{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,31]],"date-time":"2026-10-31T18:50:28Z","timestamp":1793472628758,"version":"4.5.0"},"reference-count":112,"publisher":"Public Library of Science (PLoS)","issue":"6","license":[{"start":{"date-parts":[[2025,6,26]],"date-time":"2025-06-26T00:00:00Z","timestamp":1750896000000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"the Ministry of Science and Higher Education, Science for Society","award":["NdS-II\/SP\/0438\/2024\/01"],"award-info":[{"award-number":["NdS-II\/SP\/0438\/2024\/01"]}]},{"name":"National Science Centre , Poland","award":["UMO-2018\/29\/B\/NZ7\/02489"],"award-info":[{"award-number":["UMO-2018\/29\/B\/NZ7\/02489"]}]}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS One"],"abstract":"<jats:p>The pathogenesis of urosepsis in uncomplicated and community-acquired urinary tract infections (UTIs) caused by <jats:italic>Escherichia coli<\/jats:italic> was studied. We hypothesized that siderophores involved in iron uptake may determine bacterial adaptation to the urine and blood environment in patients with UTI, leading to urosepsis. <jats:italic>E. coli<\/jats:italic> isolates were compared from urosepsis patients (cases) and UTI (control group). The patterns of bacterial DNA fingerprints isolated from the blood and urine of patients with urosepsis were compared by PCR melting profile method to detect urosepsis and exclude nosocomial infection. Chromium Azurol S (CAS) assay and RT-qPCR were used to investigate the expression levels of siderophore genes in artificial urine and M9 supplemented with whole blood. <jats:italic>E. coli<\/jats:italic> isolates from artificial urine were proteomically analysed. The pro-inflammatory factors IL-2,4,6,8,10, IFN-gamma, TNF-alpha and CRP were quantified in the patients\u2019 serum. PCR detected and co-occurrence of enterobactin, aerobactin and yersiniabactin was significantly more frequent in the urosepsis (P\u2009=\u20090.0039) and with the <jats:italic>iha<\/jats:italic> gene may represent markers of urosepsis risk. Aerobactin was dominant in urosepsis (P\u2009=\u20090.03), but its expression in artificial urine was twice higher than in blood (P\u2009=\u20090.03). When cultured in artificial urine, the expression of <jats:italic>entC<\/jats:italic> was significantly higher (P\u2009=\u20090.029), while the expression of <jats:italic>iro-2<\/jats:italic>, <jats:italic>iucA<\/jats:italic> and <jats:italic>iroB<\/jats:italic> were lower in strains obtained from urosepsis (P\u2009=\u20090.007; P\u2009=\u20090.030; P\u2009=\u20090.012; respectively) as compared to the UTI group. Ferritin-1, iron uptake system component EfeO, ferrous iron transport protein B, nitrate\/nitrite response regulator protein NarL, protein HemY, ferrienterobactin receptor FepA, lipopolysaccharide export system protein LptA and 2Fe-2S ferredoxin were found by proteomic analyses in urosepsis only. A positive association of IL-6,8,10, TNF and CRP proteins with urosepsis was observed. In conclusion, risk factors for UTI-related sepsis may be related to the iron uptake system, and genetic and proteomic profiles may help identify them.