colitis - immunology</subject><subject>Colitis - microbiology</subject><subject>Colon - drug effects</subject><subject>Colon - pathology</subject><subject>Disease Models, Animal</subject><subject>Feces - microbiology</subject><subject>Gastrointestinal Microbiome - drug effects</subject><subject>Gastrointestinal Microbiome - immunology</subject><subject>Male</subject><subject>Mice</subject><subject>Mice, Inbred C57BL</subject><subject>Mice, Knockout</subject><subject>RNA, Ribosomal, 16S - genetics</subject><subject>T-Lymphocytes - immunology</subject><issn>1078-0998</issn><issn>1536-4844</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2018</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kV-L1DAUxYO4OOPoix9A8iKI0J2kSdPEB0Hqnx0YEXR8jml740QyzWyTLrv76Y10dllfJA83cH6cm5OD0AtKzilRbO3afu1urwnlj9CSVkwUXHL-ON9JLQuilFygpzH-JqTMRz1Bi1IxQYlUS_Tzg7MWRhiSMx5_n2IHx-Ra5126wSngHW7A-2Iz9FMHPW5CFlzEbsBfXAdv8bfgAQeL0x7wZkgQkxuyURbH0LqQzDN0Zo2P8Pw0V-jHp4-75qLYfv28ad5vi44TmQoKVVlayogQilgGHRO85AyoaftaAlNG5EzWGuC9VTWvRA1EdMSAlRWzgq3Qu9n3OLUH6LucaDReH0d3MOONDsbpf5XB7fWvcKUFrYVUKhu8PhmM4XLKQfTB5d_w3gwQpqipUkRWZV2XGX0zozlkjCPY-zWU6L-V6FyJnivJ8MuHD7tH7zrIwKsZCNPxf0Z_AOxelhs</recordid><startdate>20180118</startdate><enddate>20180118</enddate><creator>Reinoso Webb, Cynthia</creator><creator>den Bakker, Hendrik</creator><creator>Koboziev, Iurii</creator><creator>Jones-Hall, Yava</creator><creator>Rao Kottapalli, Kameswara</creator><creator>Ostanin, Dmitry</creator><creator>Furr, Kathryn L</creator><creator>Mu, Qinghui</creator><creator>Luo, Xin M</creator><creator>Grisham, Matthew B</creator><general>Oxford University Press</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>7X8</scope><scope>5PM</scope></search><sort><creationdate>20180118</creationdate><title>Differential Susceptibility to T Cell-Induced Colitis in Mice: Role of the Intestinal Microbiota</title><author>Reinoso Webb, Cynthia ; den Bakker, Hendrik ; Koboziev, Iurii ; Jones-Hall, Yava ; Rao Kottapalli, Kameswara ; Ostanin, Dmitry ; Furr, Kathryn L ; Mu, Qinghui ; Luo, Xin M ; Grisham, Matthew B</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c408t-1e522f1306690f3ec364243e1abd78e39a6844ffae4df974567e06c0aef853f63</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2018</creationdate><topic>Adoptive Transfer</topic><topic>Animals</topic><topic>Anti-Bacterial Agents - pharmacology</topic><topic>Bacteria - classification</topic><topic>Basic Science Research</topic><topic>Colitis - immunology</topic><topic>Colitis - microbiology</topic><topic>Colon - drug effects</topic><topic>Colon - pathology</topic><topic>Disease Models, Animal</topic><topic>Feces - microbiology</topic><topic>Gastrointestinal Microbiome - drug effects</topic><topic>Gastrointestinal Microbiome - immunology</topic><topic>Male</topic><topic>Mice</topic><topic>Mice, Inbred C57BL</topic><topic>Mice, Knockout</topic><topic>RNA, Ribosomal, 16S - genetics</topic><topic>T-Lymphocytes - immunology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Reinoso Webb, Cynthia</creatorcontrib><creatorcontrib>den Bakker, Hendrik</creatorcontrib><creatorcontrib>Koboziev, Iurii</creatorcontrib><creatorcontrib>Jones-Hall, Yava</creatorcontrib><creatorcontrib>Rao Kottapalli, Kameswara</creatorcontrib><creatorcontrib>Ostanin, Dmitry</creatorcontrib><creatorcontrib>Furr, Kathryn L</creatorcontrib><creatorcontrib>Mu, Qinghui</creatorcontrib><creatorcontrib>Luo, Xin M</creatorcontrib><creatorcontrib>Grisham, Matthew