{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,30]],"date-time":"2026-09-30T02:14:58Z","timestamp":1790734498857,"version":"4.1.0"},"update-to":[{"DOI":"10.1371\/journal.ppat.1006186","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2017,2,8]],"date-time":"2017-02-08T00:00:00Z","timestamp":1486512000000}}],"reference-count":58,"publisher":"Public Library of Science (PLoS)","issue":"1","license":[{"start":{"date-parts":[[2017,1,27]],"date-time":"2017-01-27T00:00:00Z","timestamp":1485475200000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100000009","name":"Foundation for the National Institutes of Health","doi-asserted-by":"publisher","award":["R56AI103168"],"award-info":[{"award-number":["R56AI103168"]}],"id":[{"id":"10.13039\/100000009","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000009","name":"Foundation for the National Institutes of Health","doi-asserted-by":"publisher","award":["R21AI105714"],"award-info":[{"award-number":["R21AI105714"]}],"id":[{"id":"10.13039\/100000009","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000009","name":"Foundation for the National Institutes of Health","doi-asserted-by":"publisher","award":["R21AI117205"],"award-info":[{"award-number":["R21AI117205"]}],"id":[{"id":"10.13039\/100000009","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["www.plospathogens.org"],"crossmark-restriction":false},"short-container-title":["PLoS Pathog"],"DOI":"10.1371\/journal.ppat.1006186","type":"journal-article","created":{"date-parts":[[2017,1,27]],"date-time":"2017-01-27T13:36:25Z","timestamp":1485524185000},"page":"e1006186","update-policy":"https:\/\/doi.org\/10.1371\/journal.ppat.corrections_policy","source":"Crossref","is-referenced-by-count":71,"title":["A Legionella Effector Disrupts Host Cytoskeletal Structure by Cleaving Actin"],"prefix":"10.1371","volume":"13","author":[{"given":"Yao","family":"Liu","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wenhan","family":"Zhu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yunhao","family":"Tan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ernesto S.","family":"Nakayasu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Christopher J.","family":"Staiger","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8890-6621","authenticated-orcid":true,"given":"Zhao-Qing","family":"Luo","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2017,1,27]]},"reference":[{"key":"ref1","doi-asserted-by":"crossref","first-page":"506","DOI":"10.1128\/CMR.15.3.506-526.2002","article-title":"Legionella and Legionnaires' disease: 25 years of investigation","volume":"15","author":"BS Fields","year":"2002","journal-title":"Clin Microbiol Rev"},{"key":"ref2","doi-asserted-by":"crossref","first-page":"567","DOI":"10.1146\/annurev.micro.54.1.567","article-title":"Legionella pneumophila pathogesesis: a fateful journey from amoebae to macrophages","volume":"54","author":"MS Swanson","year":"2000","journal-title":"Annu Rev Microbiol"},{"key":"ref3","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 U S A"},{"key":"ref4","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":"ref5","doi-asserted-by":"crossref","first-page":"e17638","DOI":"10.1371\/journal.pone.0017638","article-title":"Comprehensive identification of protein substrates of the Dot\/Icm type IV transporter of Legionella pneumophila","volume":"6","author":"W Zhu","year":"2011","journal-title":"PLoS One"},{"key":"ref6","doi-asserted-by":"crossref","first-page":"971","DOI":"10.1038\/ncb1463","article-title":"The Legionella pneumophila effector protein DrrA is a Rab1 guanine nucleotide-exchange factor","volume":"8","author":"T Murata","year":"2006","journal-title":"Nat Cell