Toxoplasma Sortilin-like Receptor Regulates Protein Transport and Is Essential for Apical Secretory Organelle Biogenesis and Host Infection
Apicomplexan parasites have an assortment of unique apical secretory organelles (rhoptries and micronemes), which have crucial functions in host infection. Here, we show that a Toxoplasma gondii sortilin-like receptor (TgSORTLR) is required for the subcellular localization and formation of apical se...
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| Veröffentlicht in: | Cell host & microbe 2012-05, Vol.11 (5), p.515-527 |
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| creator | Sloves, Pierre-Julien Delhaye, Stephane Mouveaux, Thomas Werkmeister, Elisabeth Slomianny, Christian Hovasse, Agnes Dilezitoko Alayi, Tchilabalo Callebaut, Isabelle Gaji, Rajshekhar Y. Schaeffer-Reiss, Christine Van Dorsselear, Alain Carruthers, Vern B. Tomavo, Stanislas |
| description | Apicomplexan parasites have an assortment of unique apical secretory organelles (rhoptries and micronemes), which have crucial functions in host infection. Here, we show that a Toxoplasma gondii sortilin-like receptor (TgSORTLR) is required for the subcellular localization and formation of apical secretory organelles. TgSORTLR is a transmembrane protein that resides within Golgi-endosomal related compartments. The lumenal domain specifically interacts with rhoptry and microneme proteins, while the cytoplasmic tail of TgSORTLR recruits cytosolic sorting machinery involved in anterograde and retrograde protein transport. Ectopic expression of the N-terminal TgSORTLR lumenal domain results in dominant negative effects with the mislocalization of both endogenous TgSORTLR as well as rhoptry and microneme proteins. Conditional ablation of TgSORTLR disrupts rhoptry and microneme biogenesis, inhibits parasite motility, and blocks both invasion into and egress from host cells. Thus, the sortilin-like receptor is essential for protein trafficking and the biogenesis of key secretory organelles in Toxoplasma.
► TgSORTLR is a type I transmembrane cargo receptor protein in T. gondii ► TgSORTLR interacts with MIC and ROP proteins through its lumenal domain ► TgSORTLR recruits endosomal and adaptor proteins through its cytosolic domain ► TgSORTLR is essential for the biogenesis of secretory organelles in T. gondii |
| doi_str_mv | 10.1016/j.chom.2012.03.006 |
| format | Article |
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► TgSORTLR is a type I transmembrane cargo receptor protein in T. gondii ► TgSORTLR interacts with MIC and ROP proteins through its lumenal domain ► TgSORTLR recruits endosomal and adaptor proteins through its cytosolic domain ► TgSORTLR is essential for the biogenesis of secretory organelles in T. gondii</description><identifier>ISSN: 1931-3128</identifier><identifier>EISSN: 1934-6069</identifier><identifier>DOI: 10.1016/j.chom.2012.03.006</identifier><identifier>PMID: 22607804</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Adaptor Proteins, Vesicular Transport - metabolism ; Animals ; Cells, Cultured ; Female ; Humans ; Membrane Proteins ; Mice ; Mice, Inbred BALB C ; Models, Biological ; Organelles - metabolism ; Protein Binding ; Protein Interaction Mapping ; Protein Transport ; Survival Analysis ; Toxoplasma - metabolism ; Toxoplasma - pathogenicity ; Toxoplasmosis, Animal</subject><ispartof>Cell host & microbe, 2012-05, Vol.11 (5), p.515-527</ispartof><rights>2012 Elsevier Inc.</rights><rights>Copyright © 2012 Elsevier Inc. All rights reserved.