{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,29]],"date-time":"2026-09-29T15:36:55Z","timestamp":1790696215388,"version":"4.1.0"},"reference-count":60,"publisher":"Public Library of Science (PLoS)","issue":"2","license":[{"start":{"date-parts":[[2020,2,21]],"date-time":"2020-02-21T00:00:00Z","timestamp":1582243200000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"INCT-FCX FAPESP","award":["2013\/11212-9"],"award-info":[{"award-number":["2013\/11212-9"]}]},{"DOI":"10.13039\/501100001807","name":"FAPESP","doi-asserted-by":"crossref","award":["2013\/07467-1"],"award-info":[{"award-number":["2013\/07467-1"]}],"id":[{"id":"10.13039\/501100001807","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS ONE"],"DOI":"10.1371\/journal.pone.0228959","type":"journal-article","created":{"date-parts":[[2020,2,21]],"date-time":"2020-02-21T13:57:30Z","timestamp":1582293450000},"page":"e0228959","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":19,"title":["Secreted autotransporter toxin (Sat) induces cell damage during enteroaggregative Escherichia coli infection"],"prefix":"10.1371","volume":"15","author":[{"given":"Paulo C. G.","family":"Vieira","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5553-6385","authenticated-orcid":true,"given":"Abraham O.","family":"Espinoza-Culup\u00fa","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Roberto","family":"Nepomuceno","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marina R.","family":"Alves","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ivo","family":"Lebrun","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3470-5706","authenticated-orcid":true,"given":"Waldir P.","family":"Elias","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7361-1150","authenticated-orcid":true,"given":"Rita C.","family":"Ruiz","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2020,2,21]]},"reference":[{"key":"pone.0228959.ref001","doi-asserted-by":"crossref","first-page":"597","DOI":"10.1128\/MMBR.62.3.597-635.1998","article-title":"Molecular and Biotechnological Aspects of Microbial Proteases","volume":"62","author":"MB Rao","year":"1998","journal-title":"Microbiol Mol Biol Rev"},{"key":"pone.0228959.ref002","first-page":"195","article-title":"Bacterial Proteases and Virulence","author":"D Frees","year":"2013","journal-title":"Regulated Proteolysis in Microorganisms"},{"key":"pone.0228959.ref003","doi-asserted-by":"crossref","first-page":"1220","DOI":"10.1007\/s00018-008-7565-9","article-title":"Serine peptidases: Classification, structure and function","author":"MJ Page","year":"2008","journal-title":"Cellular and Molecular Life Sciences"},{"key":"pone.0228959.ref004","doi-asserted-by":"crossref","first-page":"370","DOI":"10.1016\/S0966-842X(98)01318-3","article-title":"The great escape: Structure and function of the autotransporter proteins","author":"IR Henderson","year":"1998","journal-title":"Trends in Microbiology"},{"key":"pone.0228959.ref005","doi-asserted-by":"crossref","first-page":"692","DOI":"10.1128\/MMBR.68.4.692-744.2004","article-title":"Type V Protein Secretion Pathway: the Autotransporter Story Type V Protein Secretion Pathway: the Autotransporter Story","volume":"68","author":"IR Henderson","year":"2004","journal-title":"Microbiol Mol Biol Rev"},{"key":"pone.0228959.ref006","doi-asserted-by":"crossref","first-page":"1179","DOI":"10.3390\/toxins2061179","article-title":"Serine protease autotransporters of Enterobacteriaceae (SPATEs): Biogenesis and function","author":"N. Dautin","year":"2010","journal-title":"Toxins"},{"key":"pone.0228959.ref007","doi-asserted-by":"crossref","first-page":"745","DOI":"10.1007\/s00018-013-1355-8","article-title":"Bacterial serine proteases secreted by the autotransporter pathway: Classification, specificity, and role in virulence","volume":"71","author":"F Ruiz-Perez","year":"2014","journal-title":"Cell Mol Life Sci"},{"key":"pone.0228959.ref008","doi-asserted-by":"crossref","first-page":"562","DOI":"10.1016\/j.resmic.2013.03.010","article-title":"Autotransporter secretion: Varying on a theme","volume":"164","author":"J Grijpstra","year":"2013","journal-title":"Res