{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,29]],"date-time":"2026-09-29T08:13:33Z","timestamp":1790669613264,"version":"4.1.0"},"reference-count":54,"publisher":"Public Library of Science (PLoS)","issue":"7","license":[{"start":{"date-parts":[[2016,7,26]],"date-time":"2016-07-26T00:00:00Z","timestamp":1469491200000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100000060","name":"National Institute of Allergy and Infectious Diseases","doi-asserted-by":"publisher","award":["R37AI041699"],"award-info":[{"award-number":["R37AI041699"]}],"id":[{"id":"10.13039\/100000060","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS ONE"],"DOI":"10.1371\/journal.pone.0159698","type":"journal-article","created":{"date-parts":[[2016,7,26]],"date-time":"2016-07-26T17:43:29Z","timestamp":1469555009000},"page":"e0159698","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":13,"title":["Legionella pneumophila Type IV Effectors YlfA and YlfB Are SNARE-Like Proteins that Form Homo- and Heteromeric Complexes and Enhance the Efficiency of Vacuole Remodeling"],"prefix":"10.1371","volume":"11","author":[{"given":"Eva M.","family":"Campodonico","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Craig R.","family":"Roy","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shira","family":"Ninio","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2016,7,26]]},"reference":[{"key":"ref1","doi-asserted-by":"crossref","first-page":"286","DOI":"10.1016\/0966-842X(96)10041-X","article-title":"The molecular ecology of legionellae","volume":"4","author":"BS Fields","year":"1996","journal-title":"Trends Microbiol"},{"key":"ref2","first-page":"206","article-title":"The epidemiology of Legionella pneumophila infections","volume":"2","author":"BN Doebbeling","year":"1987","journal-title":"Semin Respir Infect"},{"key":"ref3","doi-asserted-by":"crossref","first-page":"1189","DOI":"10.1056\/NEJM197712012972201","article-title":"Legionnaires&apos; disease: description of an epidemic of pneumonia","volume":"297","author":"DW Fraser","year":"1977","journal-title":"N Engl J Med"},{"key":"ref4","doi-asserted-by":"crossref","first-page":"1197","DOI":"10.1056\/NEJM197712012972202","article-title":"Legionnaires&apos; disease: isolation of a bacterium and demonstration of its role in other respiratory disease","volume":"297","author":"JE McDade","year":"1977","journal-title":"N Engl J Med"},{"key":"ref5","doi-asserted-by":"crossref","first-page":"2108","DOI":"10.1084\/jem.158.6.2108","article-title":"The Legionnaires&apos; disease bacterium (Legionella pneumophila) inhibits phagosome-lysosome fusion in human monocytes","volume":"158","author":"MA Horwitz","year":"1983","journal-title":"J Exp Med"},{"key":"ref6","doi-asserted-by":"crossref","first-page":"668","DOI":"10.1128\/IAI.64.2.668-673.1996","article-title":"Interaction of Legionella pneumophila with Acanthamoeba castellanii: uptake by coiling phagocytosis and inhibition of phagosome-lysosome fusion","volume":"64","author":"JA Bozue","year":"1996","journal-title":"Infect Immun"},{"key":"ref7","doi-asserted-by":"crossref","first-page":"1319","DOI":"10.1084\/jem.158.4.1319","article-title":"Formation of a novel phagosome by the Legionnaires&apos; disease bacterium (Legionella pneumophila) in human monocytes","volume":"158","author":"MA Horwitz","year":"1983","journal-title":"J Exp Med"},{"key":"ref8","doi-asserted-by":"crossref","first-page":"2022","DOI":"10.1128\/AEM.62.6.2022-2028.1996","article-title":"The phagosome containing Legionella pneumophila within the protozoan Hartmannella vermiformis is surrounded by the rough endoplasmic