<\/jats:p>","DOI":"10.1371\/journal.pone.0326251","type":"journal-article","created":{"date-parts":[[2025,6,26]],"date-time":"2025-06-26T17:44:43Z","timestamp":1750959883000},"page":"e0326251","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":12,"title":["Iron uptake by Escherichia coli in urinary tract infections and 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Microbiol"},{"key":"pone.0326251.ref006","doi-asserted-by":"crossref","first-page":"2065","DOI":"10.3389\/fmicb.2020.02065","article-title":"Pathogenicity Factors of Genomic Islands in Intestinal and Extraintestinal Escherichia coli","volume":"11","author":"M Desvaux","year":"2020","journal-title":"Front Microbiol"},{"key":"pone.0326251.ref007","doi-asserted-by":"crossref","first-page":"383","DOI":"10.1016\/j.ijmm.2005.07.005","article-title":"Molecular epidemiology of extraintestinal pathogenic (uropathogenic) Escherichia coli","volume":"295","author":"JR Johnson","year":"2005","journal-title":"Int J Med Microbiol"},{"issue":"3","key":"pone.0326251.ref008","doi-asserted-by":"crossref","DOI":"10.1128\/CMR.00135-18","article-title":"Global Extraintestinal Pathogenic Escherichia coli (ExPEC) Lineages","volume":"32","author":"AR Manges","year":"2019","journal-title":"Clin Microbiol Rev"},{"issue":"2","key":"pone.0326251.ref009","doi-asserted-by":"crossref","first-page":"203","DOI":"10.3343\/alm.2022.42.2.203","article-title":"Virulence Factors Associated With Escherichia coli Bacteremia and Urinary Tract Infection","volume":"42","author":"B Kim","year":"2022","journal-title":"Ann Lab Med"},{"key":"pone.0326251.ref010","doi-asserted-by":"crossref","first-page":"10","DOI":"10.1186\/s13099-019-0290-0","article-title":"Virulence factors, prevalence and potential transmission of extraintestinal pathogenic Escherichia coli isolated from different sources: recent reports","volume":"11","author":"J Sarowska","year":"2019","journal-title":"Gut Pathog"},{"issue":"3","key":"pone.0326251.ref011","doi-asserted-by":"crossref","first-page":"1225","DOI":"10.1128\/IAI.01222-10","article-title":"Redundancy and specificity of Escherichia coli iron acquisition systems during urinary tract infection","volume":"79","author":"EC Garcia","year":"2011","journal-title":"Infect 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pathogen control","volume":"71","author":"M Miethke","year":"2007","journal-title":"Microbiol Mol Biol Rev"},{"issue":"7","key":"pone.0326251.ref016","doi-asserted-by":"crossref","first-page":"1046","DOI":"10.1021\/acs.accounts.3c00814","article-title":"Exploring the antibacterial activity and cellular fates of enterobactin-drug conjugates that target gram-negative bacterial pathogens","volume":"57","author":"C Guo","year":"2024","journal-title":"Acc Chem Res"},{"issue":"5","key":"pone.0326251.ref017","doi-asserted-by":"crossref","first-page":"1931","DOI":"10.1128\/IAI.01174-09","article-title":"Sequence analysis and characterization of a transferable hybrid plasmid encoding multidrug resistance and enabling zoonotic potential for extraintestinal Escherichia coli","volume":"78","author":"TJ Johnson","year":"2010","journal-title":"Infect Immun"},{"key":"pone.0326251.ref018","doi-asserted-by":"crossref","first-page":"215","DOI":"10.1016\/S0168-6445(03)00055-X","article-title":"Bacterial iron homeostasis","volume":"27","author":"SC Andrews","year":"2003","journal-title":"FEMS Microbiol Rev"},{"issue":"1","key":"pone.0326251.ref019","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1016\/j.yexmp.2008.03.007","article-title":"Origins and virulence mechanisms of uropathogenic Escherichia coli","volume":"85","author":"TJ Wiles","year":"2008","journal-title":"Exp Mol Pathol"},{"key":"pone.0326251.ref020","doi-asserted-by":"crossref","first-page":"881","DOI":"10.1146\/annurev.micro.54.1.881","article-title":"Iron metabolism in pathogenic bacteria","volume":"54","author":"C Ratledge","year":"2000","journal-title":"Annu Rev Microbiol"},{"issue":"7019","key":"pone.0326251.ref021","doi-asserted-by":"crossref","first-page":"917","DOI":"10.1038\/nature03104","article-title":"Lipocalin 