Intestinal, extra-intestinal and systemic sequelae of Toxoplasma gondii induced acute ileitis in mice harboring a human gut microbiota
Within seven days following peroral high dose infection with Toxoplasma gondii susceptible conventionally colonized mice develop acute ileitis due to an underlying T helper cell (Th) -1 type immunopathology. We here addressed whether mice harboring a human intestinal microbiota developed intestinal,...
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| creator | von Klitzing, Eliane Ekmekciu, Ira Kühl, Anja A Bereswill, Stefan Heimesaat, Markus M |
| description | Within seven days following peroral high dose infection with Toxoplasma gondii susceptible conventionally colonized mice develop acute ileitis due to an underlying T helper cell (Th) -1 type immunopathology. We here addressed whether mice harboring a human intestinal microbiota developed intestinal, extra-intestinal and systemic sequelae upon ileitis induction.
Secondary abiotic mice were generated by broad-spectrum antibiotic treatment and associated with a complex human intestinal microbiota following peroral fecal microbiota transplantation. Within three weeks the human microbiota had stably established in the murine intestinal tract as assessed by quantitative cultural and culture-independent (i.e. molecular 16S rRNA based) methods. At day 7 post infection (p.i.) with 50 cysts of T. gondii strain ME49 by gavage human microbiota associated (hma) mice displayed severe clinical, macroscopic and microscopic sequelae indicating acute ileitis. In diseased hma mice increased numbers of innate and adaptive immune cells within the ileal mucosa and lamina propria and elevated intestinal secretion of pro-inflammatory mediators including IFN-γ, IL-12 and nitric oxide could be observed at day 7 p.i. Ileitis development was accompanied by substantial shifts in intestinal microbiota composition of hma mice characterized by elevated total bacterial loads and increased numbers of intestinal Gram-negative commensals such as enterobacteria and Bacteroides / Prevotella species overgrowing the small and large intestinal lumen. Furthermore, viable bacteria translocated from the inflamed ileum to extra-intestinal including systemic compartments. Notably, pro-inflammatory immune responses were not restricted to the intestinal tract as indicated by increased pro-inflammatory cytokine secretion in extra-intestinal (i.e. liver and kidney) and systemic compartments including spleen and serum.
With respect to the intestinal microbiota composition "humanized" mice display acute ileitis following peroral high dose T. gondii infection. Thus, hma mice constitute a suitable model to further dissect the interactions between pathogens, human microbiota and vertebrate host immunity during acute intestinal inflammation. |
| doi_str_mv | 10.1371/journal.pone.0176144 |
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Secondary abiotic mice were generated by broad-spectrum antibiotic treatment and associated with a complex human intestinal microbiota following peroral fecal microbiota transplantation. Within three weeks the human microbiota had stably established in the murine intestinal tract as assessed by quantitative cultural and culture-independent (i.e. molecular 16S rRNA based) methods. At day 7 post infection (p.i.) with 50 cysts of T. gondii strain ME49 by gavage human microbiota associated (hma) mice displayed severe clinical, macroscopic and microscopic sequelae indicating acute ileitis. In diseased hma mice increased numbers of innate and adaptive immune cells within the ileal mucosa and lamina propria and elevated intestinal secretion of pro-inflammatory mediators including IFN-γ, IL-12 and nitric oxide could be observed at day 7 p.i. Ileitis development was accompanied by substantial shifts in intestinal microbiota composition of hma mice characterized by elevated total bacterial loads and increased numbers of intestinal Gram-negative commensals such as enterobacteria and Bacteroides / Prevotella species overgrowing the small and large intestinal lumen. Furthermore, viable bacteria translocated from the inflamed ileum to extra-intestinal including systemic compartments. Notably, pro-inflammatory immune responses were not restricted to the intestinal tract as indicated by increased pro-inflammatory cytokine secretion in extra-intestinal (i.e. liver and kidney) and systemic compartments including spleen and serum.