reticulum","volume":"62","author":"Y Abu Kwaik","year":"1996","journal-title":"Appl Environ Microbiol"},{"key":"ref9","doi-asserted-by":"crossref","first-page":"4637","DOI":"10.1242\/jcs.114.24.4637","article-title":"How the parasitic bacterium Legionella pneumophila modifies its phagosome and transforms it into rough ER: implications for conversion of plasma membrane to the ER membrane","volume":"114","author":"LG Tilney","year":"2001","journal-title":"J Cell Sci"},{"key":"ref10","doi-asserted-by":"crossref","first-page":"793","DOI":"10.1111\/j.1462-5822.2005.00666.x","article-title":"Attachment and fusion of endoplasmic reticulum with vacuoles containing Legionella pneumophila","volume":"8","author":"CG Robinson","year":"2006","journal-title":"Cell Microbiol"},{"key":"ref11","doi-asserted-by":"crossref","first-page":"9607","DOI":"10.1073\/pnas.89.20.9607","article-title":"Identification of a Legionella pneumophila locus required for intracellular multiplication in human macrophages","volume":"89","author":"A Marra","year":"1992","journal-title":"Proc Natl Acad Sci USA"},{"key":"ref12","doi-asserted-by":"crossref","first-page":"1669","DOI":"10.1073\/pnas.95.4.1669","article-title":"Host cell killing and bacterial conjugation require overlapping sets of genes within a 22-kb region of the Legionella pneumophila genome","volume":"95","author":"G Segal","year":"1998","journal-title":"Proc Natl Acad Sci USA"},{"key":"ref13","doi-asserted-by":"crossref","first-page":"873","DOI":"10.1126\/science.279.5352.873","article-title":"Conjugative transfer by the virulence system of Legionella pneumophila","volume":"279","author":"JP Vogel","year":"1998","journal-title":"Science"},{"key":"ref14","doi-asserted-by":"crossref","first-page":"7","DOI":"10.1111\/j.1365-2958.1993.tb01092.x","article-title":"Two distinct defects in intracellular growth complemented by a single genetic locus in Legionella pneumophila","volume":"7","author":"KH Berger","year":"1993","journal-title":"Mol Microbiol"},{"key":"ref15","article-title":"Identification of Linked Legionella pneumophila Genes Essential for Intracellular Growth and Evasion of the Endocytic Pathway","author":"HL Andrews","year":"1998","journal-title":"Infect Immun"},{"key":"ref16","doi-asserted-by":"crossref","first-page":"663","DOI":"10.1046\/j.1365-2958.1998.00841.x","article-title":"Legionella pneumophila DotA protein is required for early phagosome trafficking decisions that occur within minutes of bacterial uptake","volume":"28","author":"CR Roy","year":"1998","journal-title":"Mol Microbiol"},{"key":"ref17","doi-asserted-by":"crossref","first-page":"2585","DOI":"10.1128\/IAI.64.7.2585-2594.1996","article-title":"Identification of Legionella pneumophila mutants that have aberrant intracellular fates","volume":"64","author":"MS Swanson","year":"1996","journal-title":"Infect Immun"},{"key":"ref18","doi-asserted-by":"crossref","first-page":"4450","DOI":"10.1128\/IAI.66.9.4450-4460.1998","article-title":"Early events in phagosome establishment are required for intracellular survival of Legionella pneumophila","volume":"66","author":"LA Wiater","year":"1998","journal-title":"Infect Immun"},{"key":"ref19","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1038\/nrmicro1967","article-title":"The Legionella pneumophila replication vacuole: making a cosy niche inside host cells","volume":"7","author":"RR Isberg","year":"2009","journal-title":"Nat Rev Microbiol"},{"key":"ref20","doi-asserted-by":"crossref","first-page":"372","DOI":"10.1016\/j.tim.2007.06.006","article-title":"Effector proteins translocated by Legionella pneumophila: strength in