Microbiol"},{"key":"pone.0228959.ref009","doi-asserted-by":"crossref","first-page":"799","DOI":"10.1002\/bies.950151205","article-title":"The secretion pathway of IgA protease\u2010type proteins in gram\u2010negative bacteria","author":"T Klauser","year":"1993","journal-title":"BioEssays"},{"key":"pone.0228959.ref010","doi-asserted-by":"crossref","first-page":"53","DOI":"10.1046\/j.1365-2958.2000.02110.x","article-title":"Identification of Sat, an autotransporter toxin produced by uropathogenic Escherichia coli","volume":"38","author":"DM Guyer","year":"2000","journal-title":"Mol Microbiol"},{"key":"pone.0228959.ref011","doi-asserted-by":"crossref","first-page":"6124","DOI":"10.1128\/IAI.01086-06","article-title":"Protease activity, secretion, cell entry, cytotoxicity, and cellular targets of secreted autotransporter toxin of uropathogenic Escherichia coli","volume":"74","author":"NM Maroncle","year":"2006","journal-title":"Infect Immun"},{"key":"pone.0228959.ref012","doi-asserted-by":"crossref","first-page":"4539","DOI":"10.1128\/IAI.70.8.4539-4546.2002","article-title":"Sat, the secreted autotransporter toxin of uropathogenic Escherichia coli, is a vacuolating cytotoxin for bladder and kidney epithelial cells","volume":"70","author":"DM Guyer","year":"2002","journal-title":"Infect Immun"},{"key":"pone.0228959.ref013","doi-asserted-by":"crossref","first-page":"992","DOI":"10.1111\/j.1462-5822.2011.01595.x","article-title":"Secreted autotransporter toxin (Sat) triggers autophagy in epithelial cells that relies on cell detachment","volume":"13","author":"V Li\u00e9vin-Le Moal","year":"2011","journal-title":"Cell Microbiol"},{"key":"pone.0228959.ref014","first-page":"7105","article-title":"Functional Comparison of Serine Protease Autotransporters of","volume":"70","author":"PR Dutta","year":"2002","journal-title":"Society"},{"key":"pone.0228959.ref015","doi-asserted-by":"crossref","first-page":"574","DOI":"10.1111\/j.1469-0691.2004.00897.x","article-title":"Prevalence of the sat, set and sen genes among diverse serotypes of Shigella flexneri strains isolated from patients with acute diarrhoea","volume":"10","author":"SK Niyogi","year":"2004","journal-title":"Clin Microbiol Infect"},{"key":"pone.0228959.ref016","doi-asserted-by":"crossref","first-page":"249","DOI":"10.1016\/S0378-1097(03)00688-8","article-title":"Prevalence of secreted autotransporter toxin gene among diffusely adhering Escherichia coli isolated from stools of children","volume":"227","author":"CR Taddei","year":"2003","journal-title":"FEMS Microbiol Lett"},{"key":"pone.0228959.ref017","doi-asserted-by":"crossref","first-page":"411","DOI":"10.1128\/AEM.02635-12","article-title":"Autotransporter protein-encoding genes of diarrheagenic Escherichia coli are found in both typical and atypical enteropathogenic E. coli strains","volume":"79","author":"AG Abreu","year":"2013","journal-title":"Appl Environ Microbiol"},{"key":"pone.0228959.ref018","doi-asserted-by":"crossref","first-page":"204","DOI":"10.1111\/j.1462-5822.2006.00782.x","article-title":"The secreted autotransporter toxin, Sat, functions as a virulence factor in Afa\/Dr diffusely adhering Escherichia coli by promoting lesions in tight junction of polarized epithelial cells","volume":"9","author":"J Guignot","year":"2007","journal-title":"Cell Microbiol"},{"key":"pone.0228959.ref019","doi-asserted-by":"crossref","first-page":"294","DOI":"10.4269\/ajtmh.2009.80.294","article-title":"Short Report: High Prevalence of Serine Protease Autotransporter Cytotoxins among Strains of Enteroaggregative Escherichia coli","volume":"80","author":"N Boisen","year":"2009","journal-title":"Am J Trop Med Hyg"},{"key":"pone.0228959.ref020","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1016\/j.meegid.2017.02.018","article-title":"Distribution of serine protease autotransporters of Enterobacteriaceae in typical and atypical enteroaggregative Escherichia coli","volume":"50","author":"FB Andrade","year":"2017","journal-title":"Infect Genet Evol"},{"key":"pone.0228959.ref021","doi-asserted-by":"crossref","first-page":"263","DOI":"10.1016\/j.femsle.2005.07.013","article-title":"Secreted autotransporter toxin produced