With respect to the intestinal microbiota composition "humanized" mice display acute ileitis following peroral high dose T. gondii infection. Thus, hma mice constitute a suitable model to further dissect the interactions between pathogens, human microbiota and vertebrate host immunity during acute intestinal inflammation.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0176144</identifier><identifier>PMID: 28414794</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Adaptive Immunity - immunology ; Animals ; Antibiotics ; Bacteria ; Bacterial Translocation - immunology ; Bacterial Translocation - physiology ; Biology and Life Sciences ; Compartments ; Composition ; Consortia ; Crohn's disease ; Crohns disease ; Cysts ; Cytokines ; Drug dosages ; E coli ; Experiments ; Fecal microflora ; Feces ; Female ; Gastroenterology ; Gastrointestinal Microbiome - immunology ; Gastrointestinal Microbiome - physiology ; Hygiene ; Ileitis - immunology ; Ileitis - microbiology ; Ileitis - parasitology ; Ileum - microbiology ; Ileum - parasitology ; Immune response ; Immune system ; Immunity, Innate - immunology ; Immunology ; Infections ; Inflammation ; Inflammation - immunology ; Inflammation - microbiology ; Inflammation - parasitology ; Inflammatory bowel disease ; Interferon-gamma - immunology ; Interleukin-12 - immunology ; Intestinal diseases ; Intestinal microflora ; Intestinal Mucosa - microbiology ; Intestinal Mucosa - parasitology ; Lymphocytes T ; Medicine ; Medicine and Health Sciences ; Mice ; Mice, Inbred C57BL ; Microbiology ; Microbiota (Symbiotic organisms) ; Microorganisms ; Nitric oxide ; Nitric Oxide - immunology ; Research and Analysis Methods ; RNA, Ribosomal, 16S - metabolism ; Toxoplasma ; Toxoplasma - immunology ; Toxoplasma - pathogenicity ; Vertebrates</subject><ispartof>PloS one, 2017-04, Vol.12 (4), p.e0176144-e0176144</ispartof><rights>COPYRIGHT 2017 Public Library of Science</rights><rights>2017 von Klitzing et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2017 von Klitzing et al 2017 von Klitzing et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c692t-7571f69646550d32d7447d5c00fd578ab63752d904637d94afbd42ec07f390053</citedby><cites>FETCH-LOGICAL-c692t-7571f69646550d32d7447d5c00fd578ab63752d904637d94afbd42ec07f390053</cites><orcidid>0000-0001-6399-651X</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5393883/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5393883/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79343,79344</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28414794$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>von Klitzing, Eliane</creatorcontrib><creatorcontrib>Ekmekciu, Ira</creatorcontrib><creatorcontrib>Kühl, Anja A</creatorcontrib><creatorcontrib>Bereswill, Stefan</creatorcontrib><creatorcontrib>Heimesaat, Markus M</creatorcontrib><title>Intestinal, extra-intestinal and systemic sequelae of Toxoplasma gondii induced acute ileitis in mice harboring a human gut microbiota</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Within seven days following peroral high dose infection with Toxoplasma gondii susceptible conventionally colonized mice develop acute ileitis due to an underlying T helper cell (Th) -1 type immunopathology. We here addressed whether mice harboring a human intestinal microbiota developed intestinal, extra-intestinal and systemic sequelae upon ileitis induction.
Secondary abiotic mice were generated by broad-spectrum antibiotic treatment and associated with a complex human intestinal microbiota following peroral fecal microbiota transplantation. Within three weeks the human microbiota had stably established in the murine intestinal tract as assessed by quantitative cultural and culture-independent (i.e. molecular 16S rRNA based) methods. At day 7 post infection (p.i.) with 50 cysts of T. gondii strain ME49 by gavage human microbiota associated (hma) mice displayed severe clinical, macroscopic and microscopic sequelae indicating acute ileitis. In diseased hma mice increased numbers of innate and adaptive immune cells within the ileal mucosa and lamina propria and elevated intestinal secretion of pro-inflammatory mediators including IFN-γ, IL-12 and nitric oxide could be observed at day 7 p.i. Ileitis development was accompanied by substantial shifts in intestinal microbiota composition of hma mice characterized by elevated total bacterial loads and increased numbers of intestinal Gram-negative commensals such as enterobacteria and Bacteroides / Prevotella species overgrowing the small and large intestinal lumen. Furthermore, viable bacteria translocated from the inflamed ileum to extra-intestinal including systemic compartments. Notably, pro-inflammatory immune responses were not restricted to the intestinal tract as indicated by increased pro-inflammatory cytokine secretion in extra-intestinal (i.e. liver and kidney) and systemic compartments including spleen and serum.