numbers","volume":"15","author":"S Ninio","year":"2007","journal-title":"Trends Microbiol"},{"key":"ref21","doi-asserted-by":"crossref","first-page":"679","DOI":"10.1126\/science.1067025","article-title":"A bacterial guanine nucleotide exchange factor activates ARF on Legionella phagosomes","volume":"295","author":"H Nagai","year":"2002","journal-title":"Science"},{"key":"ref22","doi-asserted-by":"crossref","first-page":"256","DOI":"10.1016\/j.chom.2013.08.010","article-title":"A Rab-centric perspective of bacterial pathogen-occupied vacuoles","volume":"14","author":"RK Sherwood","year":"2013","journal-title":"Cell Host Microbe"},{"key":"ref23","doi-asserted-by":"crossref","first-page":"3048","DOI":"10.1128\/IAI.72.5.3048-3053.2004","article-title":"Legionella pneumophila replication vacuole formation involves rapid recruitment of proteins of the early secretory system","volume":"72","author":"I Derr\u00e9","year":"2004","journal-title":"Infect Immun"},{"key":"ref24","doi-asserted-by":"crossref","first-page":"1201","DOI":"10.1084\/jem.20031706","article-title":"Legionella subvert the functions of Rab1 and Sec22b to create a replicative organelle","volume":"199","author":"JC Kagan","year":"2004","journal-title":"J Exp Med"},{"key":"ref25","doi-asserted-by":"crossref","first-page":"587","DOI":"10.1111\/j.1600-0854.2010.01050.x","article-title":"Legionella pneumophila promotes functional interactions between plasma membrane syntaxins and Sec22b","volume":"11","author":"K Arasaki","year":"2010","journal-title":"Traffic"},{"key":"ref26","doi-asserted-by":"crossref","first-page":"46","DOI":"10.1016\/j.chom.2011.11.009","article-title":"The Legionella pneumophila Effector DrrA Is Sufficient to Stimulate SNARE-Dependent Membrane Fusion","volume":"11","author":"K Arasaki","year":"2012","journal-title":"Cell Host Microbe"},{"key":"ref27","doi-asserted-by":"crossref","first-page":"918","DOI":"10.1111\/j.1365-2958.2005.04595.x","article-title":"A yeast genetic system for the identification and characterization of substrate proteins transferred into host cells by the Legionella pneumophila Dot\/Icm system","volume":"56","author":"EM Campodonico","year":"2005","journal-title":"Mol Microbiol"},{"key":"ref28","doi-asserted-by":"crossref","first-page":"7716","DOI":"10.1128\/JB.187.22.7716-7726.2005","article-title":"Evidence for acquisition of Legionella type IV secretion substrates via interdomain horizontal gene transfer","volume":"187","author":"KS de Felipe","year":"2005","journal-title":"J Bacteriol"},{"key":"ref29","doi-asserted-by":"crossref","first-page":"6017","DOI":"10.1128\/IAI.66.12.6017-6021.1998","article-title":"Chlamydia trachomatis IncA is localized to the inclusion membrane and is recognized by antisera from infected humans and primates","volume":"66","author":"JP Bannantine","year":"1998","journal-title":"Infect Immun"},{"key":"ref30","doi-asserted-by":"crossref","first-page":"35","DOI":"10.1046\/j.1462-5822.2000.00029.x","article-title":"A secondary structure motif predictive of protein localization to the chlamydial inclusion membrane","volume":"2","author":"JP Bannantine","year":"2000","journal-title":"Cell Microbiol"},{"key":"ref31","doi-asserted-by":"crossref","first-page":"360","DOI":"10.1128\/IAI.68.1.360-367.2000","article-title":"Isolates of Chlamydia trachomatis that occupy nonfusogenic inclusions lack IncA, a protein localized to the inclusion membrane","volume":"68","author":"RJ Suchland","year":"2000","journal-title":"Infect Immun"},{"key":"ref32","doi-asserted-by":"crossref","first-page":"e1000022","DOI":"10.1371\/journal.ppat.1000022","article-title":"SNARE protein