{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,18]],"date-time":"2026-08-18T03:03:28Z","timestamp":1787022208112,"version":"build-2736575974"},"update-to":[{"DOI":"10.1371\/journal.ppat.1011288","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2023,4,6]],"date-time":"2023-04-06T00:00:00Z","timestamp":1680739200000}}],"reference-count":38,"publisher":"Public Library of Science (PLoS)","issue":"3","license":[{"start":{"date-parts":[[2023,3,27]],"date-time":"2023-03-27T00:00:00Z","timestamp":1679875200000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["no. 31872459"],"award-info":[{"award-number":["no. 31872459"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["www.plospathogens.org"],"crossmark-restriction":false},"short-container-title":["PLoS Pathog"],"abstract":"<jats:p>\n                    Exocytosis is a key active process in cells by which proteins are released in bulk via the fusion of exocytic vesicles with the plasma membrane. Soluble N-ethylmaleimide-sensitive factor attachment protein receptor (SNARE) protein-mediated vesicle fusion with the plasma membrane is essential in most exocytotic pathways. In mammalian cells, the vesicular fusion step of exocytosis is normally mediated by Syntaxin-1 (Stx1) and SNAP25 family proteins (SNAP25 and SNAP23). However, in\n                    <jats:italic>Toxoplasma gondii<\/jats:italic>\n                    , a model organism of Apicomplexa, the only SNAP25 family protein, with a SNAP29-like molecular structure, is involved in vesicular fusion at the apicoplast. Here, we reveal that an unconventional SNARE complex comprising TgStx1, TgStx20, and TgStx21 mediates vesicular fusion at the plasma membrane. This complex is essential for the exocytosis of surface proteins and vesicular fusion at the apical annuli in\n                    <jats:italic>T<\/jats:italic>\n                    .\n                    <jats:italic>gondii<\/jats:italic>\n                    .\n                  <\/jats:p>","DOI":"10.1371\/journal.ppat.1011288","type":"journal-article","created":{"date-parts":[[2023,3,27]],"date-time":"2023-03-27T13:34:28Z","timestamp":1679924068000},"page":"e1011288","update-policy":"https:\/\/doi.org\/10.1371\/journal.ppat.corrections_policy","source":"Crossref","is-referenced-by-count":13,"title":["An unconventional SNARE complex mediates exocytosis at the plasma membrane and vesicular fusion at the apical annuli in Toxoplasma gondii"],"prefix":"10.1371","volume":"19","author":[{"given":"Jiawen","family":"Fu","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lin","family":"Zhao","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Juan","family":"Yang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Heming","family":"Chen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shinuo","family":"Cao","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7458-9565","authenticated-orcid":true,"given":"Honglin","family":"Jia","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2023,3,27]]},"reference":[{"key":"ppat.1011288.ref001","doi-asserted-by":"crossref","DOI":"10.12688\/f1000research.16021.1","article-title":"Metabolic interactions between Toxoplasma gondii and its host","volume":"7","author":"M Blume","year":"2018","journal-title":"F1000Res"},{"key":"ppat.1011288.ref002","first-page":"389","article-title":"Toxoplasma gondii Infection in Immunocompromised Patients: A Systematic Review and Meta-Analysis","volume":"8","author":"ZD Wang","year":"2017","journal-title":"Front Microbiol"},{"key":"ppat.1011288.ref003","doi-asserted-by":"crossref","first-page":"398","DOI":"10.1016\/j.micpath.2018.07.041","article-title":"Seroprevalence and associated risk factors of Toxoplasma gondii among Manchu pregnant women in northeastern China","volume":"123","author":"RL Jiang","year":"2018","journal-title":"Microb Pathog"},{"key":"ppat.1011288.ref004","doi-asserted-by":"crossref","first-page":"243","DOI":"10.1146\/annurev.cb.03.110187.001331","article-title":"Constitutive