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Campylobacter jejuni survival within human epithelial cells is enhanced by the secreted protein CiaI
Summary Although it is known that Campylobacter jejuni invade the cells that line the human intestinal tract, the bacterial proteins that enable this pathogen to survive within Campylobacter‐containing vacuoles (CCV) have not been identified. Here, we describe the identification and characterization...
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Published in: | Molecular microbiology 2011-06, Vol.80 (5), p.1296-1312 |
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description | Summary
Although it is known that Campylobacter jejuni invade the cells that line the human intestinal tract, the bacterial proteins that enable this pathogen to survive within Campylobacter‐containing vacuoles (CCV) have not been identified. Here, we describe the identification and characterization of a protein that we termed CiaI for Campylobacter invasion antigen involved in intracellular survival. We show that CiaI harbours an amino‐terminal type III secretion sequence and is secreted from C. jejuni through the flagellar type III secretion system. In addition, the ciaI mutant was impaired in intracellular survival when compared with a wild‐type strain, as judged by the gentamicin‐protection assay. Fluorescence microscopy examination of epithelial cells infected with the C. jejuni ciaI mutant revealed that the CCV were more frequently co‐localized with Cathepsin D (a lysosomal marker) than the CCV in cells infected with a C. jejuni wild‐type strain. Ectopic expression of CiaI‐GFP in epithelial cells yielded a punctate phenotype not observed with the other C. jejuni genes, and this phenotype was abolished by mutation of a dileucine motif located in the carboxy‐terminus of the protein. Based on the data, we conclude that CiaI contributes to the ability of C. jejuni to survive within epithelial cells. |
doi_str_mv | 10.1111/j.1365-2958.2011.07645.x |
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Although it is known that Campylobacter jejuni invade the cells that line the human intestinal tract, the bacterial proteins that enable this pathogen to survive within Campylobacter‐containing vacuoles (CCV) have not been identified. Here, we describe the identification and characterization of a protein that we termed CiaI for Campylobacter invasion antigen involved in intracellular survival. We show that CiaI harbours an amino‐terminal type III secretion sequence and is secreted from C. jejuni through the flagellar type III secretion system. In addition, the ciaI mutant was impaired in intracellular survival when compared with a wild‐type strain, as judged by the gentamicin‐protection assay. Fluorescence microscopy examination of epithelial cells infected with the C. jejuni ciaI mutant revealed that the CCV were more frequently co‐localized with Cathepsin D (a lysosomal marker) than the CCV in cells infected with a C. jejuni wild‐type strain. Ectopic expression of CiaI‐GFP in epithelial cells yielded a punctate phenotype not observed with the other C. jejuni genes, and this phenotype was abolished by mutation of a dileucine motif located in the carboxy‐terminus of the protein. Based on the data, we conclude that CiaI contributes to the ability of C. jejuni to survive within epithelial cells.</description><identifier>ISSN: 0950-382X</identifier><identifier>EISSN: 1365-2958</identifier><identifier>DOI: 10.1111/j.1365-2958.2011.07645.x</identifier><identifier>PMID: 21435039</identifier><language>eng</language><publisher>Oxford, UK: Blackwell Publishing Ltd</publisher><subject>Bacterial proteins ; Bacterial Proteins - genetics ; Bacterial Proteins - metabolism ; Campylobacter Infections - microbiology ; Campylobacter jejuni ; Campylobacter jejuni - genetics ; Campylobacter jejuni - growth & development ; Campylobacter jejuni - metabolism ; Cells ; Digestive system ; Epithelial Cells - microbiology ; Gene Expression Regulation, Bacterial ; Genes ; Genotype & phenotype ; Gram-negative bacteria ; Humans ; Microbial Viability ; Mutation ; Protein Transport</subject><ispartof>Molecular microbiology, 2011-06, Vol.80 (5), p.1296-1312</ispartof><rights>2011 Blackwell Publishing Ltd</rights><rights>2011 Blackwell Publishing Ltd.