Characterisation of early mucosal and neuronal lesions following Shigella flexneri infection in human colon
Shigella, an enteroinvasive bacteria induces a major inflammatory response responsible for acute rectocolitis in humans. However, early effect of Shigella flexneri (S. flexneri) infection upon the human mucosa and its microenvironement, in particular the enteric nervous system, remains currently unk...
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| Veröffentlicht in: | PloS one 2009-03, Vol.4 (3), p.e4713-e4713 |
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| creator | Coron, Emmanuel Flamant, Mathurin Aubert, Philippe Wedel, Thilo Pedron, Thierry Letessier, Eric Galmiche, Jean P Sansonetti, Philippe J Neunlist, Michel |
| description | Shigella, an enteroinvasive bacteria induces a major inflammatory response responsible for acute rectocolitis in humans. However, early effect of Shigella flexneri (S. flexneri) infection upon the human mucosa and its microenvironement, in particular the enteric nervous system, remains currently unknown. Therefore, in this study, we sought to characterize ex vivo the early events of shigellosis in a model of human colonic explants. In particular, we aimed at identifying factors produced by S. flexneri and responsible for the lesions of the barrier. We also aimed at determining the putative lesions of the enteric nervous system induced by S. flexneri.
We first showed that, following 3 h of infection, the invasive but not the non-invasive strain of S. flexneri induced significant desquamation of the intestinal epithelial barrier and a reduction of epithelial height. These changes were significantly reduced following infection with SepA deficient S. flexneri strains. Secondly, S. flexneri induced rapid neuronal morphological alterations suggestive of cell death in enteric submucosal neurones. These alterations were associated with a significant increase in the proportion of vasoactive intestinal peptide (VIP) immunoreactive (IR) neurons but not in total VIP levels. The NMDA receptor antagonist MK-801 blocked neuronal morphological changes induced by S. flexneri, but not the increase in the proportion of VIP-IR.
This human explant model can be used to gain better insight into the early pathogenic events following S. flexneri infection and the mechanisms involved. |
| doi_str_mv | 10.1371/journal.pone.0004713 |
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We first showed that, following 3 h of infection, the invasive but not the non-invasive strain of S. flexneri induced significant desquamation of the intestinal epithelial barrier and a reduction of epithelial height. These changes were significantly reduced following infection with SepA deficient S. flexneri strains. Secondly, S. flexneri induced rapid neuronal morphological alterations suggestive of cell death in enteric submucosal neurones. These alterations were associated with a significant increase in the proportion of vasoactive intestinal peptide (VIP) immunoreactive (IR) neurons but not in total VIP levels. The NMDA receptor antagonist MK-801 blocked neuronal morphological changes induced by S. flexneri, but not the increase in the proportion of VIP-IR.
