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A directed screen for chlamydial proteins secreted by a type III mechanism identifies a translocated protein and numerous other new candidates
Summary Chlamydiae are strict intracellular parasites that induce their internalization upon contact with the host cell and grow inside an intracellular compartment called an inclusion. They possess a type III secretion (TTS) apparatus, which allows for the translocation of specific proteins in the...
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Published in: | Molecular microbiology 2005-06, Vol.56 (6), p.1636-1647 |
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container_title | Molecular microbiology |
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creator | Subtil, Agathe Delevoye, Cédric Balañá, María‐Eugenia Tastevin, Laurence Perrinet, Stéphanie Dautry‐Varsat, Alice |
description | Summary
Chlamydiae are strict intracellular parasites that induce their internalization upon contact with the host cell and grow inside an intracellular compartment called an inclusion. They possess a type III secretion (TTS) apparatus, which allows for the translocation of specific proteins in the host cell cytosol. In particular, chlamydial proteins of the Inc family are secreted to the inclusion membrane by a TTS mechanism; other TTS substrates are mostly unknown. Using a secretion assay based on the recognition of TTS signals in Shigella flexneri, we searched for TTS signals in the proteins of unknown function, conserved between three different chlamydial species, Chlamydia pneumoniae, C. trachomatis and C. caviae. We identified 24 new candidate proteins which did not belong to the Inc family. Four of these proteins were also secreted as full‐length proteins by a TTS mechanism in S. flexneri, indicating that their translocation does not require other chlamydial proteins. One of these proteins was detected in the cytosol of infected cells using specific antibodies, directly demonstrating that it is translocated in the host cell during bacterial proliferation. More generally, this work represents the first directed search for TTS effectors not based on genetic information or sequence similarity. It reveals the abundance of proteins secreted in the host cell by chlamydiae. |
doi_str_mv | 10.1111/j.1365-2958.2005.04647.x |
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Chlamydiae are strict intracellular parasites that induce their internalization upon contact with the host cell and grow inside an intracellular compartment called an inclusion. They possess a type III secretion (TTS) apparatus, which allows for the translocation of specific proteins in the host cell cytosol. In particular, chlamydial proteins of the Inc family are secreted to the inclusion membrane by a TTS mechanism; other TTS substrates are mostly unknown. Using a secretion assay based on the recognition of TTS signals in Shigella flexneri, we searched for TTS signals in the proteins of unknown function, conserved between three different chlamydial species, Chlamydia pneumoniae, C. trachomatis and C. caviae. We identified 24 new candidate proteins which did not belong to the Inc family. Four of these proteins were also secreted as full‐length proteins by a TTS mechanism in S. flexneri, indicating that their translocation does not require other chlamydial proteins. One of these proteins was detected in the cytosol of infected cells using specific antibodies, directly demonstrating that it is translocated in the host cell during bacterial proliferation. More generally, this work represents the first directed search for TTS effectors not based on genetic information or sequence similarity. It reveals the abundance of proteins secreted in the host cell by chlamydiae.