Microbial Pattern Recognition Receptors Mediate M-Cell Uptake of a Gram-Negative Bacterium
The receptors involved in the sampling of particulate microbial antigens by the gut are largely unknown. Here we demonstrate for the first time in an in vitro M-cell model and in situ in isolated murine intestinal segments that the receptors TLR-4, PAF-R, and [alpha]5{szligbeta}1 integrin are all in...
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Veröffentlicht in: | Infection and Immunity 2006, Vol.74 (1), p.625-631 |
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description | The receptors involved in the sampling of particulate microbial antigens by the gut are largely unknown. Here we demonstrate for the first time in an in vitro M-cell model and in situ in isolated murine intestinal segments that the receptors TLR-4, PAF-R, and [alpha]5{szligbeta}1 integrin are all involved in mediating bacterial uptake associated with transcytosis. The pattern of expression of TLR-4 and [alpha]5{szligbeta}1 integrin differed between M cells and enterocytes. There was increased apical expression of TLR-4 in M-cell cultures, and it was present on the apical surface of murine M cells but not enterocytes in situ. In contrast, PAF-R was expressed equally by both cell types in vitro and was abundantly expressed throughout the intestinal epithelium. Inhibition of TLR-4 and PAF-R, but not TLR-2, reduced gram-negative bacterial uptake by both cell types, whereas inhibition of the apically expressed [alpha]5{szligbeta}1 integrin significantly reduced the ability of M cells to translocate bacteria. Hence, the involvement of each receptor was dependent not only on differences in the level of receptor expression but the cellular localization. Using bacteria that had mutations that affected the bacterial lipooligosaccharide structure indicated that the oligosaccharide moiety was important in bacterial uptake. Taken together, the data suggest that pathogen-associated molecular pattern interactions with pattern recognition receptors are key factors in M-cell recognition of intestinal antigens for mucosal immune priming. |
doi_str_mv | 10.1128/IAI.74.1.625-631.2006 |
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Ruth ; Cripps, Allan W ; Apicella, Michael A ; Kyd, Jennelle M</creator><creatorcontrib>Tyrer, Peter ; Foxwell, A. Ruth ; Cripps, Allan W ; Apicella, Michael A ; Kyd, Jennelle M</creatorcontrib><description>The receptors involved in the sampling of particulate microbial antigens by the gut are largely unknown. Here we demonstrate for the first time in an in vitro M-cell model and in situ in isolated murine intestinal segments that the receptors TLR-4, PAF-R, and [alpha]5{szligbeta}1 integrin are all involved in mediating bacterial uptake associated with transcytosis. The pattern of expression of TLR-4 and [alpha]5{szligbeta}1 integrin differed between M cells and enterocytes. There was increased apical expression of TLR-4 in M-cell cultures, and it was present on the apical surface of murine M cells but not enterocytes in situ. In contrast, PAF-R was expressed equally by both cell types in vitro and was abundantly expressed throughout the intestinal epithelium. Inhibition of TLR-4 and PAF-R, but not TLR-2, reduced gram-negative bacterial uptake by both cell types, whereas inhibition of the apically expressed [alpha]5{szligbeta}1 integrin significantly reduced the ability of M cells to translocate bacteria. Hence, the involvement of each receptor was dependent not only on differences in the level of receptor expression but the cellular localization. Using bacteria that had mutations that affected the bacterial lipooligosaccharide structure indicated that the oligosaccharide moiety was important in bacterial uptake. Taken together, the data suggest that pathogen-associated molecular pattern interactions with pattern recognition receptors are key factors in M-cell recognition of intestinal antigens for mucosal immune priming.