by a diffusely adhering Escherichia coli strain causes intestinal damage in animal model assays","volume":"250","author":"CR Taddei","year":"2005","journal-title":"FEMS Microbiol Lett"},{"key":"pone.0228959.ref022","doi-asserted-by":"crossref","first-page":"250","DOI":"10.1186\/s12866-015-0591-5","article-title":"The secreted autotransporter toxin (Sat) does not act as a virulence factor in the probiotic Escherichia coli strain Nissle 1917","volume":"15","author":"L Toloza","year":"2015","journal-title":"BMC Microbiol. BMC Microbiology"},{"key":"pone.0228959.ref023","doi-asserted-by":"crossref","first-page":"2015","DOI":"10.1007\/s10096-014-2161-4","article-title":"The high prevalence of serine protease autotransporters of Enterobacteriaceae (SPATEs) in Escherichia coli causing neonatal septicemia","volume":"33","author":"R Tapader","year":"2014","journal-title":"Eur J Clin Microbiol Infect Dis"},{"key":"pone.0228959.ref024","doi-asserted-by":"crossref","first-page":"461","DOI":"10.3109\/23744235.2016.1144142","article-title":"Lethal neonatal meningoencephalitis caused by multi-drug resistant, highly virulent Escherichia coli","volume":"48","author":"J Iqbal","year":"2016","journal-title":"Infect Dis (Auckl)"},{"key":"pone.0228959.ref025","first-page":"71","article-title":"Characterization of Escherichia coli bloodstream isolates associated with mortality","author":"H Miajlovic","year":"2015","journal-title":"J Med Microbiol"},{"key":"pone.0228959.ref026","doi-asserted-by":"crossref","first-page":"1844","DOI":"10.1093\/infdis\/jir189","article-title":"Escherichia coli isolates causing bacteremia via gut translocation and urinary tract infection in young infants exhibit different virulence genotypes","volume":"203","author":"F Mahjoub-Messai","year":"2011","journal-title":"J Infect Dis"},{"key":"pone.0228959.ref027","doi-asserted-by":"crossref","first-page":"872","DOI":"10.1017\/S0950268816003010","article-title":"Two levels of specialization in bacteraemic Escherichia coli strains revealed by their comparison with commensal strains","volume":"145","author":"O Clermont","year":"2017","journal-title":"Epidemiol Infect"},{"key":"pone.0228959.ref028","article-title":"The relation of phylogroups, serogroups, virulence factors and resistance pattern of Escherichia coli isolated from children with septicemia","author":"F Nojoomi","year":"2019","journal-title":"New Microbes New Infect"},{"key":"pone.0228959.ref029","article-title":"Virulence genes and subclone status as markers of experimental virulence in a murine sepsis model among Escherichia coli sequence type 131 clinical isolates from Spain","author":"I Merino","year":"2017","journal-title":"PLoS One"},{"key":"pone.0228959.ref030","doi-asserted-by":"crossref","first-page":"545","DOI":"10.1590\/S0074-02762004000600001","article-title":"Diarrheagenic Escherichia coli categories among the traditional enteropathogenic E. coli O serogroups\u2014A review","author":"LC Campos","year":"2004","journal-title":"Memorias do Instituto Oswaldo Cruz"},{"key":"pone.0228959.ref031","doi-asserted-by":"crossref","first-page":"95","DOI":"10.1111\/j.1574-6968.1997.tb10414.x","article-title":"The traditional enteropathogenic Escherichia coli (EPEC) serogroup O125 comprises serotypes which are mainly associated with the category of enteroaggregative E. coli","volume":"152","author":"GR Freitas Do Valle","year":"1997","journal-title":"FEMS Microbiol Lett"},{"key":"pone.0228959.ref032","doi-asserted-by":"crossref","first-page":"251","DOI":"10.3201\/eid0402.980212","article-title":"Enteroaggregative Escherichia coli","volume":"4","author":"JP Nataro","year":"1998","journal-title":"Emerg Infect Dis"},{"key":"pone.0228959.ref033","first-page":"1232","article-title":"Molecular cloning","volume":"68","author":"J Sambrook","year":"1989","journal-title":"Society"},{"key":"pone.0228959.ref034","article-title":"Polarized Caco-2 cells\u2014Effect of reactive oxygen metabolites on enterocyte barrier function","author":"RD Baker","year":"1995","journal-title":"Dig Dis Sci"},{"key":"pone.0228959.ref035","doi-asserted-by":"crossref","first-page":"95","DOI":"10.1007\/BF02602439","article-title":"An