</description><identifier>ISSN: 0950-382X</identifier><identifier>EISSN: 1365-2958</identifier><identifier>DOI: 10.1111/j.1365-2958.2005.04647.x</identifier><identifier>PMID: 15916612</identifier><language>eng</language><publisher>Oxford, UK: Blackwell Science Ltd</publisher><subject>Bacterial Proteins ; Bacterial Proteins - genetics ; Bacterial Proteins - metabolism ; Bacteriology ; Biological and medical sciences ; Cells ; Chlamydia ; Chlamydia - classification ; Chlamydia - genetics ; Chlamydia - metabolism ; Chlamydia - pathogenicity ; Chlamydia trachomatis ; Chlamydia trachomatis - genetics ; Chlamydia trachomatis - metabolism ; Chlamydia trachomatis - pathogenicity ; Chlamydophila pneumoniae ; Chlamydophila pneumoniae - genetics ; Chlamydophila pneumoniae - metabolism ; Chlamydophila pneumoniae - pathogenicity ; Fundamental and applied biological sciences. Psychology ; Gene Expression Regulation, Bacterial ; HeLa Cells ; Humans ; Life Sciences ; Microbiology ; Microbiology and Parasitology ; Miscellaneous ; Parasites ; Protein Transport ; Proteins ; Recombinant Proteins ; Recombinant Proteins - genetics ; Recombinant Proteins - metabolism ; Shigella flexneri ; Shigella flexneri - genetics ; Shigella flexneri - metabolism ; Signal Transduction</subject><ispartof>Molecular microbiology, 2005-06, Vol.56 (6), p.1636-1647</ispartof><rights>2005 INIST-CNRS</rights><rights>Copyright Blackwell Publishing Jun 2005</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c5397-47c9ae58e5bc5d0bbf8595c067cf73cb6ba4a00b63fa805a51610b3c4e92b8a53</citedby><cites>FETCH-LOGICAL-c5397-47c9ae58e5bc5d0bbf8595c067cf73cb6ba4a00b63fa805a51610b3c4e92b8a53</cites><orcidid>0000-0002-3835-6649</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,780,784,885,27924,27925</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=16802578$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/15916612$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-00021366$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Subtil, Agathe</creatorcontrib><creatorcontrib>Delevoye, Cédric</creatorcontrib><creatorcontrib>Balañá, María‐Eugenia</creatorcontrib><creatorcontrib>Tastevin, Laurence</creatorcontrib><creatorcontrib>Perrinet, Stéphanie</creatorcontrib><creatorcontrib>Dautry‐Varsat, Alice</creatorcontrib><title>A directed screen for chlamydial proteins secreted by a type III mechanism identifies a translocated protein and numerous other new candidates</title><title>Molecular microbiology</title><addtitle>Mol Microbiol</addtitle><description>Summary
Chlamydiae are strict intracellular parasites that induce their internalization upon contact with the host cell and grow inside an intracellular compartment called an inclusion. They possess a type III secretion (TTS) apparatus, which allows for the translocation of specific proteins in the host cell cytosol. In particular, chlamydial proteins of the Inc family are secreted to the inclusion membrane by a TTS mechanism; other TTS substrates are mostly unknown. Using a secretion assay based on the recognition of TTS signals in Shigella flexneri, we searched for TTS signals in the proteins of unknown function, conserved between three different chlamydial species, Chlamydia pneumoniae, C. trachomatis and C. caviae. We identified 24 new candidate proteins which did not belong to the Inc family. Four of these proteins were also secreted as full‐length proteins by a TTS mechanism in S. flexneri, indicating that their translocation does not require other chlamydial proteins. One of these proteins was detected in the cytosol of infected cells using specific antibodies, directly demonstrating that it is translocated in the host cell during bacterial proliferation. More generally, this work represents the first directed search for TTS effectors not based on genetic information or sequence similarity. It reveals the abundance of proteins secreted in the host cell by chlamydiae.