This human explant model can be used to gain better insight into the early pathogenic events following S. flexneri infection and the mechanisms involved.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0004713</identifier><identifier>PMID: 19274103</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Adult ; Aged ; Aged, 80 and over ; Bacteria ; Cell death ; Colon ; Colonic Diseases - microbiology ; Colonic Diseases - pathology ; Cytokines ; Dizocilpine ; Dysentery, Bacillary - microbiology ; Dysentery, Bacillary - pathology ; Enteric nervous system ; Enteric Nervous System - pathology ; Epithelium - pathology ; Explants ; Gastroenterology and Hepatology/Disorders of Neurogastroenterology and Motility ; Genotype & phenotype ; Glutamic acid receptors (ionotropic) ; Health aspects ; Humans ; Infection ; Infections ; Infectious Diseases/Gastrointestinal Infections ; Infectious Diseases/Infectious Diseases of the Nervous System ; Inflammation ; Inflammatory bowel disease ; Inflammatory response ; Intestinal Mucosa - pathology ; Intestine ; Irritable bowel syndrome ; Ischemia ; Lesions ; Middle Aged ; Motility ; Mucosa ; N-Methyl-D-aspartic acid receptors ; Nervous system ; Neurons ; Neurons - pathology ; Pathogenesis ; Rodents ; Shigella ; Shigella flexneri ; Shigellosis ; Transcription factors ; Vasoactive agents ; Vasoactive Intestinal Peptide ; Vasoactive intestinal peptides ; Young Adult</subject><ispartof>PloS one, 2009-03, Vol.4 (3), p.e4713-e4713</ispartof><rights>COPYRIGHT 2009 Public Library of Science</rights><rights>2009 Coron et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License (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>Coron et al. 2009</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c662t-35907b3ff6c43f17ab2e8c7d95c17c76ad799c2b6b455050c2d70f423d83ae5f3</citedby><cites>FETCH-LOGICAL-c662t-35907b3ff6c43f17ab2e8c7d95c17c76ad799c2b6b455050c2d70f423d83ae5f3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC2653194/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC2653194/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79342,79343</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/19274103$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Coron, Emmanuel</creatorcontrib><creatorcontrib>Flamant, Mathurin</creatorcontrib><creatorcontrib>Aubert, Philippe</creatorcontrib><creatorcontrib>Wedel, Thilo</creatorcontrib><creatorcontrib>Pedron, Thierry</creatorcontrib><creatorcontrib>Letessier, Eric</creatorcontrib><creatorcontrib>Galmiche, Jean P</creatorcontrib><creatorcontrib>Sansonetti, Philippe J</creatorcontrib><creatorcontrib>Neunlist, Michel</creatorcontrib><title>Characterisation of early mucosal and neuronal lesions following Shigella flexneri infection in human colon</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Shigella, an enteroinvasive bacteria induces a major inflammatory response responsible for acute rectocolitis in humans. However, early effect of Shigella flexneri (S. flexneri) infection upon the human mucosa and its microenvironement, in particular the enteric nervous system, remains currently unknown. Therefore, in this study, we sought to characterize ex vivo the early events of shigellosis in a model of human colonic explants. In particular, we aimed at identifying factors produced by S. flexneri and responsible for the lesions of the barrier. We also aimed at determining the putative lesions of the enteric nervous system induced by S. flexneri.
We first showed that, following 3 h of infection, the invasive but not the non-invasive strain of S. flexneri induced significant desquamation of the intestinal epithelial barrier and a reduction of epithelial height. These changes were significantly reduced following infection with SepA deficient S. flexneri strains. Secondly, S. flexneri induced rapid neuronal morphological alterations suggestive of cell death in enteric submucosal neurones. These alterations were associated with a significant increase in the proportion of vasoactive intestinal peptide (VIP) immunoreactive (IR) neurons but not in total VIP levels. The NMDA receptor antagonist MK-801 blocked neuronal morphological changes induced by S. flexneri, but not the increase in the proportion of VIP-IR.