2 mediates an innate immune response to bacterial infection by sequestrating iron","volume":"432","author":"TH Flo","year":"2004","journal-title":"Nature"},{"issue":"5","key":"pone.0326251.ref022","doi-asserted-by":"crossref","first-page":"1033","DOI":"10.1016\/S1097-2765(02)00708-6","article-title":"The neutrophil lipocalin NGAL is a bacteriostatic agent that interferes with siderophore-mediated iron acquisition","volume":"10","author":"DH Goetz","year":"2002","journal-title":"Molecular Cell"},{"issue":"1","key":"pone.0326251.ref023","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1016\/j.str.2004.10.009","article-title":"Siderocalin (Lcn 2) also binds carboxymycobactins, potentially defending against mycobacterial infections through iron sequestration","volume":"13","author":"MA Holmes","year":"2005","journal-title":"Structure"},{"issue":"34","key":"pone.0326251.ref024","doi-asserted-by":"crossref","first-page":"11524","DOI":"10.1021\/ja803524w","article-title":"The siderocalin\/enterobactin interaction: a link between mammalian immunity and bacterial iron transport","volume":"130","author":"RJ Abergel","year":"2008","journal-title":"J Am Chem Soc"},{"issue":"6","key":"pone.0326251.ref025","doi-asserted-by":"crossref","first-page":"986","DOI":"10.1039\/C4MT00333K","article-title":"Diverging roles of bacterial siderophores during infection","volume":"7","author":"VI Holden","year":"2015","journal-title":"Metallomics"},{"key":"pone.0326251.ref026","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1007\/5584_2017_107","article-title":"Neutrophil gelatinase-associated lipocalin: a biomarker for early diagnosis of urinary tract infections in infants","author":"G Krzemie\u0144","year":"2017","journal-title":"Adv Exp Med Biol"},{"issue":"5","key":"pone.0326251.ref027","doi-asserted-by":"crossref","first-page":"1154","DOI":"10.1021\/acschembio.9b00741","article-title":"Site-Specific Siderocalin Binding to Ferric and Ferric-Free Enterobactin As Revealed by Mass Spectrometry","volume":"15","author":"C Guo","year":"2020","journal-title":"ACS Chem Biol"},{"issue":"7","key":"pone.0326251.ref028","doi-asserted-by":"crossref","first-page":"2963","DOI":"10.1172\/JCI71630","article-title":"\u03b1-Intercalated cells defend the urinary system from bacterial infection","volume":"124","author":"N Paragas","year":"2014","journal-title":"J Clin Invest"},{"issue":"40","key":"pone.0326251.ref029","article-title":"Urinary Biomarkers Improve the Diagnosis of Intrinsic Acute Kidney Injury in Coronary Care Units","volume":"94","author":"C-H Chang","year":"2015","journal-title":"Medicine (Baltimore)"},{"issue":"6","key":"pone.0326251.ref030","doi-asserted-by":"crossref","first-page":"1677","DOI":"10.1681\/ASN.2016101127","article-title":"Perspective on Clinical Application of Biomarkers in AKI","volume":"28","author":"CR Parikh","year":"2017","journal-title":"J Am Soc Nephrol"},{"issue":"4","key":"pone.0326251.ref031","doi-asserted-by":"crossref","first-page":"1911","DOI":"10.4049\/jimmunol.1200892","article-title":"Lipocalin 2 deficiency dysregulates iron homeostasis and exacerbates endotoxin-induced sepsis","volume":"189","author":"G Srinivasan","year":"2012","journal-title":"J Immunol"},{"issue":"2","key":"pone.0326251.ref032","doi-asserted-by":"crossref","DOI":"10.1371\/journal.ppat.1000305","article-title":"Quantitative metabolomics reveals an epigenetic blueprint for iron acquisition in uropathogenic Escherichia coli","volume":"5","author":"JP Henderson","year":"2009","journal-title":"PLoS