B</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>PubMed Central (Full Participant titles)</collection><jtitle>Inflammatory bowel diseases</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Reinoso Webb, Cynthia</au><au>den Bakker, Hendrik</au><au>Koboziev, Iurii</au><au>Jones-Hall, Yava</au><au>Rao Kottapalli, Kameswara</au><au>Ostanin, Dmitry</au><au>Furr, Kathryn L</au><au>Mu, Qinghui</au><au>Luo, Xin M</au><au>Grisham, Matthew B</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Differential Susceptibility to T Cell-Induced Colitis in Mice: Role of the Intestinal Microbiota</atitle><jtitle>Inflammatory bowel diseases</jtitle><addtitle>Inflamm Bowel Dis</addtitle><date>2018-01-18</date><risdate>2018</risdate><volume>24</volume><issue>2</issue><spage>361</spage><epage>379</epage><pages>361-379</pages><issn>1078-0998</issn><eissn>1536-4844</eissn><abstract>Abstract One of the best characterized mouse models of the inflammatory bowel diseases (IBD; Crohn's disease, ulcerative colitis) is the CD4+CD45RBhigh T cell transfer model of chronic colitis. Following our relocation to Texas Tech University Health Sciences Center (TTUHSC), we observed a dramatic reduction in the incidence of moderate-to-severe colitis from a 16-year historical average of 90% at Louisiana State University Health Sciences Center (LSUHSC) to &lt;30% at TTUHSC. We hypothesized that differences in the commensal microbiota at the 2 institutions may account for the differences in susceptibility to T cell-induced colitis. Using bioinformatic analyses of 16S rRNA amplicon sequence data, we quantified and compared the major microbial populations in feces from healthy and colitic mice housed at the 2 institutions. We found that the bacterial composition differed greatly between mice housed at LSUHSC vs TTUHSC. We identified several genera strongly associated with, and signficantly overrepresented in high responding RAG-/- mice housed at LSUHSC. In addition, we found that colonization of healthy TTUHSC RAG-/- mice with feces obtained from healthy or colitic RAG-/- mice housed at LSUHSC transferred susceptibility to T cell-induced colitis such that the recipients developed chronic colitis with incidence and severity similar to mice generated at LSUHSC. Finally, we found that the treatment of mice with preexisting colitis with antibiotics remarkably attenuated disease. Taken together, our data demonstrate that specific microbial communities determine disease susceptibility and that manipulation of the intestinal microbiota alters the induction and/or perpetuation of chronic colitis.</abstract><cop>US</cop><pub>Oxford University Press</pub><pmid>29361089</pmid><doi>10.1093/ibd/izx014</doi><tpages>19</tpages><oa>free_for_read</oa></addata></record>
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source Oxford University Press Journals All Titles (1996-Current); MEDLINE
subjects Adoptive Transfer
Animals
Anti-Bacterial Agents - pharmacology
Bacteria - classification
Basic Science Research
Colitis - immunology
Colitis - microbiology
Colon - drug effects
Colon - pathology
Disease Models, Animal
Feces - microbiology
Gastrointestinal Microbiome - drug effects
Gastrointestinal Microbiome - immunology
Male
Mice
Mice, Inbred C57BL
Mice, Knockout
RNA, Ribosomal, 16S - genetics
T-Lymphocytes - immunology
title Differential Susceptibility to T Cell-Induced Colitis in Mice: Role of the Intestinal Microbiota
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