and regulated secretion of proteins","volume":"3","author":"TL Burgess","year":"1987","journal-title":"Annu Rev Cell Biol"},{"issue":"19","key":"ppat.1011288.ref005","doi-asserted-by":"crossref","first-page":"7717","DOI":"10.1073\/pnas.87.19.7717","article-title":"Exocytic transport vesicles generated in vitro from the trans-Golgi network carry secretory and plasma membrane proteins","volume":"87","author":"J Salamero","year":"1990","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"8","key":"ppat.1011288.ref006","doi-asserted-by":"crossref","first-page":"R397","DOI":"10.1016\/j.cub.2018.01.005","article-title":"SNARE complex assembly and disassembly","volume":"28","author":"TY Yoon","year":"2018","journal-title":"Curr Biol"},{"issue":"26","key":"ppat.1011288.ref007","doi-asserted-by":"crossref","first-page":"15781","DOI":"10.1073\/pnas.95.26.15781","article-title":"Conserved structural features of the synaptic fusion complex: SNARE proteins reclassified as Q- and R-SNAREs","volume":"95","author":"D Fasshauer","year":"1998","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"7419","key":"ppat.1011288.ref008","doi-asserted-by":"crossref","first-page":"201","DOI":"10.1038\/nature11320","article-title":"Molecular machines governing exocytosis of synaptic vesicles","volume":"490","author":"R Jahn","year":"2012","journal-title":"Nature"},{"issue":"11","key":"ppat.1011288.ref009","doi-asserted-by":"crossref","first-page":"8240","DOI":"10.1074\/jbc.275.11.8240","article-title":"Role of SNAP23 in insulin-induced translocation of GLUT4 in 3T3-L1 adipocytes. Mediation of complex formation between syntaxin4 and VAMP2","volume":"275","author":"M Kawanishi","year":"2000","journal-title":"J Biol Chem"},{"key":"ppat.1011288.ref010","doi-asserted-by":"crossref","first-page":"97","DOI":"10.1016\/j.neulet.2017.01.031","article-title":"Syntaxin-4 and SNAP23 act as exocytic SNAREs to release NGF from cultured Schwann cells","volume":"653","author":"M Lin","year":"2017","journal-title":"Neurosci Lett"},{"issue":"12","key":"ppat.1011288.ref011","doi-asserted-by":"crossref","first-page":"3499","DOI":"10.1021\/bi036338y","article-title":"Syntaxin 2 and SNAP-23 are required for regulated surfactant secretion","volume":"43","author":"BO Abonyo","year":"2004","journal-title":"Biochemistry"},{"issue":"10","key":"ppat.1011288.ref012","doi-asserted-by":"crossref","first-page":"6686","DOI":"10.4049\/jimmunol.175.10.6686","article-title":"Identification of soluble N-ethylmaleimide-sensitive factor attachment protein receptor exocytotic machinery in human plasma cells: SNAP-23 is essential for antibody secretion","volume":"175","author":"E Reales","year":"2005","journal-title":"J Immunol"},{"issue":"6","key":"ppat.1011288.ref013","doi-asserted-by":"crossref","first-page":"1256","DOI":"10.1016\/j.cell.2012.11.001","article-title":"The hairpin-type tail-anchored SNARE syntaxin 17 targets to autophagosomes for fusion with endosomes\/lysosomes","volume":"151","author":"E Itakura","year":"2012","journal-title":"Cell"},{"key":"ppat.1011288.ref014","first-page":"1","article-title":"Apicoplast biogenesis mediated by ATG8 requires the ATG12-ATG5-ATG16L and SNAP29 complexes in Toxoplasma gondii","author":"J Fu","year":"2022","journal-title":"Autophagy"},{"issue":"5","key":"ppat.1011288.ref015","doi-asserted-by":"crossref","first-page":"e1008106","DOI":"10.1371\/journal.ppat.1008106","article-title":"Rab11A regulates dense granule transport and secretion during Toxoplasma gondii invasion of host cells and parasite replication","volume":"16","author":"K Venugopal","year":"2020","journal-title":"PLoS Pathog"},{"issue":"9","key":"ppat.1011288.ref016","doi-asserted-by":"crossref","first-page":"2202","DOI":"10.1093\/emboj\/20.9.2202","article-title":"SNAREs are concentrated in cholesterol-dependent clusters that define docking and fusion sites for exocytosis","volume":"20","author":"T Lang","year":"2001","journal-title":"EMBO