</description><identifier>ISSN: 0019-9567</identifier><identifier>EISSN: 1098-5522</identifier><identifier>DOI: 10.1128/IAI.74.1.625-631.2006</identifier><identifier>PMID: 16369019</identifier><identifier>CODEN: INFIBR</identifier><language>eng</language><publisher>Washington, DC: American Society for Microbiology</publisher><subject>Animals ; Bacteria ; Biological and medical sciences ; Caco-2 Cells ; Cellular Microbiology: Pathogen-Host Cell Molecular Interactions ; Enterocytes - immunology ; Enterocytes - microbiology ; Fundamental and applied biological sciences. Psychology ; Haemophilus Infections - immunology ; Haemophilus influenzae - immunology ; Humans ; Intestinal Mucosa - cytology ; Intestinal Mucosa - metabolism ; Intestinal Mucosa - microbiology ; Lipopolysaccharides - chemistry ; Male ; Mice ; Mice, Inbred BALB C ; Microbiology ; Peyer's Patches - cytology ; Peyer's Patches - immunology ; Peyer's Patches - metabolism ; Peyer's Patches - microbiology ; Platelet Membrane Glycoproteins - physiology ; Receptors, G-Protein-Coupled - physiology ; Receptors, Pattern Recognition - physiology ; Toll-Like Receptor 4 - physiology</subject><ispartof>Infection and Immunity, 2006, Vol.74 (1), p.625-631</ispartof><rights>2006 INIST-CNRS</rights><rights>Copyright © 2006, American Society for Microbiology 2006</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c585t-c29eec33202392b627945f859da3971aa0e046b15ab76d8ecc399a47812ae9b93</citedby><cites>FETCH-LOGICAL-c585t-c29eec33202392b627945f859da3971aa0e046b15ab76d8ecc399a47812ae9b93</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/PMC1346623/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC1346623/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,727,780,784,885,3188,3189,4024,27923,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=17462430$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/16369019$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Tyrer, Peter</creatorcontrib><creatorcontrib>Foxwell, A. Ruth</creatorcontrib><creatorcontrib>Cripps, Allan W</creatorcontrib><creatorcontrib>Apicella, Michael A</creatorcontrib><creatorcontrib>Kyd, Jennelle M</creatorcontrib><title>Microbial Pattern Recognition Receptors Mediate M-Cell Uptake of a Gram-Negative Bacterium</title><title>Infection and Immunity</title><addtitle>Infect Immun</addtitle><description>The receptors involved in the sampling of particulate microbial antigens by the gut are largely unknown. Here we demonstrate for the first time in an in vitro M-cell model and in situ in isolated murine intestinal segments that the receptors TLR-4, PAF-R, and [alpha]5{szligbeta}1 integrin are all involved in mediating bacterial uptake associated with transcytosis. The pattern of expression of TLR-4 and [alpha]5{szligbeta}1 integrin differed between M cells and enterocytes. There was increased apical expression of TLR-4 in M-cell cultures, and it was present on the apical surface of murine M cells but not enterocytes in situ. In contrast, PAF-R was expressed equally by both cell types in vitro and was abundantly expressed throughout the intestinal epithelium. Inhibition of TLR-4 and PAF-R, but not TLR-2, reduced gram-negative bacterial uptake by both cell types, whereas inhibition of the apically expressed [alpha]5{szligbeta}1 integrin significantly reduced the ability of M cells to translocate bacteria. Hence, the involvement of each receptor was dependent not only on differences in the level of receptor expression but the cellular localization. Using bacteria that had mutations that affected the bacterial lipooligosaccharide structure indicated that the oligosaccharide moiety was important in bacterial uptake. 