Pathog"},{"issue":"6","key":"pone.0326251.ref033","doi-asserted-by":"crossref","first-page":"3427","DOI":"10.1128\/IAI.00107-06","article-title":"Iha from an Escherichia coli urinary tract infection outbreak clonal group A strain is expressed in vivo in the mouse urinary tract and functions as a catecholate siderophore receptor","volume":"74","author":"S L\u00e9veill\u00e9","year":"2006","journal-title":"Infect Immun"},{"issue":"3","key":"pone.0326251.ref034","article-title":"Ferric Citrate Uptake Is a Virulence Factor in Uropathogenic Escherichia coli","volume":"13","author":"AE Frick-Cheng","year":"2022","journal-title":"mBio"},{"issue":"1","key":"pone.0326251.ref035","doi-asserted-by":"crossref","first-page":"78","DOI":"10.1016\/S0014-5793(02)03185-X","article-title":"Iron transport and signaling in Escherichia coli","volume":"529","author":"V Braun","year":"2002","journal-title":"FEBS Lett"},{"issue":"1","key":"pone.0326251.ref036","doi-asserted-by":"crossref","first-page":"125","DOI":"10.1039\/C5MT00218D","article-title":"FecB, a periplasmic ferric-citrate transporter from E. coli, can bind different forms of ferric-citrate as well as a wide variety of metal-free and metal-loaded tricarboxylic acids","volume":"8","author":"S Banerjee","year":"2016","journal-title":"Metallomics"},{"issue":"1","key":"pone.0326251.ref037","doi-asserted-by":"crossref","first-page":"79","DOI":"10.1111\/j.1365-2958.2008.06509.x","article-title":"Haem acquisition is facilitated by a novel receptor Hma and required by uropathogenic Escherichia coli for kidney infection","volume":"71","author":"EC Hagan","year":"2009","journal-title":"Mol Microbiol"},{"issue":"12","key":"pone.0326251.ref038","doi-asserted-by":"crossref","first-page":"946","DOI":"10.1038\/nrmicro1046","article-title":"Iron and microbial infection","volume":"2","author":"UE Schaible","year":"2004","journal-title":"Nat Rev Microbiol"},{"issue":"8","key":"pone.0326251.ref039","doi-asserted-by":"crossref","first-page":"3941","DOI":"10.1128\/IAI.00337-07","article-title":"Uropathogenic Escherichia coli outer membrane antigens expressed during urinary tract infection","volume":"75","author":"EC Hagan","year":"2007","journal-title":"Infect Immun"},{"issue":"23","key":"pone.0326251.ref040","doi-asserted-by":"crossref","first-page":"6551","DOI":"10.1128\/JB.184.23.6551-6558.2002","article-title":"Gene expression profiling of the pH response in Escherichia coli","volume":"184","author":"DL Tucker","year":"2002","journal-title":"J Bacteriol"},{"issue":"2","key":"pone.0326251.ref041","doi-asserted-by":"crossref","first-page":"362","DOI":"10.1128\/MMBR.00036-05","article-title":"The Escherichia coli proteome: past, present, and future prospects","volume":"70","author":"M-J Han","year":"2006","journal-title":"Microbiol Mol Biol Rev"},{"issue":"16","key":"pone.0326251.ref042","doi-asserted-by":"crossref","first-page":"1800435","DOI":"10.1002\/pmic.201800435","article-title":"Targeted proteomics for studying pathogenic bacteria","volume":"19","author":"S Saleh","year":"2019","journal-title":"Proteomics"},{"key":"pone.0326251.ref043","doi-asserted-by":"crossref","first-page":"824039","DOI":"10.3389\/fcimb.2022.824039","article-title":"\u201cOmics\u201d Technologies - What Have They Told Us About Uropathogenic Escherichia coli Fitness and Virulence During Urinary Tract Infection?","volume":"12","author":"S Torres-Puig","year":"2022","journal-title":"Front Cell Infect Microbiol"},{"key":"pone.0326251.ref044","doi-asserted-by":"crossref","first-page":"165974","DOI":"10.1155\/2013\/165974","article-title":"Cytokines