J"},{"issue":"48","key":"ppat.1011288.ref017","doi-asserted-by":"crossref","first-page":"20804","DOI":"10.1073\/pnas.1014823107","article-title":"Syntaxin clusters assemble reversibly at sites of secretory granules in live cells","volume":"107","author":"S Barg","year":"2010","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"4","key":"ppat.1011288.ref018","doi-asserted-by":"crossref","first-page":"e0138021","DOI":"10.1128\/mBio.01380-21","article-title":"The Dissection of SNAREs Reveals Key Factors for Vesicular Trafficking to the Endosome-like Compartment and Apicoplast via the Secretory System in Toxoplasma gondii","volume":"12","author":"S Cao","year":"2021","journal-title":"mBio"},{"key":"ppat.1011288.ref019","doi-asserted-by":"crossref","first-page":"11191","DOI":"10.1038\/ncomms11191","article-title":"Unconventional endosome-like compartment and retromer complex in Toxoplasma gondii govern parasite integrity and host infection","volume":"7","author":"LO Sangare","year":"2016","journal-title":"Nat Commun"},{"issue":"31","key":"ppat.1011288.ref020","doi-asserted-by":"crossref","first-page":"12998","DOI":"10.1073\/pnas.0903831106","article-title":"Host-derived glucose and its transporter in the obligate intracellular pathogen Toxoplasma gondii are dispensable by glutaminolysis","volume":"106","author":"M Blume","year":"2009","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"1","key":"ppat.1011288.ref021","doi-asserted-by":"crossref","first-page":"126","DOI":"10.1074\/jbc.M114.624619","article-title":"Metabolic Cooperation of Glucose and Glutamine Is Essential for the Lytic Cycle of Obligate Intracellular Parasite Toxoplasma gondii","volume":"291","author":"R Nitzsche","year":"2016","journal-title":"J Biol Chem"},{"issue":"2","key":"ppat.1011288.ref022","doi-asserted-by":"crossref","first-page":"60","DOI":"10.1016\/j.pt.2014.12.002","article-title":"Toxoplasma secretory granules: one population or more?","volume":"31","author":"C Mercier","year":"2015","journal-title":"Trends Parasitol"},{"issue":"12","key":"ppat.1011288.ref023","doi-asserted-by":"crossref","first-page":"4235","DOI":"10.1083\/jcb.201701108","article-title":"The parasite Toxoplasma sequesters diverse Rab host vesicles within an intravacuolar network","volume":"216","author":"JD Romano","year":"2017","journal-title":"J Cell Biol"},{"issue":"2","key":"ppat.1011288.ref024","doi-asserted-by":"crossref","first-page":"C545","DOI":"10.1152\/ajpcell.00097.2008","article-title":"Active Rab11 and functional recycling endosome are required for E-cadherin trafficking and lumen formation during epithelial morphogenesis","volume":"295","author":"M Desclozeaux","year":"2008","journal-title":"Am J Physiol Cell Physiol"},{"issue":"6","key":"ppat.1011288.ref025","doi-asserted-by":"crossref","first-page":"406","DOI":"10.1111\/tra.12565","article-title":"Rab11 mediates selective recycling and endocytic trafficking in Trypanosoma brucei","volume":"19","author":"K Umaer","year":"2018","journal-title":"Traffic"},{"issue":"7","key":"ppat.1011288.ref026","doi-asserted-by":"crossref","first-page":"e1001029","DOI":"10.1371\/journal.ppat.1001029","article-title":"Biogenesis of the inner membrane complex is dependent on vesicular transport by the alveolate specific GTPase Rab11B","volume":"6","author":"C Agop-Nersesian","year":"2010","journal-title":"PLoS Pathog"},{"key":"ppat.1011288.ref027","doi-asserted-by":"crossref","first-page":"257","DOI":"10.1146\/annurev-biophys-060414-033901","article-title":"Structural Biology of the Major Facilitator Superfamily Transporters","volume":"44","author":"N. Yan","year":"2015","journal-title":"Annu Rev Biophys"},{"issue":"7","key":"ppat.1011288.ref028","doi-asserted-by":"crossref","first-page":"910","DOI":"10.1242\/bio.012146","article-title":"SNAP23\/25 and VAMP2 mediate exocytic event of transferrin receptor-containing recycling vesicles","volume":"4","author":"K Kubo","year":"2015","journal-title":"Biol