</rights><rights>Copyright Blackwell Publishing Ltd. Jun 2011</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c5335-b1f4b4ecb06f7394437c1073ccd4450ce38d1455d8ba05bb8042890c85ca4c3b3</citedby><cites>FETCH-LOGICAL-c5335-b1f4b4ecb06f7394437c1073ccd4450ce38d1455d8ba05bb8042890c85ca4c3b3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,776,780,881,27903,27904</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/21435039$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Buelow, Daelynn R.</creatorcontrib><creatorcontrib>Christensen, Jeffrey E.</creatorcontrib><creatorcontrib>Neal‐McKinney, Jason M.</creatorcontrib><creatorcontrib>Konkel, Michael E.</creatorcontrib><title>Campylobacter jejuni survival within human epithelial cells is enhanced by the secreted protein CiaI</title><title>Molecular microbiology</title><addtitle>Mol Microbiol</addtitle><description>Summary
Although it is known that Campylobacter jejuni invade the cells that line the human intestinal tract, the bacterial proteins that enable this pathogen to survive within Campylobacter‐containing vacuoles (CCV) have not been identified. Here, we describe the identification and characterization of a protein that we termed CiaI for Campylobacter invasion antigen involved in intracellular survival. We show that CiaI harbours an amino‐terminal type III secretion sequence and is secreted from C. jejuni through the flagellar type III secretion system. In addition, the ciaI mutant was impaired in intracellular survival when compared with a wild‐type strain, as judged by the gentamicin‐protection assay. Fluorescence microscopy examination of epithelial cells infected with the C. jejuni ciaI mutant revealed that the CCV were more frequently co‐localized with Cathepsin D (a lysosomal marker) than the CCV in cells infected with a C. jejuni wild‐type strain. Ectopic expression of CiaI‐GFP in epithelial cells yielded a punctate phenotype not observed with the other C. jejuni genes, and this phenotype was abolished by mutation of a dileucine motif located in the carboxy‐terminus of the protein. Based on the data, we conclude that CiaI contributes to the ability of C. jejuni to survive within epithelial cells.</description><subject>Bacterial proteins</subject><subject>Bacterial Proteins - genetics</subject><subject>Bacterial Proteins - metabolism</subject><subject>Campylobacter Infections - microbiology</subject><subject>Campylobacter jejuni</subject><subject>Campylobacter jejuni - genetics</subject><subject>Campylobacter jejuni - growth & development</subject><subject>Campylobacter jejuni - metabolism</subject><subject>Cells</subject><subject>Digestive system</subject><subject>Epithelial Cells - microbiology</subject><subject>Gene Expression Regulation, Bacterial</subject><subject>Genes</subject><subject>Genotype & phenotype</subject><subject>Gram-negative bacteria</subject><subject>Humans</subject><subject>Microbial Viability</subject><subject>Mutation</subject><subject>Protein Transport</subject><issn>0950-382X</issn><issn>1365-2958</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2011</creationdate><recordtype>article</recordtype><recordid>eNqNkUtv1DAUhS0EokPhLyCLDWwS7FzbcRYgVSMeI7ViAxI7y3Y8jKO8sJNp59_jdMqoZVHhjX19v3Pk64MQpiSnab1vcgqCZ0XFZV4QSnNSCsbzmydodWo8RStScZKBLH6eoRcxNoRQIAKeo7OCMuAEqhWq17obD-1gtJ1cwI1r5t7jOIe93-sWX_tp53u8mzvdYzemyrU-3VvXthH7iF2_0711NTYHnJo4OhvclOoxDJNL0rXXm5fo2Va30b2628_Rj8-fvq-_ZpffvmzWF5eZ5QA8M3TLDHPWELEtoWIMSktJCdbWjHFiHciaMs5raTThxkjCClkRK7nVzIKBc_Tx6DvOpnO1df0UdKvG4DsdDmrQXj3s9H6nfg17BZSAoJAM3t4ZhOH37OKkOh-XWXXvhjkqKWRVVUQUiXz3KEnLBMlCAEvom3_QZphDnz5CyZIyWoAQCZJHyIYhxuC2p1dTopbMVaOWaNUSrVoyV7eZq5skfX1_6pPwb8gJ-HAErn3rDv9trK6uNssJ_gDHirvS</recordid><startdate>201106</startdate><enddate>201106</enddate><creator>Buelow, Daelynn R.</creator><creator>Christensen, Jeffrey E.</creator><creator>Neal‐McKinney, Jason M.</creator><creator>Konkel, Michael E.