With respect to the intestinal microbiota composition "humanized" mice display acute ileitis following peroral high dose T. gondii infection. Thus, hma mice constitute a suitable model to further dissect the interactions between pathogens, human microbiota and vertebrate host immunity during acute intestinal inflammation.</description><subject>Adaptive Immunity - immunology</subject><subject>Animals</subject><subject>Antibiotics</subject><subject>Bacteria</subject><subject>Bacterial Translocation - immunology</subject><subject>Bacterial Translocation - physiology</subject><subject>Biology and Life Sciences</subject><subject>Compartments</subject><subject>Composition</subject><subject>Consortia</subject><subject>Crohn's disease</subject><subject>Crohns disease</subject><subject>Cysts</subject><subject>Cytokines</subject><subject>Drug dosages</subject><subject>E coli</subject><subject>Experiments</subject><subject>Fecal microflora</subject><subject>Feces</subject><subject>Female</subject><subject>Gastroenterology</subject><subject>Gastrointestinal Microbiome - immunology</subject><subject>Gastrointestinal Microbiome - physiology</subject><subject>Hygiene</subject><subject>Ileitis - immunology</subject><subject>Ileitis - microbiology</subject><subject>Ileitis - parasitology</subject><subject>Ileum - microbiology</subject><subject>Ileum - parasitology</subject><subject>Immune response</subject><subject>Immune system</subject><subject>Immunity, Innate - immunology</subject><subject>Immunology</subject><subject>Infections</subject><subject>Inflammation</subject><subject>Inflammation - immunology</subject><subject>Inflammation - microbiology</subject><subject>Inflammation - parasitology</subject><subject>Inflammatory bowel disease</subject><subject>Interferon-gamma - immunology</subject><subject>Interleukin-12 - immunology</subject><subject>Intestinal diseases</subject><subject>Intestinal microflora</subject><subject>Intestinal Mucosa - microbiology</subject><subject>Intestinal Mucosa - parasitology</subject><subject>Lymphocytes T</subject><subject>Medicine</subject><subject>Medicine and Health Sciences</subject><subject>Mice</subject><subject>Mice, Inbred C57BL</subject><subject>Microbiology</subject><subject>Microbiota (Symbiotic organisms)</subject><subject>Microorganisms</subject><subject>Nitric oxide</subject><subject>Nitric Oxide - immunology</subject><subject>Research and Analysis Methods</subject><subject>RNA, Ribosomal, 16S - metabolism</subject><subject>Toxoplasma</subject><subject>Toxoplasma - immunology</subject><subject>Toxoplasma - pathogenicity</subject><subject>Vertebrates</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><sourceid>DOA</sourceid><recordid>eNqNk11rFDEUhgdRbK3-A9GAIArumkwy-bgRSvFjoVDQ6m3ITJLZlNlkO8lI-wf83Wa602VHeiFzMeHkOW9y3pxTFC8RXCLM0MerMPRedctt8GYJEaOIkEfFMRK4XNAS4scH66PiWYxXEFaYU_q0OCo5QYQJclz8WflkYnJZ6QMwN6lXC7ePAOU1iLcxmY1rQDTXg-mUAcGCy3ATtp2KGwXa4LVzwHk9NEYD1QzJANcZl1zMUZBTDVirvg698y1QYD1slAftkMatPtQuJPW8eGJVF82L6X9S_Pzy-fLs2-L84uvq7PR80VBRpgWrGLJUUEKrCmpcakYI01UDodUV46qmmFWlFpDkhRZE2VqT0jSQWSzG8k-K1zvdbReinCyMEnHOBWEl45lY7Qgd1JXc9m6j-lsZlJN3gdC3UvXJNZ2RhNqKG2JKqEpiCRIGYmORrSmCtK5Q1vo0nTbUG6Mb47O_3Ux0vuPdWrbht6ywwJzjLPBuEuhDNj8muXGxMV2nvAnD3b0zSHA1om_-QR-ubqJalQtw3oZ8bjOKylPCBS8pE6PW8gEqf3pshNxvNr_vPOH9LCEzKTdTq4YY5erH9_9nL37N2bcH7NqoLq1j6Ibkgo9zkOzA3FAx9sbuTUZQjuNy74Ycx0VO45LTXh0-0D7pfj7wX9y1EOo</recordid><startdate>20170417</startdate><enddate>20170417</enddate><creator>von Klitzing, Eliane</creator><creator>Ekmekciu, Ira</creator><creator>Kühl, Anja A</creator><creator>Bereswill, Stefan</creator><creator>Heimesaat, Markus M</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</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>IOV</scope><scope>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0001-6399-651X</orcidid></search><sort><creationdate>20170417</creationdate><title>Intestinal, extra-intestinal and systemic sequelae of Toxoplasma gondii induced acute ileitis in mice harboring a human gut microbiota</title><author>von Klitzing, Eliane ; Ekmekciu, Ira ; Kühl, Anja A ; Bereswill, Stefan ; Heimesaat, Markus M</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c692t-7571f69646550d32d7447d5c00fd578ab63752d904637d94afbd42ec07f390053</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>Adaptive Immunity - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>von Klitzing, Eliane</au><au>Ekmekciu, Ira</au><au>Kühl, Anja A</au><au>Bereswill, Stefan</au><au>Heimesaat, Markus M</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Intestinal, extra-intestinal and systemic sequelae of Toxoplasma gondii induced acute ileitis in mice harboring a human gut microbiota</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2017-04-17</date><risdate>2017</risdate><volume>12</volume><issue>4</issue><spage>e0176144</spage><epage>e0176144</epage><pages>e0176144-e0176144</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Within seven days following peroral high dose infection with Toxoplasma gondii susceptible conventionally colonized mice develop acute ileitis due to an underlying T helper cell (Th) -1 type immunopathology. We here addressed whether mice harboring a human intestinal microbiota developed intestinal, extra-intestinal and systemic sequelae upon ileitis induction.