adhesive factor found in strains of Escherichia coli belonging to the traditional infantile enteropathogenic serotypes","volume":"3","author":"A Cravioto","year":"1979","journal-title":"Curr Microbiol"},{"key":"pone.0228959.ref036","doi-asserted-by":"crossref","first-page":"49","DOI":"10.1017\/S0950268802007136","article-title":"Combinations of putative virulence markers in typical and variant enteroaggregative Escherichia coli strains from children with and without diarrhoea","volume":"129","author":"WP Elias","year":"2002","journal-title":"Epidemiol Infect"},{"key":"pone.0228959.ref037","first-page":"6863","article-title":"dentification and Characterization of a Novel Genomic Island Integrated at","volume":"69","author":"H Schmidt","year":"2001","journal-title":"ISociety"},{"key":"pone.0228959.ref038","doi-asserted-by":"crossref","first-page":"431","DOI":"10.1093\/infdis\/jir757","article-title":"Genomic characterization of enteroaggregative Escherichia coli from children in Mali","volume":"205","author":"N Boisen","year":"2012","journal-title":"J Infect Dis"},{"key":"pone.0228959.ref039","doi-asserted-by":"crossref","first-page":"16","DOI":"10.1016\/j.mimet.2014.07.030","article-title":"A sensitive and specific molecular tool for detection of both typical and atypical enteroaggregative Escherichia coli","volume":"106","author":"FB Andrade","year":"2014","journal-title":"J Microbiol Methods"},{"key":"pone.0228959.ref040","article-title":"Molecular characterization of enterotoxigenic Escherichia coli strains isolated from diarrheal patients in Korea during 2003\u20132011","author":"KH Oh","year":"2014","journal-title":"PLoS One"},{"key":"pone.0228959.ref041","doi-asserted-by":"crossref","first-page":"5029","DOI":"10.1128\/IAI.64.12.5029-5034.1996","article-title":"Bacteroides fragilis Toxin Rapidly Intoxicates Human Intestinal Epithelial Cells (HT29 \/ C 1) In Vitro","volume":"64","author":"RF Saidi","year":"1996","journal-title":"Infect Immun"},{"key":"pone.0228959.ref042","doi-asserted-by":"crossref","first-page":"2184","DOI":"10.1128\/IAI.67.5.2184-2192.1999","article-title":"Cytoskeletal effects induced by Pet, the serine protease enterotoxin of enteroaggregative Escherichia coli","volume":"67","author":"F Navarro-Garc\u00eda","year":"1999","journal-title":"Infect Immun"},{"key":"pone.0228959.ref043","article-title":"A simple method for displaying the hydropathic character of a protein","author":"J Kyte","year":"1982","journal-title":"J Mol Biol"},{"key":"pone.0228959.ref044","doi-asserted-by":"crossref","first-page":"2606","DOI":"10.1139\/v82-374","article-title":"Theoretical prediction of protein antigenic determinants from amino acid sequences","volume":"60","author":"S. Fraga","year":"1982","journal-title":"Can J Chem"},{"key":"pone.0228959.ref045","first-page":"34","article-title":"Perfil etiol\u00f3gico da diarr\u00e9ias agudas de crian\u00e7as atendidas em S\u00e4o Paulo \/ Etiologic prosfile of acute diarrhea in children in the city of S\u00e4o Paulo","volume":"78","author":"Marina B Souza","year":"2002","journal-title":"J pediatr (Rio J)"},{"key":"pone.0228959.ref046","article-title":"Autotransporters and virulence of enteroaggregative E","volume":"2","author":"F Navarro-Garcia","year":"2011","journal-title":"coli. Gut Microbes"},{"key":"pone.0228959.ref047","doi-asserted-by":"crossref","first-page":"3155","DOI":"10.1128\/IAI.66.7.3155-3163.1998","article-title":"Pet, an autotransporter enterotoxin from enteroaggregative Escherichia coli","volume":"66","author":"C Eslava","year":"1998","journal-title":"Infect Immun"},{"key":"pone.0228959.ref048","doi-asserted-by":"crossref","first-page":"1005","DOI":"10.2217\/fmb.10.69","article-title":"Enteroaggregative Escherichia coli plasmid-encoded toxin","volume":"5","author":"F. Navarro-Garcia","year":"2010","journal-title":"Futur Microbiol"},{"key":"pone.0228959.ref049","doi-asserted-by":"crossref","first-page":"5920","DOI":"10.1128\/IAI.68.10.5920-5927.2000","article-title":"Pet toxin from enteroaggregative Escherichia coli produces cellular damage associated with fodrin disruption","volume":"68","author":"JM