</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-c500t-5a4d1606ad1d0644038096bd5b034d5313d5248219e99b6314b8de26ac880f823</citedby><cites>FETCH-LOGICAL-c500t-5a4d1606ad1d0644038096bd5b034d5313d5248219e99b6314b8de26ac880f823</cites><orcidid>0000-0003-3124-887X ; 0000-0001-5241-9688</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S1931312812001230$$EHTML$$P50$$Gelsevier$$Hfree_for_read</linktohtml><link.rule.ids>230,314,776,780,881,3537,27901,27902,65306</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/22607804$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-00701381$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Sloves, Pierre-Julien</creatorcontrib><creatorcontrib>Delhaye, Stephane</creatorcontrib><creatorcontrib>Mouveaux, Thomas</creatorcontrib><creatorcontrib>Werkmeister, Elisabeth</creatorcontrib><creatorcontrib>Slomianny, Christian</creatorcontrib><creatorcontrib>Hovasse, Agnes</creatorcontrib><creatorcontrib>Dilezitoko Alayi, Tchilabalo</creatorcontrib><creatorcontrib>Callebaut, Isabelle</creatorcontrib><creatorcontrib>Gaji, Rajshekhar Y.</creatorcontrib><creatorcontrib>Schaeffer-Reiss, Christine</creatorcontrib><creatorcontrib>Van Dorsselear, Alain</creatorcontrib><creatorcontrib>Carruthers, Vern B.</creatorcontrib><creatorcontrib>Tomavo, Stanislas</creatorcontrib><title>Toxoplasma Sortilin-like Receptor Regulates Protein Transport and Is Essential for Apical Secretory Organelle Biogenesis and Host Infection</title><title>Cell host & microbe</title><addtitle>Cell Host Microbe</addtitle><description>Apicomplexan parasites have an assortment of unique apical secretory organelles (rhoptries and micronemes), which have crucial functions in host infection. Here, we show that a Toxoplasma gondii sortilin-like receptor (TgSORTLR) is required for the subcellular localization and formation of apical secretory organelles. TgSORTLR is a transmembrane protein that resides within Golgi-endosomal related compartments. The lumenal domain specifically interacts with rhoptry and microneme proteins, while the cytoplasmic tail of TgSORTLR recruits cytosolic sorting machinery involved in anterograde and retrograde protein transport. Ectopic expression of the N-terminal TgSORTLR lumenal domain results in dominant negative effects with the mislocalization of both endogenous TgSORTLR as well as rhoptry and microneme proteins. Conditional ablation of TgSORTLR disrupts rhoptry and microneme biogenesis, inhibits parasite motility, and blocks both invasion into and egress from host cells. Thus, the sortilin-like receptor is essential for protein trafficking and the biogenesis of key secretory organelles in Toxoplasma.
► TgSORTLR is a type I transmembrane cargo receptor protein in T. gondii ► TgSORTLR interacts with MIC and ROP proteins through its lumenal domain ► TgSORTLR recruits endosomal and adaptor proteins through its cytosolic domain ► TgSORTLR is essential for the biogenesis of secretory organelles in T. gondii</description><subject>Adaptor Proteins, Vesicular Transport - metabolism</subject><subject>Animals</subject><subject>Cells, Cultured</subject><subject>Female</subject><subject>Humans</subject><subject>Membrane Proteins</subject><subject>Mice</subject><subject>Mice, Inbred BALB C</subject><subject>Models, Biological</subject><subject>Organelles - metabolism</subject><subject>Protein Binding</subject><subject>Protein Interaction Mapping</subject><subject>Protein Transport</subject><subject>Survival Analysis</subject><subject>Toxoplasma - metabolism</subject><subject>Toxoplasma - pathogenicity</subject><subject>Toxoplasmosis, Animal</subject><issn>1931-3128</issn><issn>1934-6069</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2012</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kUFv1DAQhSMEoqXwBzggH-GQMLYTryNxWarCrrRSEV3OlmNPtl4SO9jZiv4G_jTebumRk0fW997ozSuKtxQqClR83FfmNowVA8oq4BWAeFac05bXpQDRPn-Yackpk2fFq5T2AE0DC_qyOGNMwEJCfV782YbfYRp0GjW5CXF2g_Pl4H4i-Y4GpznEPOwOg54xkW8xzOg82Ubt05Rpor0l60SuUkI_Oz2QPguWkzN5vEETMRvck-u40x6HAclnF3boMbn0IF2FNJO179HMLvjXxYteDwnfPL4XxY8vV9vLVbm5_rq-XG5K0wDMZaNrS3NCbakFUdfAJbSis00HvLYNp9w2rJaMtti2neC07qRFJrSREnrJ-EXx4eR7qwc1RTfqeK-Cdmq13KjjH8ACKJf0jmb2_YmdYvh1wDSr0SWTs-RA4ZBULiIvEw2XGWUn1MSQUsT-yZvCkRNqr46FqWNhCnheI7Lo3aP_oRvRPkn-NZSBTycA80XuHEaVjENv0LqYz6ZscP_z_wtrjacJ</recordid><startdate>20120517</startdate><enddate>20120517</enddate><creator>Sloves, Pierre-Julien</creator><creator>Delhaye, Stephane</creator><creator>Mouveaux, Thomas</creator><creator>Werkmeister, Elisabeth</creator><creator>Slomianny, Christian</creator><creator>Hovasse, Agnes</creator><creator>Dilezitoko Alayi, Tchilabalo</creator><creator>Callebaut, Isabelle</creator><creator>Gaji, Rajshekhar Y.</creator><creator>Schaeffer-Reiss, Christine</creator><creator>Van Dorsselear, Alain</creator><creator>Carruthers, Vern B.</creator><creator>Tomavo, Stanislas</creator><general>Elsevier Inc</general><general>Elsevier</general><scope>6I.</scope><scope>AAFTH</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>7X8</scope><scope>1XC</scope><orcidid>https://orcid.org/0000-0003-3124-887X</orcidid><orcidid>https://orcid.org/0000-0001-5241-9688</orcidid></search><sort><creationdate>20120517</creationdate><title>Toxoplasma Sortilin-like Receptor Regulates Protein Transport and Is Essential for Apical Secretory Organelle Biogenesis and Host Infection</title><author>Sloves, Pierre-Julien ; Delhaye, Stephane ; Mouveaux, Thomas ; Werkmeister, Elisabeth ; Slomianny, Christian ; Hovasse, Agnes ; Dilezitoko Alayi, Tchilabalo ; Callebaut, Isabelle ; Gaji, Rajshekhar Y. ; Schaeffer-Reiss, Christine ; Van Dorsselear, Alain ; Carruthers, Vern B. ; Tomavo, Stanislas</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c500t-5a4d1606ad1d0644038096bd5b034d5313d5248219e99b6314b8de26ac880f823</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2012</creationdate><topic>Adaptor Proteins, Vesicular Transport - metabolism</topic><topic>Animals</topic><topic>Cells, Cultured</topic><topic>Female</topic><topic>Humans</topic><topic>Membrane Proteins</topic><topic>Mice</topic><topic>Mice, Inbred BALB C</topic><topic>Models, Biological</topic><topic>Organelles - metabolism</topic><topic>Protein Binding</topic><topic>Protein Interaction Mapping</topic><topic>Protein Transport</topic><topic>Survival Analysis</topic><topic>Toxoplasma - metabolism</topic><topic>Toxoplasma - pathogenicity</topic><topic>Toxoplasmosis, Animal</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Sloves, Pierre-Julien</creatorcontrib><creatorcontrib>Delhaye, Stephane</creatorcontrib><creatorcontrib>Mouveaux, Thomas</creatorcontrib><creatorcontrib>Werkmeister, Elisabeth</creatorcontrib><creatorcontrib>Slomianny, Christian</creatorcontrib><creatorcontrib>Hovasse, Agnes</creatorcontrib><creatorcontrib>Dilezitoko Alayi, Tchilabalo</creatorcontrib><creatorcontrib>Callebaut, Isabelle</creatorcontrib><creatorcontrib>Gaji, Rajshekhar Y.</creatorcontrib><creatorcontrib>Schaeffer-Reiss, Christine</creatorcontrib><creatorcontrib>Van Dorsselear, Alain</creatorcontrib><creatorcontrib>Carruthers, Vern B.