</description><subject>Bacterial Proteins</subject><subject>Bacterial Proteins - genetics</subject><subject>Bacterial Proteins - metabolism</subject><subject>Bacteriology</subject><subject>Biological and medical sciences</subject><subject>Cells</subject><subject>Chlamydia</subject><subject>Chlamydia - classification</subject><subject>Chlamydia - genetics</subject><subject>Chlamydia - metabolism</subject><subject>Chlamydia - pathogenicity</subject><subject>Chlamydia trachomatis</subject><subject>Chlamydia trachomatis - genetics</subject><subject>Chlamydia trachomatis - metabolism</subject><subject>Chlamydia trachomatis - pathogenicity</subject><subject>Chlamydophila pneumoniae</subject><subject>Chlamydophila pneumoniae - genetics</subject><subject>Chlamydophila pneumoniae - metabolism</subject><subject>Chlamydophila pneumoniae - pathogenicity</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>Gene Expression Regulation, Bacterial</subject><subject>HeLa Cells</subject><subject>Humans</subject><subject>Life Sciences</subject><subject>Microbiology</subject><subject>Microbiology and Parasitology</subject><subject>Miscellaneous</subject><subject>Parasites</subject><subject>Protein Transport</subject><subject>Proteins</subject><subject>Recombinant Proteins</subject><subject>Recombinant Proteins - genetics</subject><subject>Recombinant Proteins - metabolism</subject><subject>Shigella flexneri</subject><subject>Shigella flexneri - genetics</subject><subject>Shigella flexneri - metabolism</subject><subject>Signal Transduction</subject><issn>0950-382X</issn><issn>1365-2958</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2005</creationdate><recordtype>article</recordtype><recordid>eNqNkk2LFDEQhoMo7jj6FyQICnuYttLpfPTBw7C4bsMsXhS8hXS6msnQH2PSs7vzJ_zNpp1hF7xoLglVT71U5S1CKIOMpfNxlzEuxSovhc5yAJFBIQuVPTwji8fEc7KAUsCK6_zHBXkV4w6AcZD8JblgomRSsnxBfq1p4wO6CRsaXUAcaDsG6rad7Y-Ntx3dh3FCP0QaMeVnrj5SS6fjHmlVVbRHt7WDjz31DQ6Tbz3GOR_sELvR2bnirEHt0NDh0GMYD5GO0xYDHfCeuhT3TSLja_KitV3EN-d7Sb5ff_52dbPafP1SXa03Kyd4qVaFcqVFoVHUTjRQ160WpXAglWsVd7WsbWEBaslbq0FYwSSDmrsCy7zWVvAluTzpbm1n9sH3NhzNaL25WW_MHAOAPH2lvGOJ_XBi0xQ_Dxgn0_vosOvsgGkOI5VWoBT_J8hUoXWZyCV59xe4Gw9hSAMbVkrBmZZzi_oEuTDGGLB97JOBmbfA7MxstpnNNvMWmD9bYB5S6duz_qHusXkqPNuegPdnwEZnuzZ55Xx84qSGXCiduE8n7t53ePzvBsztbTW_-G_hps5v</recordid><startdate>200506</startdate><enddate>200506</enddate><creator>Subtil, Agathe</creator><creator>Delevoye, Cédric</creator><creator>Balañá, María‐Eugenia</creator><creator>Tastevin, Laurence</creator><creator>Perrinet, Stéphanie</creator><creator>Dautry‐Varsat, Alice</creator><general>Blackwell Science Ltd</general><general>Blackwell Science</general><general>Blackwell Publishing Ltd</general><general>Wiley</general><scope>IQODW</scope><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>1XC</scope><orcidid>https://orcid.org/0000-0002-3835-6649</orcidid></search><sort><creationdate>200506</creationdate><title>A directed screen for chlamydial proteins secreted by a type III mechanism identifies a translocated protein and numerous other new candidates</title><author>Subtil, Agathe ; Delevoye, Cédric ; Balañá, María‐Eugenia ; Tastevin, Laurence ; Perrinet, Stéphanie ; Dautry‐Varsat, Alice</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c5397-47c9ae58e5bc5d0bbf8595c067cf73cb6ba4a00b63fa805a51610b3c4e92b8a53</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2005</creationdate><topic>Bacterial Proteins</topic><topic>Bacterial Proteins - genetics</topic><topic>Bacterial Proteins - metabolism</topic><topic>Bacteriology</topic><topic>Biological and medical sciences</topic><topic>Cells</topic><topic>Chlamydia</topic><topic>Chlamydia - classification</topic><topic>Chlamydia - genetics</topic><topic>Chlamydia - metabolism</topic><topic>Chlamydia - pathogenicity</topic><topic>Chlamydia trachomatis</topic><topic>Chlamydia trachomatis - genetics</topic><topic>Chlamydia trachomatis - metabolism</topic><topic>Chlamydia trachomatis - pathogenicity</topic><topic>Chlamydophila pneumoniae</topic><topic>Chlamydophila pneumoniae - genetics</topic><topic>Chlamydophila pneumoniae - metabolism</topic><topic>Chlamydophila pneumoniae - pathogenicity</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>Gene Expression Regulation, Bacterial</topic><topic>HeLa Cells</topic><topic>Humans</topic><topic>Life Sciences</topic><topic>Microbiology</topic><topic>Microbiology and Parasitology</topic><topic>Miscellaneous</topic><topic>Parasites</topic><topic>Protein Transport</topic><topic>Proteins</topic><topic>Recombinant Proteins</topic><topic>Recombinant Proteins - genetics</topic><topic>Recombinant