</creator><general>Blackwell Publishing Ltd</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>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7TK</scope><scope>7TM</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>201106</creationdate><title>Campylobacter jejuni survival within human epithelial cells is enhanced by the secreted protein CiaI</title><author>Buelow, Daelynn R. ; Christensen, Jeffrey E. ; Neal‐McKinney, Jason M. ; Konkel, Michael E.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c5335-b1f4b4ecb06f7394437c1073ccd4450ce38d1455d8ba05bb8042890c85ca4c3b3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2011</creationdate><topic>Bacterial proteins</topic><topic>Bacterial Proteins - genetics</topic><topic>Bacterial Proteins - metabolism</topic><topic>Campylobacter Infections - microbiology</topic><topic>Campylobacter jejuni</topic><topic>Campylobacter jejuni - genetics</topic><topic>Campylobacter jejuni - growth & development</topic><topic>Campylobacter jejuni - metabolism</topic><topic>Cells</topic><topic>Digestive system</topic><topic>Epithelial Cells - microbiology</topic><topic>Gene Expression Regulation, Bacterial</topic><topic>Genes</topic><topic>Genotype & phenotype</topic><topic>Gram-negative bacteria</topic><topic>Humans</topic><topic>Microbial Viability</topic><topic>Mutation</topic><topic>Protein Transport</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Buelow, Daelynn R.</creatorcontrib><creatorcontrib>Christensen, Jeffrey E.</creatorcontrib><creatorcontrib>Neal‐McKinney, Jason M.</creatorcontrib><creatorcontrib>Konkel, Michael E.</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Molecular microbiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Buelow, Daelynn R.</au><au>Christensen, Jeffrey E.</au><au>Neal‐McKinney, Jason M.</au><au>Konkel, Michael E.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Campylobacter jejuni survival within human epithelial cells is enhanced by the secreted protein CiaI</atitle><jtitle>Molecular microbiology</jtitle><addtitle>Mol Microbiol</addtitle><date>2011-06</date><risdate>2011</risdate><volume>80</volume><issue>5</issue><spage>1296</spage><epage>1312</epage><pages>1296-1312</pages><issn>0950-382X</issn><eissn>1365-2958</eissn><abstract>Summary
Although it is known that Campylobacter jejuni invade the cells that line the human intestinal tract, the bacterial proteins that enable this pathogen to survive within Campylobacter‐containing vacuoles (CCV) have not been identified. Here, we describe the identification and characterization of a protein that we termed CiaI for Campylobacter invasion antigen involved in intracellular survival. We show that CiaI harbours an amino‐terminal type III secretion sequence and is secreted from C. jejuni through the flagellar type III secretion system. In addition, the ciaI mutant was impaired in intracellular survival when compared with a wild‐type strain, as judged by the gentamicin‐protection assay. Fluorescence microscopy examination of epithelial cells infected with the C. jejuni ciaI mutant revealed that the CCV were more frequently co‐localized with Cathepsin D (a lysosomal marker) than the CCV in cells infected with a C. jejuni wild‐type strain. Ectopic expression of CiaI‐GFP in epithelial cells yielded a punctate phenotype not observed with the other C. jejuni genes, and this phenotype was abolished by mutation of a dileucine motif located in the carboxy‐terminus of the protein. Based on the data, we conclude that CiaI contributes to the ability of C. jejuni to survive within epithelial cells.</abstract><cop>Oxford, UK</cop><pub>Blackwell Publishing Ltd</pub><pmid>21435039</pmid><doi>10.1111/j.1365-2958.2011.07645.x</doi><tpages>17</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Bacterial proteins Bacterial Proteins - genetics Bacterial Proteins - metabolism Campylobacter Infections - microbiology Campylobacter jejuni Campylobacter jejuni - genetics Campylobacter jejuni - growth & development Campylobacter jejuni - metabolism Cells Digestive system Epithelial Cells - microbiology Gene Expression Regulation, Bacterial Genes Genotype & phenotype Gram-negative bacteria Humans Microbial Viability Mutation Protein Transport |
title | Campylobacter jejuni survival within human epithelial cells is enhanced by the secreted protein CiaI |
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