Biol"},{"key":"ref7","doi-asserted-by":"crossref","first-page":"47","DOI":"10.1016\/j.devcel.2006.05.013","article-title":"Targeting of host Rab GTPase function by the intravacuolar pathogen Legionella pneumophila","volume":"11","author":"MP Machner","year":"2006","journal-title":"Dev Cell"},{"key":"ref8","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":"ref9","doi-asserted-by":"crossref","first-page":"10538","DOI":"10.1073\/pnas.1402605111","article-title":"The Legionella effector SidC defines a unique family of ubiquitin ligases important for bacterial phagosomal remodeling","volume":"111","author":"F Hsu","year":"2014","journal-title":"Proc Natl Acad Sci U S A"},{"key":"ref10","doi-asserted-by":"crossref","first-page":"1072","DOI":"10.1126\/science.1227026","article-title":"The Legionella effector RavZ inhibits host autophagy through irreversible Atg8 deconjugation","volume":"338","author":"A Choy","year":"2012","journal-title":"Science"},{"key":"ref11","doi-asserted-by":"crossref","first-page":"e00354","DOI":"10.1128\/mBio.00354-15","article-title":"The Legionella Kinase LegK2 Targets the ARP2\/3 Complex To Inhibit Actin Nucleation on Phagosomes and Allow Bacterial Evasion of the Late Endocytic Pathway","volume":"6","author":"C Michard","year":"2015","journal-title":"MBio"},{"key":"ref12","doi-asserted-by":"crossref","first-page":"225","DOI":"10.1016\/j.micinf.2013.11.007","article-title":"A Legionella effector modulates host cytoskeletal structure by inhibiting actin polymerization","volume":"16","author":"Z Guo","year":"2014","journal-title":"Microbes Infect"},{"key":"ref13","doi-asserted-by":"crossref","first-page":"e1002546","DOI":"10.1371\/journal.ppat.1002546","article-title":"The Legionella pneumophila effector VipA is an actin nucleator that alters host cell organelle trafficking","volume":"8","author":"IS Franco","year":"2012","journal-title":"PLoS Pathog"},{"key":"ref14","doi-asserted-by":"crossref","first-page":"935","DOI":"10.1111\/cmi.12450","article-title":"Formation of a pathogen vacuole according to Legionella pneumophila: how to kill one bird with many stones","volume":"17","author":"I Finsel","year":"2015","journal-title":"Cell Microbiol"},{"key":"ref15","doi-asserted-by":"crossref","first-page":"157","DOI":"10.1016\/j.micinf.2012.11.001","article-title":"Cell biology of infection by Legionella pneumophila","volume":"15","author":"L Xu","year":"2013","journal-title":"Microbes Infect"},{"key":"ref16","doi-asserted-by":"crossref","first-page":"1208","DOI":"10.1126\/science.1175862","article-title":"Actin, a central player in cell shape and movement","volume":"326","author":"TD Pollard","year":"2009","journal-title":"Science"},{"key":"ref17","doi-asserted-by":"crossref","first-page":"242","DOI":"10.1016\/j.chom.2013.08.011","article-title":"Arp2\/3-Mediated Actin-Based Motility: A Tail of Pathogen Abuse","volume":"14","author":"MD Welch","year":"2013","journal-title":"Cell Host & Microbe"},{"key":"ref18","doi-asserted-by":"crossref","first-page":"53","DOI":"10.1146\/annurev.cellbio.17.1.53","article-title":"Salmonella interactions with host cells: Type III secretion at work","volume":"17","author":"JE Galan","year":"2001","journal-title":"Annual Review of Cell and Developmental Biology"},{"key":"ref19","doi-asserted-by":"crossref","first-page":"159","DOI":"10.1016\/j.chom.2008.05.018","article-title":"Actin and intermediate filaments stabilize the Chlamydia trachomatis vacuole by forming dynamic structural scaffolds","volume":"4","author":"Y Kumar","year":"2008","journal-title":"Cell Host & Microbe"},{"key":"ref20","doi-asserted-by":"crossref","first-page":"390","DOI":"10.1038\/322390a0","article-title":"Botulinum C2 toxin ADP-ribosylates