in sepsis: potent immunoregulators and potential therapeutic targets--an updated view","volume":"2013","author":"W Schulte","year":"2013","journal-title":"Mediators Inflamm"},{"issue":"5","key":"pone.0326251.ref045","doi-asserted-by":"crossref","first-page":"517","DOI":"10.1007\/s00281-017-0639-8","article-title":"Cytokine storm and sepsis disease pathogenesis","volume":"39","author":"BG Chousterman","year":"2017","journal-title":"Semin Immunopathol"},{"issue":"9","key":"pone.0326251.ref046","doi-asserted-by":"crossref","first-page":"872","DOI":"10.3390\/medicina57090872","article-title":"The Urosepsis-A Literature Review","volume":"57","author":"M Guliciuc","year":"2021","journal-title":"Medicina (Kaunas)"},{"key":"pone.0326251.ref047","article-title":"Biomarkers in urinary tract infections - which ones are suitable for diagnostics and follow-up?","volume":"8","author":"J Horv\u00e1th","year":"2020","journal-title":"GMS Infect Dis"},{"key":"pone.0326251.ref048","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1155\/2019\/1089107","article-title":"Diagnosis and prognosis of sepsis based on use of cytokines, chemokines, and growth factors","volume":"2019","author":"DW Jekarl","year":"2019","journal-title":"Dis Markers"},{"issue":"7","key":"pone.0326251.ref049","doi-asserted-by":"crossref","first-page":"2327","DOI":"10.1128\/JCM.00052-06","article-title":"Evaluation of a PCR melting profile technique for bacterial strain differentiation","volume":"44","author":"B Krawczyk","year":"2006","journal-title":"J Clin Microbiol"},{"issue":"6","key":"pone.0326251.ref050","doi-asserted-by":"crossref","first-page":"2206","DOI":"10.1021\/ci0496144","article-title":"Analysis of data fusion methods in virtual screening: similarity and group fusion","volume":"46","author":"M Whittle","year":"2006","journal-title":"J Chem Inf Model"},{"issue":"3","key":"pone.0326251.ref051","doi-asserted-by":"crossref","first-page":"203","DOI":"10.1046\/j.1472-765X.1997.00378.x","article-title":"A simple artificial urine for the growth of urinary pathogens","volume":"24","author":"T Brooks","year":"1997","journal-title":"Lett Appl Microbiol"},{"issue":"1","key":"pone.0326251.ref052","article-title":"rpoB, a promising marker for analyzing the diversity of bacterial communities by amplicon sequencing","volume":"19","author":"J-C Ogier","year":"2019","journal-title":"BMC Microbiology"},{"issue":"1","key":"pone.0326251.ref053","doi-asserted-by":"crossref","first-page":"47","DOI":"10.1016\/0003-2697(87)90612-9","article-title":"Universal chemical assay for the detection and determination of siderophores","volume":"160","author":"B Schwyn","year":"1987","journal-title":"Anal Biochem"},{"issue":"6","key":"pone.0326251.ref054","doi-asserted-by":"crossref","first-page":"381","DOI":"10.1007\/s13205-017-1008-y","article-title":"Modified microplate method for rapid and efficient estimation of siderophore produced by bacteria","volume":"7","author":"NK Arora","year":"2017","journal-title":"3 Biotech"},{"issue":"2","key":"pone.0326251.ref055","doi-asserted-by":"crossref","first-page":"66","DOI":"10.1016\/0966-842X(93)90036-Q","article-title":"Iron acquisition in microbial pathogenesis","volume":"1","author":"SM Payne","year":"1993","journal-title":"Trends Microbiol"},{"issue":"4","key":"pone.0326251.ref056","doi-asserted-by":"crossref","first-page":"2343","DOI":"10.1021\/cr3003533","article-title":"Protein analysis by shotgun\/bottom-up proteomics","volume":"113","author":"Y Zhang","year":"2013","journal-title":"Chem