Villaseca","year":"2000","journal-title":"Infect Immun"},{"key":"pone.0228959.ref050","doi-asserted-by":"crossref","DOI":"10.1128\/mBio.00838-13","article-title":"Cytokeratin 8 is an epithelial cell receptor for pet, a cytotoxic serine protease autotransporter of Enterobacteriaceae","volume":"4","author":"R Nava-Acosta","year":"2013","journal-title":"MBio"},{"key":"pone.0228959.ref051","doi-asserted-by":"crossref","first-page":"2101","DOI":"10.1128\/IAI.01515-06","article-title":"Pet, a non-AB toxin, is transported and translocated into epithelial cells by a retrograde trafficking pathway","volume":"75","author":"F Navarro-Garc\u00eda","year":"2007","journal-title":"Infect Immun"},{"key":"pone.0228959.ref052","doi-asserted-by":"crossref","first-page":"2692","DOI":"10.1128\/IAI.67.6.2692-2699.1999","article-title":"Phylogenetic analysis of enteroaggregative and diffusely adherent Escherichia coli","volume":"67","author":"JR Czeczulin","year":"1999","journal-title":"Infect Immun"},{"key":"pone.0228959.ref053","doi-asserted-by":"crossref","first-page":"1827","DOI":"10.1128\/JCM.41.5.1827-1832.2003","article-title":"Virulence markers of enteroaggregative Escherichia coli isolated from children and adults with diarrhea in Bras\u00edlia, Brazil","volume":"41","author":"IC Piva","year":"2003","journal-title":"J Clin Microbiol"},{"key":"pone.0228959.ref054","article-title":"Antisecretory factor peptide AF-16 inhibits the secreted autotransporter toxin-stimulated transcellular and paracellular passages of fluid in cultured human enterocyte-like cells","author":"V Nicolas","year":"2015","journal-title":"Infect Immun"},{"key":"pone.0228959.ref055","doi-asserted-by":"crossref","DOI":"10.1016\/j.ijbiomac.2018.02.091","article-title":"Non-active site mutation (Q123A) in New Delhi metallo-\u03b2-lactamase (NDM-1) enhanced its enzyme activity","author":"A Ali","year":"2018","journal-title":"Int J Biol Macromol"},{"key":"pone.0228959.ref056","doi-asserted-by":"crossref","first-page":"35","DOI":"10.1128\/microbiolspec.UTI-0011-2012","article-title":"Uropathogenic Escherichia coli-Associated Exotoxins","volume":"4","author":"RA Welch","year":"2016","journal-title":"Microbiol Spectr"},{"key":"pone.0228959.ref057","doi-asserted-by":"crossref","first-page":"5587","DOI":"10.1128\/IAI.67.11.5587-5596.1999","article-title":"Characterization of Pic, a secreted protease of Shigella flexneri and enteroaggregative Escherichia coli","volume":"67","author":"IR Henderson","year":"1999","journal-title":"Infect Immun"},{"key":"pone.0228959.ref058","doi-asserted-by":"crossref","first-page":"951","DOI":"10.1046\/j.1365-2958.2002.03094.x","article-title":"Characterization of Cah, a calcium-binding and heat-extractable autotransporter protein of enterohaemorrhagic Escherichia coli","volume":"45","author":"AG Torres","year":"2002","journal-title":"Mol Microbiol"},{"key":"pone.0228959.ref059","doi-asserted-by":"crossref","first-page":"589","DOI":"10.1111\/j.1462-2920.2007.01479.x","article-title":"EhaA is a novel autotransporter protein of enterohemorrhagic Escherichia coli O157:H7 that contributes to adhesion and biofilm formation","volume":"10","author":"TJ Wells","year":"2008","journal-title":"Environ Microbiol"},{"key":"pone.0228959.ref060","first-page":"2","article-title":"Characterization of EhaJ, a new autotransporter protein from enterohemorrhagic and enteropathogenic Escherichia coli","author":"DM Easton","year":"2011","journal-title":"Front Microbiol"}],"container-title":["PLOS ONE"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0228959","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,2,28]],"date-time":"2021-02-28T07:11:41Z","timestamp":1614496301000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0228959"}},"subtitle":[],"editor":[{"given":"Fernando","family":"Navarro-Garcia","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2020,2,21]]},"references-count":60,"journal-issue":{"issue":"2","published-online":{"date-parts":[[2020,2,21]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pone.0228959","relation":{},"ISSN":["1932-6203"],"issn-type":[{"value":"1932-6203","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,2,21]]}}}