This human explant model can be used to gain better insight into the early pathogenic events following S. flexneri infection and the mechanisms involved.</description><subject>Adult</subject><subject>Aged</subject><subject>Aged, 80 and over</subject><subject>Bacteria</subject><subject>Cell death</subject><subject>Colon</subject><subject>Colonic Diseases - microbiology</subject><subject>Colonic Diseases - pathology</subject><subject>Cytokines</subject><subject>Dizocilpine</subject><subject>Dysentery, Bacillary - microbiology</subject><subject>Dysentery, Bacillary - pathology</subject><subject>Enteric nervous system</subject><subject>Enteric Nervous System - pathology</subject><subject>Epithelium - pathology</subject><subject>Explants</subject><subject>Gastroenterology and Hepatology/Disorders of Neurogastroenterology and Motility</subject><subject>Genotype & phenotype</subject><subject>Glutamic acid receptors (ionotropic)</subject><subject>Health aspects</subject><subject>Humans</subject><subject>Infection</subject><subject>Infections</subject><subject>Infectious Diseases/Gastrointestinal Infections</subject><subject>Infectious Diseases/Infectious Diseases of the Nervous System</subject><subject>Inflammation</subject><subject>Inflammatory bowel disease</subject><subject>Inflammatory response</subject><subject>Intestinal Mucosa - pathology</subject><subject>Intestine</subject><subject>Irritable bowel syndrome</subject><subject>Ischemia</subject><subject>Lesions</subject><subject>Middle Aged</subject><subject>Motility</subject><subject>Mucosa</subject><subject>N-Methyl-D-aspartic acid receptors</subject><subject>Nervous system</subject><subject>Neurons</subject><subject>Neurons - pathology</subject><subject>Pathogenesis</subject><subject>Rodents</subject><subject>Shigella</subject><subject>Shigella flexneri</subject><subject>Shigellosis</subject><subject>Transcription factors</subject><subject>Vasoactive agents</subject><subject>Vasoactive Intestinal Peptide</subject><subject>Vasoactive intestinal peptides</subject><subject>Young Adult</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2009</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><sourceid>DOA</sourceid><recordid>eNqNkl2L1DAUhoso7rr6D0QLwoIXM-arTXsjLIMfAwsLrnob0vSkzZgms0mru__ezE7VGfFCcpFw8pz35Jy8WfYcoyWmHL_Z-Ck4aZdb72CJEGIc0wfZKa4pWZQE0YcH55PsSYwbhApaleXj7ATXhDOM6Gn2bdXLINUIwUQ5Gu9yr3OQwd7lw6R8lDaXrs0dTMGnarmFmKCYa2-t_2Fcl1_3pgNrZa4t3LqkkxunQd1rGZf30yBdrrz17mn2SEsb4dm8n2Vf3r_7vPq4uLz6sF5dXC5UWZJxQYsa8YZqXSpGNeayIVAp3taFwlzxUra8rhVpyoYVBSqQIi1HmhHaVlRCoelZ9nKvu7U-inlOUWBSI1rgCuFErPdE6-VGbIMZZLgTXhpxH_ChEzKMRlkQRDHMa41I1TJWIahx0yigNRCkGFCStN7O1aZmgFaBG4O0R6LHN870ovPfBSkLimuWBM5ngeBvJoijGExUu5E68FMUJUeYcV4k8NVf4L97W-6pTqbnp7_wqapKq4XBqGQWbVL8gnFKK5KclBJeHyUkZoTbsZNTjGJ9_en_2auvx-z5AduDtGMfvZ12zojHINuDKvgYA-jfw8NI7Lz-q0-x87qYvZ7SXhwO_k_SbG76EyE5-44</recordid><startdate>20090305</startdate><enddate>20090305</enddate><creator>Coron, Emmanuel</creator><creator>Flamant, Mathurin</creator><creator>Aubert, Philippe</creator><creator>Wedel, Thilo</creator><creator>Pedron, Thierry</creator><creator>Letessier, Eric</creator><creator>Galmiche, Jean P</creator><creator>Sansonetti, Philippe J</creator><creator>Neunlist, Michel</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></search><sort><creationdate>20090305</creationdate><title>Characterisation of early mucosal and neuronal lesions following Shigella flexneri infection in human colon</title><author>Coron, Emmanuel ; Flamant, Mathurin ; Aubert, Philippe ; Wedel, Thilo ; Pedron, Thierry ; Letessier, Eric ; Galmiche, Jean P ; Sansonetti, Philippe J ; Neunlist, Michel</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c662t-35907b3ff6c43f17ab2e8c7d95c17c76ad799c2b6b455050c2d70f423d83ae5f3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2009</creationdate><topic>Adult</topic><topic>Aged</topic><topic>Aged, 80 and over</topic><topic>Bacteria</topic><topic>Cell death</topic><topic>Colon</topic><topic>Colonic Diseases - 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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>Coron, Emmanuel</au><au>Flamant, Mathurin</au><au>Aubert, Philippe</au><au>Wedel, Thilo</au><au>Pedron, Thierry</au><au>Letessier, Eric</au><au>Galmiche, Jean P</au><au>Sansonetti, Philippe J</au><au>Neunlist, Michel</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Characterisation of early mucosal and neuronal lesions following Shigella flexneri infection in human colon</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2009-03-05</date><risdate>2009</risdate><volume>4</volume><issue>3</issue><spage>e4713</spage><epage>e4713</epage><pages>e4713-e4713</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Shigella, an enteroinvasive bacteria induces a major inflammatory response responsible for acute rectocolitis in humans. However, early effect of Shigella flexneri (S. flexneri) infection upon the human mucosa and its microenvironement, in particular the enteric nervous system, remains currently unknown. Therefore, in this study, we sought to characterize ex vivo the early events of shigellosis in a model of human colonic explants. In particular, we aimed at identifying factors produced by S. flexneri and responsible for the lesions of the barrier. We also aimed at determining the putative lesions of the enteric nervous system induced by S. flexneri.