Rev"},{"issue":"3","key":"pone.0326251.ref057","doi-asserted-by":"crossref","first-page":"213","DOI":"10.1139\/cjm-2020-0324","article-title":"Proteomics of host-bacterial interactions: new insights from dual perspectives","volume":"67","author":"A Sukumaran","year":"2021","journal-title":"Can J Microbiol"},{"key":"pone.0326251.ref058","doi-asserted-by":"crossref","DOI":"10.3389\/fvets.2022.1079359","article-title":"Proteomics approaches: A review regarding an importance of proteome analyses in understanding the pathogens and diseases","volume":"9","author":"M Zubair","year":"2022","journal-title":"Front Vet Sci"},{"key":"pone.0326251.ref059","first-page":"125","volume-title":"Proteomics Analysis for Identification and Antimicrobial Resistance Analysis of Bacteria","author":"D Zhang","year":"2023"},{"issue":"2","key":"pone.0326251.ref060","doi-asserted-by":"crossref","first-page":"131","DOI":"10.1016\/j.mimet.2009.04.013","article-title":"Identification of uropathogenic Escherichia coli surface proteins by shotgun proteomics","volume":"78","author":"MS Walters","year":"2009","journal-title":"J Microbiol Methods"},{"issue":"2","key":"pone.0326251.ref061","doi-asserted-by":"crossref","first-page":"112","DOI":"10.1093\/bfgp\/ell018","article-title":"Shotgun proteomics using the iTRAQ isobaric tags","volume":"5","author":"K Aggarwal","year":"2006","journal-title":"Brief Funct Genomics"},{"issue":"5","key":"pone.0326251.ref062","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pone.0233504","article-title":"Linezolid-resistant Enterococcus faecium strains isolated from one hospital in Poland -commensals or hospital-adapted pathogens?","volume":"15","author":"B Krawczyk","year":"2020","journal-title":"PLoS One"},{"issue":"6","key":"pone.0326251.ref063","doi-asserted-by":"crossref","DOI":"10.1007\/s10096-015-2331-z","article-title":"Characterisation of Escherichia coli isolates from the blood of haematological adult patients with bacteraemia: translocation from gut to blood requires the cooperation of multiple virulence factors","volume":"34","author":"B Krawczyk","year":"2015","journal-title":"Eur J Clin Microbiol Infect Dis"},{"issue":"2","key":"pone.0326251.ref064","doi-asserted-by":"crossref","first-page":"138","DOI":"10.1056\/NEJMra021333","article-title":"The pathophysiology and treatment of sepsis","volume":"348","author":"RS Hotchkiss","year":"2003","journal-title":"N Engl J Med"},{"issue":"1154","key":"pone.0326251.ref065","doi-asserted-by":"crossref","first-page":"803","DOI":"10.1136\/postgradmedj-2020-139090","article-title":"Symptoms, risk factors, diagnosis and treatment of urinary tract infections","volume":"97","author":"R Kaur","year":"2021","journal-title":"Postgrad Med J"},{"issue":"13","key":"pone.0326251.ref066","doi-asserted-by":"crossref","first-page":"10537","DOI":"10.3390\/ijms241310537","article-title":"Urinary Tract Infections Caused by Uropathogenic Escherichia coli: Mechanisms of Infection and Treatment Options","volume":"24","author":"Y Zhou","year":"2023","journal-title":"Int J Mol Sci"},{"issue":"5","key":"pone.0326251.ref067","doi-asserted-by":"crossref","first-page":"509","DOI":"10.1016\/j.chom.2013.04.010","article-title":"Iron in infection and immunity","volume":"13","author":"JE Cassat","year":"2013","journal-title":"Cell Host Microbe"},{"key":"pone.0326251.ref068","doi-asserted-by":"crossref","first-page":"1566","DOI":"10.3389\/fmicb.2017.01566","article-title":"UroPathogenic Escherichia coli (UPEC) Infections: Virulence Factors, Bladder Responses, Antibiotic, and Non-antibiotic Antimicrobial Strategies","volume":"8","author":"ME Terlizzi","year":"2017","journal-title":"Front