actin","volume":"322","author":"K Aktories","year":"1986","journal-title":"Nature"},{"key":"ref21","doi-asserted-by":"crossref","first-page":"1139","DOI":"10.1126\/science.1184557","article-title":"Photorhabdus luminescens toxins ADP-ribosylate actin and RhoA to force actin clustering","volume":"327","author":"AE Lang","year":"2010","journal-title":"Science"},{"key":"ref22","doi-asserted-by":"crossref","first-page":"111","DOI":"10.1042\/CBI20100314","article-title":"Bacterial invasion of eukaryotic cells can be mediated by actin-hydrolysing metalloproteases grimelysin and protealysin","volume":"35","author":"ES Bozhokina","year":"2011","journal-title":"Cell Biology International"},{"key":"ref23","first-page":"1783","article-title":"Induction of caspase 3 activation by multiple Legionella pneumophila Dot\/Icm substrates","volume":"15","author":"WH Zhu","year":"2013","journal-title":"Cellular Microbiology"},{"key":"ref24","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":"ref25","doi-asserted-by":"crossref","first-page":"911","DOI":"10.1111\/j.1462-5822.2009.01301.x","article-title":"Targeting eEF1A by a Legionella pneumophila effector leads to inhibition of protein synthesis and induction of host stress response","volume":"11","author":"X Shen","year":"2009","journal-title":"Cell Microbiol"},{"key":"ref26","doi-asserted-by":"crossref","first-page":"21212","DOI":"10.1073\/pnas.1114023109","article-title":"Legionella pneumophila regulates the small GTPase Rab1 activity by reversible phosphorylcholination","volume":"108","author":"Y Tan","year":"2011","journal-title":"Proc Natl Acad Sci U S A"},{"key":"ref27","doi-asserted-by":"crossref","first-page":"227","DOI":"10.1111\/j.1462-5822.2010.01531.x","article-title":"The E Block motif is associated with Legionella pneumophila translocated substrates","volume":"13","author":"L Huang","year":"2011","journal-title":"Cell Microbiol"},{"key":"ref28","doi-asserted-by":"crossref","first-page":"E344","DOI":"10.1093\/nar\/gks1067","article-title":"New and continuing developments at PROSITE","volume":"41","author":"CJA Sigrist","year":"2013","journal-title":"Nucleic Acids Research"},{"key":"ref29","doi-asserted-by":"crossref","first-page":"211","DOI":"10.1016\/0014-5793(89)80471-5","article-title":"A unique signature identifies a family of zinc-dependent metallopeptidases","volume":"242","author":"CV Jongeneel","year":"1989","journal-title":"FEBS Lett"},{"key":"ref30","doi-asserted-by":"crossref","first-page":"169","DOI":"10.1146\/annurev-biophys-042910-155359","article-title":"Actin structure and function","volume":"40","author":"R Dominguez","year":"2011","journal-title":"Annu Rev Biophys"},{"key":"ref31","doi-asserted-by":"crossref","first-page":"48","DOI":"10.1016\/S0955-0674(05)80007-9","article-title":"Actin isoforms","volume":"5","author":"IM Herman","year":"1993","journal-title":"Curr Opin Cell Biol"},{"key":"ref32","doi-asserted-by":"crossref","first-page":"7360","DOI":"10.1021\/ja9906960","article-title":"Manganese as a replacement for magnesium and zinc: Functional comparison of the divalent ions","volume":"121","author":"CW Bock","year":"1999","journal-title":"Journal of the American Chemical Society"},{"key":"ref33","doi-asserted-by":"crossref","first-page":"2087","DOI":"10.1073\/pnas.0409468102","article-title":"Molecular characterization of proteolytic cleavage sites of the Pseudomonas syringae effector AvrRpt2","volume":"102","author":"ST Chisholm","year":"2005","journal-title":"Proc Natl Acad Sci U S A"},{"key":"ref34","doi-asserted-by":"crossref","first-page":"503","DOI":"10.1093\/oxfordjournals.jbchem.a123929","article-title":"Human T cell L-plastin bundles actin filaments in a calcium-dependent