We first showed that, following 3 h of infection, the invasive but not the non-invasive strain of S. flexneri induced significant desquamation of the intestinal epithelial barrier and a reduction of epithelial height. These changes were significantly reduced following infection with SepA deficient S. flexneri strains. Secondly, S. flexneri induced rapid neuronal morphological alterations suggestive of cell death in enteric submucosal neurones. These alterations were associated with a significant increase in the proportion of vasoactive intestinal peptide (VIP) immunoreactive (IR) neurons but not in total VIP levels. The NMDA receptor antagonist MK-801 blocked neuronal morphological changes induced by S. flexneri, but not the increase in the proportion of VIP-IR.
This human explant model can be used to gain better insight into the early pathogenic events following S. flexneri infection and the mechanisms involved.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>19274103</pmid><doi>10.1371/journal.pone.0004713</doi><tpages>e4713</tpages><oa>free_for_read</oa></addata></record> |
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| source | MEDLINE; DOAJ Directory of Open Access Journals; EZB-FREE-00999 freely available EZB journals; PubMed Central; Free Full-Text Journals in Chemistry; Public Library of Science (PLoS) |
| subjects | Adult Aged Aged, 80 and over Bacteria Cell death Colon Colonic Diseases - microbiology Colonic Diseases - pathology Cytokines Dizocilpine Dysentery, Bacillary - microbiology Dysentery, Bacillary - pathology Enteric nervous system Enteric Nervous System - pathology Epithelium - pathology Explants Gastroenterology and Hepatology/Disorders of Neurogastroenterology and Motility Genotype & phenotype Glutamic acid receptors (ionotropic) Health aspects Humans Infection Infections Infectious Diseases/Gastrointestinal Infections Infectious Diseases/Infectious Diseases of the Nervous System Inflammation Inflammatory bowel disease Inflammatory response Intestinal Mucosa - pathology Intestine Irritable bowel syndrome Ischemia Lesions Middle Aged Motility Mucosa N-Methyl-D-aspartic acid receptors Nervous system Neurons Neurons - pathology Pathogenesis Rodents Shigella Shigella flexneri Shigellosis Transcription factors Vasoactive agents Vasoactive Intestinal Peptide Vasoactive intestinal peptides Young Adult |
| title | Characterisation of early mucosal and neuronal lesions following Shigella flexneri infection in human colon |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-10T15%3A41%3A45IST&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=Characterisation%20of%20early%20mucosal%20and%20neuronal%20lesions%20following%20Shigella%20flexneri%20infection%20in%20human%20colon&rft.jtitle=PloS%20one&rft.au=Coron,%20Emmanuel&rft.date=2009-03-05&rft.volume=4&rft.issue=3&rft.spage=e4713&rft.epage=e4713&rft.pages=e4713-e4713&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0004713&rft_dat=%3Cgale_plos_%3EA473382137%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=1290351801&rft_id=info:pmid/19274103&rft_galeid=A473382137&rft_doaj_id=oai_doaj_org_article_2c4179f028d4480e91bbce39e20c4e32&rfr_iscdi=true |