mimicry by an intracellular bacterium","volume":"4","author":"C Delevoye","year":"2008","journal-title":"PLoS Pathog"},{"key":"ref33","doi-asserted-by":"crossref","first-page":"e69769","DOI":"10.1371\/journal.pone.0069769","article-title":"Two coiled-coil domains of Chlamydia trachomatis IncA affect membrane fusion events during infection","volume":"8","author":"E Ronzone","year":"2013","journal-title":"PLoS ONE"},{"key":"ref34","doi-asserted-by":"crossref","first-page":"841","DOI":"10.1073\/pnas.0304916101","article-title":"Multiple substrates of the Legionella pneumophila Dot\/Icm system identified by interbacterial protein transfer","volume":"101","author":"Z-Q Luo","year":"2004","journal-title":"Proc Natl Acad Sci USA"},{"key":"ref35","doi-asserted-by":"crossref","first-page":"912","DOI":"10.1111\/j.1365-2958.2004.04435.x","article-title":"The Legionella IcmS-IcmW protein complex is important for Dot\/Icm-mediated protein translocation","volume":"55","author":"S Ninio","year":"2005","journal-title":"Mol Microbiol"},{"key":"ref36","doi-asserted-by":"crossref","first-page":"719","DOI":"10.1046\/j.1365-2958.2000.02176.x","article-title":"Identification of Icm protein complexes that play distinct roles in the biogenesis of an organelle permissive for Legionella pneumophila intracellular growth","volume":"38","author":"J Coers","year":"2000","journal-title":"Mol Microbiol"},{"key":"ref37","doi-asserted-by":"crossref","first-page":"415","DOI":"10.1083\/jcb.200205011","article-title":"The road less traveled: transport of Legionella to the endoplasmic reticulum","volume":"158","author":"CR Roy","year":"2002","journal-title":"J Cell Biol"},{"key":"ref38","doi-asserted-by":"crossref","first-page":"945","DOI":"10.1038\/ncb883","article-title":"Legionella phagosomes intercept vesicular traffic from endoplasmic reticulum exit sites","volume":"4","author":"JC Kagan","year":"2002","journal-title":"Nat Cell Biol"},{"key":"ref39","doi-asserted-by":"crossref","first-page":"1165","DOI":"10.1038\/ng1447","article-title":"Evidence in the Legionella pneumophila genome for exploitation of host cell functions and high genome plasticity","volume":"36","author":"C Cazalet","year":"2004","journal-title":"Nat Genet"},{"key":"ref40","article-title":"Identification and Characterization of the Legionella Pneumophila Dot\/Icm Substrates YlfA and YlfB","author":"EM Campodonico","year":"2007"},{"key":"ref41","doi-asserted-by":"crossref","first-page":"e1001216","DOI":"10.1371\/journal.ppat.1001216","article-title":"Legionella metaeffector exploits host proteasome to temporally regulate cognate effector","volume":"6","author":"T Kubori","year":"2010","journal-title":"PLoS Pathog"},{"key":"ref42","doi-asserted-by":"crossref","first-page":"46896","DOI":"10.1074\/jbc.M407227200","article-title":"Conservation of the biochemical properties of IncA from Chlamydia trachomatis and Chlamydia caviae: oligomerization of IncA mediates interaction between facing membranes","volume":"279","author":"C Delevoye","year":"2004","journal-title":"J Biol Chem"},{"key":"ref43","doi-asserted-by":"crossref","first-page":"e1000117","DOI":"10.1371\/journal.ppat.1000117","article-title":"Legionella eukaryotic-like type IV substrates interfere with organelle trafficking","volume":"4","author":"KS de Felipe","year":"2008","journal-title":"PLoS Pathog"},{"key":"ref44","doi-asserted-by":"crossref","first-page":"e56798","DOI":"10.1371\/journal.pone.0056798","article-title":"LegC3, an effector protein from Legionella pneumophila, inhibits homotypic yeast vacuole fusion in vivo and in vitro","volume":"8","author":"TL Bennett","year":"2013","journal-title":"PLoS