O-antigen delays lipopolysaccharide recognition and impairs antibacterial host defense in murine intestinal epithelial cells
Although Toll-like receptor (TLR) 4 signals from the cell surface of myeloid cells, it is restricted to an intracellular compartment and requires ligand internalization in intestinal epithelial cells (IECs). Yet, the functional consequence of cell-type specific receptor localization and uptake-depen...
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| creator | Duerr, Claudia U Zenk, Sebastian F Chassin, Cécilia Pott, Johanna Gütle, Dominique Hensel, Michael Hornef, Mathias W |
| description | Although Toll-like receptor (TLR) 4 signals from the cell surface of myeloid cells, it is restricted to an intracellular compartment and requires ligand internalization in intestinal epithelial cells (IECs). Yet, the functional consequence of cell-type specific receptor localization and uptake-dependent lipopolysaccharide (LPS) recognition is unknown. Here, we demonstrate a strikingly delayed activation of IECs but not macrophages by wildtype Salmonella enterica subsp. enterica sv. (S.) Typhimurium as compared to isogenic O-antigen deficient mutants. Delayed epithelial activation is associated with impaired LPS internalization and retarded TLR4-mediated immune recognition. The O-antigen-mediated evasion from early epithelial innate immune activation significantly enhances intraepithelial bacterial survival in vitro and in vivo following oral challenge. These data identify O-antigen expression as an innate immune evasion mechanism during apical intestinal epithelial invasion and illustrate the importance of early innate immune recognition for efficient host defense against invading Salmonella. |
| doi_str_mv | 10.1371/journal.ppat.1000567 |
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Yet, the functional consequence of cell-type specific receptor localization and uptake-dependent lipopolysaccharide (LPS) recognition is unknown. Here, we demonstrate a strikingly delayed activation of IECs but not macrophages by wildtype Salmonella enterica subsp. enterica sv. (S.) Typhimurium as compared to isogenic O-antigen deficient mutants. Delayed epithelial activation is associated with impaired LPS internalization and retarded TLR4-mediated immune recognition. The O-antigen-mediated evasion from early epithelial innate immune activation significantly enhances intraepithelial bacterial survival in vitro and in vivo following oral challenge. These data identify O-antigen expression as an innate immune evasion mechanism during apical intestinal epithelial invasion and illustrate the importance of early innate immune recognition for efficient host defense against invading Salmonella.</description><identifier>ISSN: 1553-7374</identifier><identifier>ISSN: 1553-7366</identifier><identifier>EISSN: 1553-7374</identifier><identifier>DOI: 10.1371/journal.ppat.1000567</identifier><identifier>PMID: 19730692</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Animals ; Antigens, Bacterial - genetics ; Antigens, Bacterial - immunology ; Antigens, Bacterial - metabolism ; Bacteria ; Bacterial infections ; Bacterial Proteins - metabolism ; Cell culture ; Chemokine CXCL2 - metabolism ; Data Interpretation, Statistical ; Epithelial Cells - immunology ; Female ; Gastroenterology and Hepatology/Gastrointestinal Infections ; Host-Pathogen Interactions - immunology ; Immunity, Innate ; Immunohistochemistry ; Immunology/Innate Immunity ; Infectious Diseases/Bacterial Infections ; Intestinal Mucosa - cytology ; Intestinal Mucosa - immunology ; Kinetics ; Ligands ; Lipopolysaccharides - immunology ; Macrophages - immunology ; Mice ; Mice, Inbred BALB C ; Microbiology ; NF-kappa B - metabolism ; O Antigens - genetics ; O Antigens - immunology ; O Antigens - metabolism ; Rodents ; Salmonella - genetics ; Salmonella - immunology ; Salmonella - pathogenicity ; Salmonella typhimurium - genetics ; Salmonella typhimurium - immunology ; Salmonella typhimurium - pathogenicity ; Signal transduction ; Toll-Like Receptor 4 - immunology</subject><ispartof>PLoS pathogens, 2009-09, Vol.5 (9), p.e1000567-e1000567</ispartof><rights>Duerr et al. 2009</rights><rights>2009 Duerr et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Duerr CU, Zenk SF, Chassin C, Pott J, Gütle D, et al. (2009) O-Antigen Delays Lipopolysaccharide Recognition and Impairs Antibacterial Host Defense in Murine Intestinal Epithelial Cells. 