Proteins - metabolism</topic><topic>Shigella flexneri</topic><topic>Shigella flexneri - genetics</topic><topic>Shigella flexneri - metabolism</topic><topic>Signal Transduction</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Subtil, Agathe</creatorcontrib><creatorcontrib>Delevoye, Cédric</creatorcontrib><creatorcontrib>Balañá, María‐Eugenia</creatorcontrib><creatorcontrib>Tastevin, Laurence</creatorcontrib><creatorcontrib>Perrinet, Stéphanie</creatorcontrib><creatorcontrib>Dautry‐Varsat, Alice</creatorcontrib><collection>Pascal-Francis</collection><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>Hyper Article en Ligne (HAL)</collection><jtitle>Molecular microbiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Subtil, Agathe</au><au>Delevoye, Cédric</au><au>Balañá, María‐Eugenia</au><au>Tastevin, Laurence</au><au>Perrinet, Stéphanie</au><au>Dautry‐Varsat, Alice</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>A directed screen for chlamydial proteins secreted by a type III mechanism identifies a translocated protein and numerous other new candidates</atitle><jtitle>Molecular microbiology</jtitle><addtitle>Mol Microbiol</addtitle><date>2005-06</date><risdate>2005</risdate><volume>56</volume><issue>6</issue><spage>1636</spage><epage>1647</epage><pages>1636-1647</pages><issn>0950-382X</issn><eissn>1365-2958</eissn><abstract>Summary
Chlamydiae are strict intracellular parasites that induce their internalization upon contact with the host cell and grow inside an intracellular compartment called an inclusion. They possess a type III secretion (TTS) apparatus, which allows for the translocation of specific proteins in the host cell cytosol. In particular, chlamydial proteins of the Inc family are secreted to the inclusion membrane by a TTS mechanism; other TTS substrates are mostly unknown. Using a secretion assay based on the recognition of TTS signals in Shigella flexneri, we searched for TTS signals in the proteins of unknown function, conserved between three different chlamydial species, Chlamydia pneumoniae, C. trachomatis and C. caviae. We identified 24 new candidate proteins which did not belong to the Inc family. Four of these proteins were also secreted as full‐length proteins by a TTS mechanism in S. flexneri, indicating that their translocation does not require other chlamydial proteins. One of these proteins was detected in the cytosol of infected cells using specific antibodies, directly demonstrating that it is translocated in the host cell during bacterial proliferation. More generally, this work represents the first directed search for TTS effectors not based on genetic information or sequence similarity. It reveals the abundance of proteins secreted in the host cell by chlamydiae.</abstract><cop>Oxford, UK</cop><pub>Blackwell Science Ltd</pub><pmid>15916612</pmid><doi>10.1111/j.1365-2958.2005.04647.x</doi><tpages>12</tpages><orcidid>https://orcid.org/0000-0002-3835-6649</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Bacterial Proteins Bacterial Proteins - genetics Bacterial Proteins - metabolism Bacteriology Biological and medical sciences Cells Chlamydia Chlamydia - classification Chlamydia - genetics Chlamydia - metabolism Chlamydia - pathogenicity Chlamydia trachomatis Chlamydia trachomatis - genetics Chlamydia trachomatis - metabolism Chlamydia trachomatis - pathogenicity Chlamydophila pneumoniae Chlamydophila pneumoniae - genetics Chlamydophila pneumoniae - metabolism Chlamydophila pneumoniae - pathogenicity Fundamental and applied biological sciences. Psychology Gene Expression Regulation, Bacterial HeLa Cells Humans Life Sciences Microbiology Microbiology and Parasitology Miscellaneous Parasites Protein Transport Proteins Recombinant Proteins Recombinant Proteins - genetics Recombinant Proteins - metabolism Shigella flexneri Shigella flexneri - genetics Shigella flexneri - metabolism Signal Transduction |
title | A directed screen for chlamydial proteins secreted by a type III mechanism identifies a translocated protein and numerous other new candidates |
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