Secondary abiotic mice were generated by broad-spectrum antibiotic treatment and associated with a complex human intestinal microbiota following peroral fecal microbiota transplantation. Within three weeks the human microbiota had stably established in the murine intestinal tract as assessed by quantitative cultural and culture-independent (i.e. molecular 16S rRNA based) methods. At day 7 post infection (p.i.) with 50 cysts of T. gondii strain ME49 by gavage human microbiota associated (hma) mice displayed severe clinical, macroscopic and microscopic sequelae indicating acute ileitis. In diseased hma mice increased numbers of innate and adaptive immune cells within the ileal mucosa and lamina propria and elevated intestinal secretion of pro-inflammatory mediators including IFN-γ, IL-12 and nitric oxide could be observed at day 7 p.i. Ileitis development was accompanied by substantial shifts in intestinal microbiota composition of hma mice characterized by elevated total bacterial loads and increased numbers of intestinal Gram-negative commensals such as enterobacteria and Bacteroides / Prevotella species overgrowing the small and large intestinal lumen. Furthermore, viable bacteria translocated from the inflamed ileum to extra-intestinal including systemic compartments. Notably, pro-inflammatory immune responses were not restricted to the intestinal tract as indicated by increased pro-inflammatory cytokine secretion in extra-intestinal (i.e. liver and kidney) and systemic compartments including spleen and serum.
With respect to the intestinal microbiota composition "humanized" mice display acute ileitis following peroral high dose T. gondii infection. Thus, hma mice constitute a suitable model to further dissect the interactions between pathogens, human microbiota and vertebrate host immunity during acute intestinal inflammation.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>28414794</pmid><doi>10.1371/journal.pone.0176144</doi><tpages>e0176144</tpages><orcidid>https://orcid.org/0000-0001-6399-651X</orcidid><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1932-6203 |
| ispartof | PloS one, 2017-04, Vol.12 (4), p.e0176144-e0176144 |
| issn | 1932-6203 1932-6203 |
| language | eng |
| recordid | cdi_plos_journals_1888947278 |
| source | MEDLINE; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central; Free Full-Text Journals in Chemistry; Public Library of Science (PLoS) |
| subjects | Adaptive Immunity - immunology Animals Antibiotics Bacteria Bacterial Translocation - immunology Bacterial Translocation - physiology Biology and Life Sciences Compartments Composition Consortia Crohn's disease Crohns disease Cysts Cytokines Drug dosages E coli Experiments Fecal microflora Feces Female Gastroenterology Gastrointestinal Microbiome - immunology Gastrointestinal Microbiome - physiology Hygiene Ileitis - immunology Ileitis - microbiology Ileitis - parasitology Ileum - microbiology Ileum - parasitology Immune response Immune system Immunity, Innate - immunology Immunology Infections Inflammation Inflammation - immunology Inflammation - microbiology Inflammation - parasitology Inflammatory bowel disease Interferon-gamma - immunology Interleukin-12 - immunology Intestinal diseases Intestinal microflora Intestinal Mucosa - microbiology Intestinal Mucosa - parasitology Lymphocytes T Medicine Medicine and Health Sciences Mice Mice, Inbred C57BL Microbiology Microbiota (Symbiotic organisms) Microorganisms Nitric oxide Nitric Oxide - immunology Research and Analysis Methods RNA, Ribosomal, 16S - metabolism Toxoplasma Toxoplasma - immunology Toxoplasma - pathogenicity Vertebrates |
| title | Intestinal, extra-intestinal and systemic sequelae of Toxoplasma gondii induced acute ileitis in mice harboring a human gut microbiota |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-02T17%3A22%3A09IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Intestinal,%20extra-intestinal%20and%20systemic%20sequelae%20of%20Toxoplasma%20gondii%20induced%20acute%20ileitis%20in%20mice%20harboring%20a%20human%20gut%20microbiota&rft.jtitle=PloS%20one&rft.au=von%20Klitzing,%20Eliane&rft.date=2017-04-17&rft.volume=12&rft.issue=4&rft.spage=e0176144&rft.epage=e0176144&rft.pages=e0176144-e0176144&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0176144&rft_dat=%3Cgale_plos_%3EA489826793%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1888947278&rft_id=info:pmid/28414794&rft_galeid=A489826793&rft_doaj_id=oai_doaj_org_article_46f58e4e20a24f419e03ef1fb6106b51&rfr_iscdi=true |