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Yet, the functional consequence of cell-type specific receptor localization and uptake-dependent lipopolysaccharide (LPS) recognition is unknown. Here, we demonstrate a strikingly delayed activation of IECs but not macrophages by wildtype Salmonella enterica subsp. enterica sv. (S.) Typhimurium as compared to isogenic O-antigen deficient mutants. Delayed epithelial activation is associated with impaired LPS internalization and retarded TLR4-mediated immune recognition. The O-antigen-mediated evasion from early epithelial innate immune activation significantly enhances intraepithelial bacterial survival in vitro and in vivo following oral challenge. These data identify O-antigen expression as an innate immune evasion mechanism during apical intestinal epithelial invasion and illustrate the importance of early innate immune recognition for efficient host defense against invading Salmonella.</description><subject>Animals</subject><subject>Antigens, Bacterial - genetics</subject><subject>Antigens, Bacterial - immunology</subject><subject>Antigens, Bacterial - metabolism</subject><subject>Bacteria</subject><subject>Bacterial infections</subject><subject>Bacterial Proteins - metabolism</subject><subject>Cell culture</subject><subject>Chemokine CXCL2 - metabolism</subject><subject>Data Interpretation, Statistical</subject><subject>Epithelial Cells - immunology</subject><subject>Female</subject><subject>Gastroenterology and Hepatology/Gastrointestinal Infections</subject><subject>Host-Pathogen Interactions - immunology</subject><subject>Immunity, Innate</subject><subject>Immunohistochemistry</subject><subject>Immunology/Innate Immunity</subject><subject>Infectious Diseases/Bacterial Infections</subject><subject>Intestinal Mucosa - cytology</subject><subject>Intestinal Mucosa - immunology</subject><subject>Kinetics</subject><subject>Ligands</subject><subject>Lipopolysaccharides - immunology</subject><subject>Macrophages - immunology</subject><subject>Mice</subject><subject>Mice, Inbred BALB C</subject><subject>Microbiology</subject><subject>NF-kappa B - metabolism</subject><subject>O Antigens - genetics</subject><subject>O Antigens - immunology</subject><subject>O Antigens - metabolism</subject><subject>Rodents</subject><subject>Salmonella - genetics</subject><subject>Salmonella - immunology</subject><subject>Salmonella - pathogenicity</subject><subject>Salmonella typhimurium - genetics</subject><subject>Salmonella typhimurium - immunology</subject><subject>Salmonella typhimurium - pathogenicity</subject><subject>Signal transduction</subject><subject>Toll-Like Receptor 4 - immunology</subject><issn>1553-7374</issn><issn>1553-7366</issn><issn>1553-7374</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2009</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>DOA</sourceid><recordid>eNpVUk2PFCEU7BiN-6H_wGjfPPUIDd3AxcRsdN1kk73omTzo1zNMGGiBMZnEH2-30-ruiReoV1VUqqreULKhTNAP-3hMAfxmmqBsKCGk68Wz6pJ2HWsEE_z5o_miusp5TwinjPYvqwuqBCO9ai-rXw8NhOK2GOoBPZxy7d0Up-hPGazdQXID1glt3AZXXAw1hKF2hwlcyvWyacAWTA58vYu5zCQjhoy1C_XhmFxYpoK5uNlqjZMrO_QL2KL3-VX1YgSf8fV6Xlffv3z-dvO1uX-4vbv5dN9YrkRpTN9xa7hQA2eS9gNYIdAgAh9UD0OHynDCGRhkHXZmZEwx6EdCrRFctSO7rt6deScfs16Dy5q2UpFZQfYz4u6MGCLs9ZTcAdJJR3D6z0VMWw2pOOtRdwB2RCm5kYwLxuTA-s5KA9RKSiSZuT6uakdzwMFiKAn8E9KnL8Ht9Db-1K1olWrlTPB-JUjxx3EOTx9cXgKDgPGYtWCcMNmLxTY_I22KOScc_6lQopeW_P2sXlqi15bMa28fO_y_tNaC_QZ6uMAC</recordid><startdate>20090901</startdate><enddate>20090901</enddate><creator>Duerr, Claudia U</creator><creator>Zenk, Sebastian F</creator><creator>Chassin, Cécilia</creator><creator>Pott, Johanna</creator><creator>Gütle, Dominique</creator><creator>Hensel, Michael</creator><creator>Hornef, Mathias W</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>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20090901</creationdate><title>O-antigen delays lipopolysaccharide recognition and impairs antibacterial host defense in murine intestinal epithelial cells</title><author>Duerr, Claudia U ; Zenk, Sebastian F ; Chassin, Cécilia ; Pott, Johanna ; Gütle, Dominique ; Hensel, Michael ; Hornef, Mathias W</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c497t-b654cb479d43816dac77ebeea4d96ad5e9b4043abe35e5bf3393a6f01cb7492f3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2009</creationdate><topic>Animals</topic><topic>Antigens, Bacterial - genetics</topic><topic>Antigens, Bacterial - immunology</topic><topic>Antigens, Bacterial - metabolism</topic><topic>Bacteria</topic><topic>Bacterial infections</topic><topic>Bacterial Proteins - metabolism</topic><topic>Cell culture</topic><topic>Chemokine CXCL2 - metabolism</topic><topic>Data Interpretation, Statistical</topic><topic>Epithelial Cells - immunology</topic><topic>Female</topic><topic>Gastroenterology and Hepatology/Gastrointestinal Infections</topic><topic>Host-Pathogen Interactions - immunology</topic><topic>Immunity, Innate</topic><topic>Immunohistochemistry</topic><topic>Immunology/Innate Immunity</topic><topic>Infectious Diseases/Bacterial Infections</topic><topic>Intestinal Mucosa - cytology</topic><topic>Intestinal Mucosa - immunology</topic><topic>Kinetics</topic><topic>Ligands</topic><topic>Lipopolysaccharides - immunology</topic><topic>Macrophages - immunology</topic><topic>Mice</topic><topic>Mice, Inbred BALB C</topic><topic>Microbiology</topic><topic>NF-kappa B - metabolism</topic><topic>O Antigens - genetics</topic><topic>O Antigens - immunology</topic><topic>O Antigens - metabolism</topic><topic>Rodents</topic><topic>Salmonella - genetics</topic><topic>Salmonella - immunology</topic><topic>Salmonella - pathogenicity</topic><topic>Salmonella typhimurium - genetics</topic><topic>Salmonella typhimurium - immunology</topic><topic>Salmonella typhimurium - pathogenicity</topic><topic>Signal transduction</topic><topic>Toll-Like Receptor 4 - immunology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Duerr, Claudia U</creatorcontrib><creatorcontrib>Zenk, Sebastian F</creatorcontrib><creatorcontrib>Chassin, Cécilia</creatorcontrib><creatorcontrib>Pott, Johanna</creatorcontrib><creatorcontrib>Gütle, Dominique</creatorcontrib><creatorcontrib>Hensel, Michael</creatorcontrib><creatorcontrib>Hornef, Mathias W</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><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PLoS pathogens</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Duerr, Claudia U</au><au>Zenk, Sebastian F</au><au>Chassin, Cécilia</au><au>Pott, Johanna</au><au>Gütle, Dominique</au><au>Hensel, Michael</au><au>Hornef, Mathias W</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>O-antigen delays lipopolysaccharide recognition and impairs antibacterial host defense in murine intestinal epithelial cells</atitle><jtitle>PLoS pathogens</jtitle><addtitle>PLoS Pathog</addtitle><date>2009-09-01</date><risdate>2009</risdate><volume>5</volume><issue>9</issue><spage>e1000567</spage><epage>e1000567</epage><pages>e1000567-e1000567</pages><issn>1553-7374</issn><issn>1553-7366</issn><eissn>1553-7374</eissn><abstract>Although Toll-like receptor (TLR) 4 signals from the cell surface of myeloid cells, it is restricted to an intracellular compartment and requires ligand internalization in intestinal epithelial cells (IECs). Yet, the functional consequence of cell-type specific receptor localization and uptake-dependent lipopolysaccharide (LPS) recognition is unknown. Here, we demonstrate a strikingly delayed activation of IECs but not macrophages by wildtype Salmonella enterica subsp. enterica sv. (S.) Typhimurium as compared to isogenic O-antigen deficient mutants. Delayed epithelial activation is associated with impaired LPS internalization and retarded TLR4-mediated immune recognition. The O-antigen-mediated evasion from early epithelial innate immune activation significantly enhances intraepithelial bacterial survival in vitro and in vivo following oral challenge. These data identify O-antigen expression as an innate immune evasion mechanism during apical intestinal epithelial invasion and illustrate the importance of early innate immune recognition for efficient host defense against invading Salmonella.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>19730692</pmid><doi>10.1371/journal.ppat.1000567</doi><oa>free_for_read</oa></addata></record> |
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| subjects | Animals Antigens, Bacterial - genetics Antigens, Bacterial - immunology Antigens, Bacterial - metabolism Bacteria Bacterial infections Bacterial Proteins - metabolism Cell culture Chemokine CXCL2 - metabolism Data Interpretation, Statistical Epithelial Cells - immunology Female Gastroenterology and Hepatology/Gastrointestinal Infections Host-Pathogen Interactions - immunology Immunity, Innate Immunohistochemistry Immunology/Innate Immunity Infectious Diseases/Bacterial Infections Intestinal Mucosa - cytology Intestinal Mucosa - immunology Kinetics Ligands Lipopolysaccharides - immunology Macrophages - immunology Mice Mice, Inbred BALB C Microbiology NF-kappa B - metabolism O Antigens - genetics O Antigens - immunology O Antigens - metabolism Rodents Salmonella - genetics Salmonella - immunology Salmonella - pathogenicity Salmonella typhimurium - genetics Salmonella typhimurium - immunology Salmonella typhimurium - pathogenicity Signal transduction Toll-Like Receptor 4 - immunology |
| title | O-antigen delays lipopolysaccharide recognition and impairs antibacterial host defense in murine intestinal epithelial cells |
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