Microbiol"},{"issue":"3","key":"pone.0326251.ref069","doi-asserted-by":"crossref","first-page":"412","DOI":"10.1080\/19490976.2018.1546519","article-title":"The bacterial siderophore enterobactin confers survival advantage to Salmonella in macrophages","volume":"10","author":"P Saha","year":"2019","journal-title":"Gut Microbes"},{"issue":"6","key":"pone.0326251.ref070","doi-asserted-by":"crossref","DOI":"10.1128\/mBio.00224-11","article-title":"Interaction of lipocalin 2, transferrin, and siderophores determines the replicative niche of Klebsiella pneumoniae during pneumonia","volume":"3","author":"MA Bachman","year":"2012","journal-title":"MBio"},{"issue":"13","key":"pone.0326251.ref071","doi-asserted-by":"crossref","first-page":"1881","DOI":"10.1096\/fj.05-3809fje","article-title":"Lipocalin 2 functions as a negative regulator of red blood cell production in an autocrine fashion","volume":"19","author":"K Miharada","year":"2005","journal-title":"FASEB J"},{"issue":"7","key":"pone.0326251.ref072","doi-asserted-by":"crossref","first-page":"745","DOI":"10.2217\/fmb-2017-0295","article-title":"The iron hand of uropathogenic Escherichia coli: the role of transition metal control in virulence","volume":"13","author":"AE Robinson","year":"2018","journal-title":"Future Microbiol"},{"key":"pone.0326251.ref073","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1016\/j.ijmm.2004.06.026","article-title":"The Yersinia high-pathogenicity island (HPI): evolutionary and functional aspects","volume":"294","author":"S Schubert","year":"2004","journal-title":"Int J Med Microbiol"},{"issue":"1","key":"pone.0326251.ref074","doi-asserted-by":"crossref","DOI":"10.1371\/journal.ppat.1000257","article-title":"Role of intraspecies recombination in the spread of pathogenicity islands within the Escherichia coli species","volume":"5","author":"S Schubert","year":"2009","journal-title":"PLoS Pathog"},{"key":"pone.0326251.ref075","doi-asserted-by":"crossref","first-page":"167","DOI":"10.1099\/mic.0.2007\/011981-0","article-title":"The ferric yersiniabactin uptake receptor FyuA is required for efficient biofilm formation by urinary tract infectious Escherichia coli in human urine","volume":"154","author":"V Hancock","year":"2008","journal-title":"Microbiology (Reading)"},{"key":"pone.0326251.ref076","doi-asserted-by":"crossref","first-page":"699913","DOI":"10.3389\/fmicb.2021.699913","article-title":"Aerobactin-Mediated Iron Acquisition Enhances Biofilm Formation, Oxidative Stress Resistance, and Virulence of Yersinia pseudotuberculosis","volume":"12","author":"C Li","year":"2021","journal-title":"Front Microbiol"},{"issue":"2","key":"pone.0326251.ref077","doi-asserted-by":"crossref","first-page":"48","DOI":"10.1016\/j.imlet.2014.04.014","article-title":"The impact of intestinal inflammation on the nutritional environment of the gut microbiota","volume":"162","author":"F Faber","year":"2014","journal-title":"Immunol Lett"},{"issue":"2","key":"pone.0326251.ref078","doi-asserted-by":"crossref","first-page":"965","DOI":"10.1128\/IAI.73.2.965-971.2005","article-title":"The IrgA homologue adhesin Iha is an Escherichia coli virulence factor in murine urinary tract infection","volume":"73","author":"JR Johnson","year":"2005","journal-title":"Infect Immun"},{"issue":"4","key":"pone.0326251.ref079","doi-asserted-by":"crossref","first-page":"420","DOI":"10.1016\/S0272-6386(12)80635-4","article-title":"Citrate and renal calculi: new insights and future directions","volume":"17","author":"CY Pak","year":"1991","journal-title":"Am J Kidney