Open"},{"issue":"13","key":"ppat.1011288.ref029","doi-asserted-by":"crossref","first-page":"1817","DOI":"10.1016\/j.yexcr.2011.04.016","article-title":"VAMP3 regulates podosome organisation in macrophages and together with Stx4\/SNAP23 mediates adhesion, cell spreading and persistent migration","volume":"317","author":"KJ Veale","year":"2011","journal-title":"Exp Cell Res"},{"issue":"2","key":"ppat.1011288.ref030","doi-asserted-by":"crossref","first-page":"1236","DOI":"10.1074\/jbc.M410674200","article-title":"The SNARE proteins SNAP-25 and SNAP-23 display different affinities for lipid rafts in PC12 cells. Regulation by distinct cysteine-rich domains","volume":"280","author":"C Salaun","year":"2005","journal-title":"J Biol Chem"},{"issue":"3","key":"ppat.1011288.ref031","article-title":"Ferlins and TgDOC2 in Toxoplasma Microneme, Rhoptry and Dense Granule Secretion","volume":"11","author":"DNA Tagoe","year":"2021","journal-title":"Life (Basel)"},{"issue":"6065","key":"ppat.1011288.ref032","doi-asserted-by":"crossref","first-page":"218","DOI":"10.1126\/science.1210829","article-title":"A DOC2 protein identified by mutational profiling is essential for apicomplexan parasite exocytosis","volume":"335","author":"A Farrell","year":"2012","journal-title":"Science"},{"issue":"2","key":"ppat.1011288.ref033","first-page":"114","article-title":"Sequential protein secretion from three distinct organelles of Toxoplasma gondii accompanies invasion of human fibroblasts","volume":"73","author":"VB Carruthers","year":"1997","journal-title":"Eur J Cell Biol"},{"issue":"1","key":"ppat.1011288.ref034","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1038\/nn783","article-title":"Genetic ablation of the t-SNARE SNAP-25 distinguishes mechanisms of neuroexocytosis","volume":"5","author":"P Washbourne","year":"2002","journal-title":"Nat Neurosci"},{"issue":"1","key":"ppat.1011288.ref035","doi-asserted-by":"crossref","first-page":"e13112","DOI":"10.1111\/cmi.13112","article-title":"The apical annuli of Toxoplasma gondii are composed of coiled-coil and signalling proteins embedded in the inner membrane complex sutures","volume":"22","author":"K Engelberg","year":"2020","journal-title":"Cell Microbiol"},{"issue":"1","key":"ppat.1011288.ref036","doi-asserted-by":"crossref","first-page":"35","DOI":"10.1016\/j.tcb.2013.09.006","article-title":"Tethering the assembly of SNARE complexes","volume":"24","author":"W Hong","year":"2014","journal-title":"Trends Cell Biol"},{"key":"ppat.1011288.ref037","doi-asserted-by":"crossref","first-page":"34448","DOI":"10.1038\/srep34448","article-title":"Characterization of aspartyl aminopeptidase from Toxoplasma gondii","volume":"6","author":"J Zheng","year":"2016","journal-title":"Sci Rep"},{"issue":"1","key":"ppat.1011288.ref038","doi-asserted-by":"crossref","first-page":"208","DOI":"10.1111\/mmi.14411","article-title":"The Sec1\/Munc18-like proteins TgSec1 and TgVps45 play pivotal roles in assembly of the pellicle and sub-pellicle network in Toxoplasma gondii","volume":"113","author":"S Cao","year":"2020","journal-title":"Mol Microbiol"}],"updated-by":[{"DOI":"10.1371\/journal.ppat.1011288","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2023,4,6]],"date-time":"2023-04-06T00:00:00Z","timestamp":1680739200000}}],"container-title":["PLOS Pathogens"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.ppat.1011288","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,4,6]],"date-time":"2023-04-06T13:55:54Z","timestamp":1680789354000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.ppat.1011288"}},"subtitle":[],"editor":[{"given":"Dominique","family":"Soldati-Favre","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2023,3,27]]},"references-count":38,"journal-issue":{"issue":"3","published-online":{"date-parts":[[2023,3,27]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.ppat.1011288","relation":{},"ISSN":["1553-7374"],"issn-type":[{"value":"1553-7374","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,3,27]]}}}