manner","volume":"112","author":"Y Namba","year":"1992","journal-title":"J Biochem"},{"key":"ref35","doi-asserted-by":"crossref","first-page":"167","DOI":"10.1038\/ng.3481","article-title":"Genomic analysis of 38 Legionella species identifies large and diverse effector repertoires","volume":"48","author":"D Burstein","year":"2016","journal-title":"Nat Genet"},{"key":"ref36","doi-asserted-by":"crossref","first-page":"500","DOI":"10.1038\/375500a0","article-title":"Glucosylation of Rho proteins by Clostridium difficile toxin B","volume":"375","author":"I Just","year":"1995","journal-title":"Nature"},{"key":"ref37","doi-asserted-by":"crossref","first-page":"575","DOI":"10.1016\/S0092-8674(02)00766-3","article-title":"A Yersinia effector and a Pseudomonas avirulence protein define a family of cysteine proteases functioning in bacterial pathogenesis","volume":"109","author":"F Shao","year":"2002","journal-title":"Cell"},{"key":"ref38","doi-asserted-by":"crossref","first-page":"269","DOI":"10.1126\/science.1166382","article-title":"AMPylation of Rho GTPases by Vibrio VopS disrupts effector binding and downstream signaling","volume":"323","author":"ML Yarbrough","year":"2009","journal-title":"Science"},{"key":"ref39","doi-asserted-by":"crossref","first-page":"725","DOI":"10.1038\/42735","article-title":"Gln 63 of Rho is deamidated by Escherichia coli cytotoxic necrotizing factor-1","volume":"387","author":"G Schmidt","year":"1997","journal-title":"Nature"},{"key":"ref40","doi-asserted-by":"crossref","first-page":"93","DOI":"10.1016\/j.molcel.2009.03.008","article-title":"The fic domain: regulation of cell signaling by adenylylation","volume":"34","author":"CA Worby","year":"2009","journal-title":"Mol Cell"},{"key":"ref41","doi-asserted-by":"crossref","first-page":"293","DOI":"10.1038\/45829","article-title":"A salmonella protein antagonizes Rac-1 and Cdc42 to mediate host-cell recovery after bacterial invasion","volume":"401","author":"Y Fu","year":"1999","journal-title":"Nature"},{"key":"ref42","doi-asserted-by":"crossref","first-page":"36369","DOI":"10.1074\/jbc.274.51.36369","article-title":"The N-terminal domain of Pseudomonas aeruginosa exoenzyme S is a GTPase-activating protein for Rho GTPases","volume":"274","author":"UM Goehring","year":"1999","journal-title":"J Biol Chem"},{"key":"ref43","doi-asserted-by":"crossref","first-page":"815","DOI":"10.1016\/S0092-8674(00)81442-7","article-title":"S. typhimurium encodes an activator of Rho GTPases that induces membrane ruffling and nuclear responses in host cells","volume":"93","author":"WD Hardt","year":"1998","journal-title":"Cell"},{"key":"ref44","doi-asserted-by":"crossref","first-page":"535","DOI":"10.1126\/science.aab4090","article-title":"ACTIN-DIRECTED TOXIN. ACD toxin-produced actin oligomers poison formin-controlled actin polymerization","volume":"349","author":"DB Heisler","year":"2015","journal-title":"Science"},{"key":"ref45","doi-asserted-by":"crossref","first-page":"1440","DOI":"10.1126\/science.1229556","article-title":"Aggravating genetic interactions allow a solution to redundancy in a bacterial pathogen","volume":"338","author":"TJ O'Connor","year":"2012","journal-title":"Science"},{"key":"ref46","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":"ref47","doi-asserted-by":"crossref","first-page":"305","DOI":"10.1046\/j.1365-2958.2003.03400.x","article-title":"The Legionella pneumophila LidA protein: a translocated substrate of the Dot\/Icm system associated with maintenance of bacterial integrity","volume":"48","author":"GM Conover","year":"2003","journal-title":"Molecular Microbiology"},{"key":"ref48","doi-asserted-by":"crossref","first-page":"e1000822","DOI":"10.1371\/journal.ppat.1000822","article-title":"Inhibition