ONE"},{"key":"ref45","doi-asserted-by":"crossref","first-page":"437","DOI":"10.1128\/JCM.10.4.437-441.1979","article-title":"Charcoal-yeast extract agar: primary isolation medium for Legionella pneumophila","volume":"10","author":"JC Feeley","year":"1979","journal-title":"J Clin Microbiol"},{"key":"ref46","doi-asserted-by":"crossref","first-page":"55","DOI":"10.1084\/jem.160.1.55","article-title":"Evidence for a gamma-interferon receptor that regulates macrophage tumoricidal activity","volume":"160","author":"A Celada","year":"1984","journal-title":"J Exp Med"},{"key":"ref47","doi-asserted-by":"crossref","first-page":"3971","DOI":"10.1128\/IAI.68.7.3971-3982.2000","article-title":"Identification and subcellular localization of the Legionella pneumophila IcmX protein: a factor essential for establishment of a replicative organelle in eukaryotic host cells","volume":"68","author":"M Matthews","year":"2000","journal-title":"Infect Immun"},{"key":"ref48","doi-asserted-by":"crossref","first-page":"105","DOI":"10.1016\/0022-2836(82)90515-0","article-title":"A simple method for displaying the hydropathic character of a protein","volume":"157","author":"J Kyte","year":"1982","journal-title":"J Mol Biol"},{"key":"ref49","article-title":"Biol Chem Hoppe-Seyler","volume":"374","author":"K Hofmann","year":"1993"},{"key":"ref50","first-page":"175","article-title":"A hidden Markov model for predicting transmembrane helices in protein sequences","volume":"6","author":"EL Sonnhammer","year":"1998","journal-title":"Proc Int Conf Intell Syst Mol Biol"},{"key":"ref51","doi-asserted-by":"crossref","first-page":"990","DOI":"10.1046\/j.1365-2958.1999.01410.x","article-title":"Pore-forming activity is not sufficient for Legionella pneumophila phagosome trafficking and intracellular growth","volume":"32","author":"DM Zuckman","year":"1999","journal-title":"Mol Microbiol"},{"key":"ref52","doi-asserted-by":"crossref","first-page":"2497","DOI":"10.1128\/IAI.65.6.2497-2501.1997","article-title":"Analysis of the Legionella pneumophila fliI gene: intracellular growth of a defined mutant defective for flagellum biosynthesis","volume":"65","author":"JJ Merriam","year":"1997","journal-title":"Infect Immun"},{"key":"ref53","doi-asserted-by":"crossref","first-page":"451","DOI":"10.1038\/15687","article-title":"Modulation of phagosome biogenesis by Legionella pneumophila creates an organelle permissive for intracellular growth","volume":"1","author":"J Coers","year":"1999","journal-title":"Nat Cell Biol"},{"key":"ref54","doi-asserted-by":"crossref","first-page":"262","DOI":"10.1016\/0003-2697(91)90534-Z","article-title":"Eukaryotic proteins expressed in Escherichia coli: an improved thrombin cleavage and purification procedure of fusion proteins with glutathione S-transferase","volume":"192","author":"KL Guan","year":"1991","journal-title":"Anal Biochem"}],"container-title":["PLOS ONE"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/dx.plos.org\/10.1371\/journal.pone.0159698","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,7,3]],"date-time":"2022-07-03T21:21:56Z","timestamp":1656883316000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0159698"}},"subtitle":[],"editor":[{"given":"Zhao-Qing","family":"Luo","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2016,7,26]]},"references-count":54,"journal-issue":{"issue":"7","published-online":{"date-parts":[[2016,7,26]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pone.0159698","relation":{},"ISSN":["1932-6203"],"issn-type":[{"value":"1932-6203","type":"electronic"}],"subject":[],"published":{"date-parts":[[2016,7,26]]}}}