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Psychology</subject><subject>Haemophilus Infections - immunology</subject><subject>Haemophilus influenzae - immunology</subject><subject>Humans</subject><subject>Intestinal Mucosa - cytology</subject><subject>Intestinal Mucosa - metabolism</subject><subject>Intestinal Mucosa - microbiology</subject><subject>Lipopolysaccharides - chemistry</subject><subject>Male</subject><subject>Mice</subject><subject>Mice, Inbred BALB C</subject><subject>Microbiology</subject><subject>Peyer's Patches - cytology</subject><subject>Peyer's Patches - immunology</subject><subject>Peyer's Patches - metabolism</subject><subject>Peyer's Patches - microbiology</subject><subject>Platelet Membrane Glycoproteins - physiology</subject><subject>Receptors, G-Protein-Coupled - physiology</subject><subject>Receptors, Pattern Recognition - physiology</subject><subject>Toll-Like Receptor 4 - physiology</subject><issn>0019-9567</issn><issn>1098-5522</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2006</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkU1vEzEQhi0EomnhJwC-wG0Xf-_6glQiKJEaQEAuXKxZZzYx7Edqb1rx73FJoHBCPtijeeYdz7yEPOGs5FzULxfni7JSJS-N0IWRvBSMmXtkxpmtC62FuE9mjHFbWG2qE3Ka0rccKqXqh-SEG2lsTs7I12XwcWwCdPQjTBPGgX5CP26GMIXx1xt30xgTXeI6wIR0Wcyx6-hqN8F3pGNLgV5E6Iv3uIEpXCN9DT7LhH3_iDxooUv4-HifkdXbN1_m74rLDxeL-fll4XWtp8ILi-ilFExIKxojKqt0W2u7BmkrDsCQKdNwDU1l1jV6L60FVdVcANrGyjPy6qC72zc9rj0OU4TO7WLoIf5wIwT3b2YIW7cZrx2Xyhghs8CLo0Acr_aYJteH5POUMOC4T85Uus7t_g9yW1uTTwb1Acy7TSli--c3nLlb-1y2z1XKcZftc9k-d2tfrnv69yh3VUe_MvD8CEDy0LURBh_SHVcpI5RkmaMHbhs225sQ0UHqXcir-N00I88OSAujg03MMqvPgnHJeN63sFL-BFewt4Q</recordid><startdate>2006</startdate><enddate>2006</enddate><creator>Tyrer, Peter</creator><creator>Foxwell, A. 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Ruth</au><au>Cripps, Allan W</au><au>Apicella, Michael A</au><au>Kyd, Jennelle M</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Microbial Pattern Recognition Receptors Mediate M-Cell Uptake of a Gram-Negative Bacterium</atitle><jtitle>Infection and Immunity</jtitle><addtitle>Infect Immun</addtitle><date>2006</date><risdate>2006</risdate><volume>74</volume><issue>1</issue><spage>625</spage><epage>631</epage><pages>625-631</pages><issn>0019-9567</issn><eissn>1098-5522</eissn><coden>INFIBR</coden><abstract>The receptors involved in the sampling of particulate microbial antigens by the gut are largely unknown. Here we demonstrate for the first time in an in vitro M-cell model and in situ in isolated murine intestinal segments that the receptors TLR-4, PAF-R, and [alpha]5{szligbeta}1 integrin are all involved in mediating bacterial uptake associated with transcytosis. The pattern of expression of TLR-4 and [alpha]5{szligbeta}1 integrin differed between M cells and enterocytes. There was increased apical expression of TLR-4 in M-cell cultures, and it was present on the apical surface of murine M cells but not enterocytes in situ. In contrast, PAF-R was expressed equally by both cell types in vitro and was abundantly expressed throughout the intestinal epithelium. Inhibition of TLR-4 and PAF-R, but not TLR-2, reduced gram-negative bacterial uptake by both cell types, whereas inhibition of the apically expressed [alpha]5{szligbeta}1 integrin significantly reduced the ability of M cells to translocate bacteria. Hence, the involvement of each receptor was dependent not only on differences in the level of receptor expression but the cellular localization. Using bacteria that had mutations that affected the bacterial lipooligosaccharide structure indicated that the oligosaccharide moiety was important in bacterial uptake. 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subjects | Animals Bacteria Biological and medical sciences Caco-2 Cells Cellular Microbiology: Pathogen-Host Cell Molecular Interactions Enterocytes - immunology Enterocytes - microbiology Fundamental and applied biological sciences. Psychology Haemophilus Infections - immunology Haemophilus influenzae - immunology Humans Intestinal Mucosa - cytology Intestinal Mucosa - metabolism Intestinal Mucosa - microbiology Lipopolysaccharides - chemistry Male Mice Mice, Inbred BALB C Microbiology Peyer's Patches - cytology Peyer's Patches - immunology Peyer's Patches - metabolism Peyer's Patches - microbiology Platelet Membrane Glycoproteins - physiology Receptors, G-Protein-Coupled - physiology Receptors, Pattern Recognition - physiology Toll-Like Receptor 4 - physiology |
title | Microbial Pattern Recognition Receptors Mediate M-Cell Uptake of a Gram-Negative Bacterium |
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