of host vacuolar H+-ATPase activity by a Legionella pneumophila effector","volume":"6","author":"L Xu","year":"2010","journal-title":"PLoS Pathog"},{"key":"ref49","doi-asserted-by":"crossref","first-page":"749","DOI":"10.1093\/genetics\/142.3.749","article-title":"Mutations in the RNA polymerase II transcription machinery suppress the hyperrecombination mutant hpr1 delta of Saccharomyces cerevisiae","volume":"142","author":"HY Fan","year":"1996","journal-title":"Genetics"},{"key":"ref50","doi-asserted-by":"crossref","first-page":"355","DOI":"10.1002\/yea.320110408","article-title":"Studies on the transformation of intact yeast cells by the LiAc\/SS-DNA\/PEG procedure","volume":"11","author":"RD Gietz","year":"1995","journal-title":"Yeast"},{"key":"ref51","doi-asserted-by":"crossref","first-page":"506","DOI":"10.1038\/nature10307","article-title":"Legionella pneumophila SidD is a deAMPylase that modifies Rab1","volume":"475","author":"Y Tan","year":"2011","journal-title":"Nature"},{"key":"ref52","doi-asserted-by":"crossref","first-page":"3609","DOI":"10.1128\/IAI.63.9.3609-3620.1995","article-title":"Association of Legionella pneumophila with the macrophage endoplasmic reticulum","volume":"63","author":"MS Swanson","year":"1995","journal-title":"Infect Immun"},{"key":"ref53","doi-asserted-by":"crossref","first-page":"e1004222","DOI":"10.1371\/journal.ppat.1004222","article-title":"The machinery at endoplasmic reticulum-plasma membrane contact sites contributes to spatial regulation of multiple Legionella effector proteins","volume":"10","author":"A Hubber","year":"2014","journal-title":"PLoS Pathog"},{"key":"ref54","doi-asserted-by":"crossref","first-page":"169","DOI":"10.1083\/jcb.135.1.169","article-title":"Dynamics of capping protein and actin assembly in vitro: uncapping barbed ends by polyphosphoinositides","volume":"135","author":"DA Schafer","year":"1996","journal-title":"J Cell Biol"},{"key":"ref55","doi-asserted-by":"crossref","first-page":"54","DOI":"10.1016\/j.devcel.2014.10.026","article-title":"Profilin-1 serves as a gatekeeper for actin assembly by Arp2\/3-dependent and -independent pathways","volume":"32","author":"JD Rotty","year":"2015","journal-title":"Dev Cell"},{"key":"ref56","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":"ref57","doi-asserted-by":"crossref","first-page":"317","DOI":"10.1016\/0092-8674(89)90846-5","article-title":"Fc receptor isoforms exhibit distinct abilities for coated pit localization as a result of cytoplasmic domain heterogeneity","volume":"58","author":"HM Miettinen","year":"1989","journal-title":"Cell"},{"key":"ref58","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":"ZQ Luo","year":"2004","journal-title":"Proc Natl Acad Sci U S A"}],"updated-by":[{"DOI":"10.1371\/journal.ppat.1006186","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2017,2,8]],"date-time":"2017-02-08T00:00:00Z","timestamp":1486512000000}}],"container-title":["PLOS Pathogens"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/dx.plos.org\/10.1371\/journal.ppat.1006186","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,7,22]],"date-time":"2022-07-22T18:45:28Z","timestamp":1658515528000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.ppat.1006186"}},"subtitle":[],"editor":[{"given":"Craig R.","family":"Roy","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2017,1,27]]},"references-count":58,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2017,1,27]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.ppat.1006186","relation":{},"ISSN":["1553-7374"],"issn-type":[{"value":"1553-7374","type":"electronic"}],"subject":[],"published":{"date-parts":[[2017,1,27]]}}}