</creatorcontrib><creatorcontrib>Tomavo, Stanislas</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><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>Hyper Article en Ligne (HAL)</collection><jtitle>Cell host & microbe</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Sloves, Pierre-Julien</au><au>Delhaye, Stephane</au><au>Mouveaux, Thomas</au><au>Werkmeister, Elisabeth</au><au>Slomianny, Christian</au><au>Hovasse, Agnes</au><au>Dilezitoko Alayi, Tchilabalo</au><au>Callebaut, Isabelle</au><au>Gaji, Rajshekhar Y.</au><au>Schaeffer-Reiss, Christine</au><au>Van Dorsselear, Alain</au><au>Carruthers, Vern B.</au><au>Tomavo, Stanislas</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Toxoplasma Sortilin-like Receptor Regulates Protein Transport and Is Essential for Apical Secretory Organelle Biogenesis and Host Infection</atitle><jtitle>Cell host & microbe</jtitle><addtitle>Cell Host Microbe</addtitle><date>2012-05-17</date><risdate>2012</risdate><volume>11</volume><issue>5</issue><spage>515</spage><epage>527</epage><pages>515-527</pages><issn>1931-3128</issn><eissn>1934-6069</eissn><abstract>Apicomplexan parasites have an assortment of unique apical secretory organelles (rhoptries and micronemes), which have crucial functions in host infection. Here, we show that a Toxoplasma gondii sortilin-like receptor (TgSORTLR) is required for the subcellular localization and formation of apical secretory organelles. TgSORTLR is a transmembrane protein that resides within Golgi-endosomal related compartments. The lumenal domain specifically interacts with rhoptry and microneme proteins, while the cytoplasmic tail of TgSORTLR recruits cytosolic sorting machinery involved in anterograde and retrograde protein transport. Ectopic expression of the N-terminal TgSORTLR lumenal domain results in dominant negative effects with the mislocalization of both endogenous TgSORTLR as well as rhoptry and microneme proteins. Conditional ablation of TgSORTLR disrupts rhoptry and microneme biogenesis, inhibits parasite motility, and blocks both invasion into and egress from host cells. Thus, the sortilin-like receptor is essential for protein trafficking and the biogenesis of key secretory organelles in Toxoplasma.
► TgSORTLR is a type I transmembrane cargo receptor protein in T. gondii ► TgSORTLR interacts with MIC and ROP proteins through its lumenal domain ► TgSORTLR recruits endosomal and adaptor proteins through its cytosolic domain ► TgSORTLR is essential for the biogenesis of secretory organelles in T. gondii</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>22607804</pmid><doi>10.1016/j.chom.2012.03.006</doi><tpages>13</tpages><orcidid>https://orcid.org/0000-0003-3124-887X</orcidid><orcidid>https://orcid.org/0000-0001-5241-9688</orcidid><oa>free_for_read</oa></addata></record> |
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| source | MEDLINE; Cell Press Free Archives; Elsevier ScienceDirect Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals |
| subjects | Adaptor Proteins, Vesicular Transport - metabolism Animals Cells, Cultured Female Humans Membrane Proteins Mice Mice, Inbred BALB C Models, Biological Organelles - metabolism Protein Binding Protein Interaction Mapping Protein Transport Survival Analysis Toxoplasma - metabolism Toxoplasma - pathogenicity Toxoplasmosis, Animal |
| title | Toxoplasma Sortilin-like Receptor Regulates Protein Transport and Is Essential for Apical Secretory Organelle Biogenesis and Host Infection |
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