Dis"},{"issue":"3","key":"pone.0326251.ref080","doi-asserted-by":"crossref","first-page":"227","DOI":"10.1078\/1438-4221-00123","article-title":"Distribution of the outer membrane haem receptor protein ChuA in environmental and human isolates of Escherichia coli","volume":"291","author":"H Hoffmann","year":"2001","journal-title":"Int J Med Microbiol"},{"issue":"1","key":"pone.0326251.ref081","doi-asserted-by":"crossref","first-page":"58","DOI":"10.1111\/1758-2229.12019","article-title":"The Clermont Escherichia coli phylo-typing method revisited: improvement of specificity and detection of new phylo-groups","volume":"5","author":"O Clermont","year":"2012","journal-title":"Environ Microbiol Rep"},{"key":"pone.0326251.ref082","doi-asserted-by":"crossref","first-page":"521","DOI":"10.1016\/j.ijmm.2014.05.005","article-title":"Hemolysin of enterohemorrhagic Escherichia coli: structure, transport, biological activity and putative role in virulence","volume":"304","author":"M Bielaszewska","year":"2014","journal-title":"Int J Med Microbiol"},{"issue":"1","key":"pone.0326251.ref083","doi-asserted-by":"crossref","first-page":"26","DOI":"10.1038\/nrmicro2265","article-title":"Molecular mechanisms of Escherichia coli pathogenicity","volume":"8","author":"MA Croxen","year":"2010","journal-title":"Nat Rev Microbiol"},{"issue":"5","key":"pone.0326251.ref084","doi-asserted-by":"crossref","first-page":"318","DOI":"10.3390\/pathogens9050318","article-title":"Escherichia coli Strains with Virulent Factors Typical for Uropathogens were Isolated from Sinuses from Patients with Chronic Rhinosinusitis-Case Report","volume":"9","author":"B Krawczyk","year":"2020","journal-title":"Pathogens"},{"issue":"6","key":"pone.0326251.ref085","doi-asserted-by":"crossref","DOI":"10.1084\/jem.20210518","article-title":"Ferroptosis in infection, inflammation, and immunity","volume":"218","author":"X Chen","year":"2021","journal-title":"J Exp Med"},{"issue":"2","key":"pone.0326251.ref086","doi-asserted-by":"crossref","DOI":"10.1152\/ajplung.00482.2004","article-title":"E. coli virulence factor hemolysin induces neutrophil apoptosis and necrosis\/lysis in vitro and necrosis\/lysis and lung injury in a rat pneumonia model","volume":"289","author":"TA Russo","year":"2005","journal-title":"Am J Physiol Lung Cell Mol Physiol"},{"issue":"8","key":"pone.0326251.ref087","doi-asserted-by":"crossref","DOI":"10.1073\/pnas.1500374112","article-title":"Dysregulation of Escherichia coli \u03b1-hemolysin expression alters the course of acute and persistent urinary tract infection","volume":"112","author":"K Nagamatsu","year":"2015","journal-title":"Proc Natl Acad Sci U S A"},{"key":"pone.0326251.ref088","article-title":"Yersiniabactin is a quorum-sensing autoinducer and siderophore in uropathogenic Escherichia coli","author":"JR Heffernan","year":"2024","journal-title":"MBio"},{"issue":"1","key":"pone.0326251.ref089","article-title":"Bacterial siderophores hijack neutrophil functions","volume":"198","author":"P Saha","year":"2017","journal-title":"J Immunol"},{"key":"pone.0326251.ref090","doi-asserted-by":"crossref","first-page":"143","DOI":"10.1186\/1471-2180-12-143","article-title":"Roles of iron acquisition systems in virulence of extraintestinal pathogenic Escherichia coli: salmochelin and aerobactin contribute more to virulence than heme in a chicken infection model","volume":"12","author":"Q Gao","year":"2012","journal-title":"BMC Microbiol"},{"key":"pone.0326251.ref091","doi-asserted-by":"crossref","first-page":"128","DOI":"10.1016\/j.micpath.2018.04.048","article-title":"Contribution of yersiniabactin to the virulence of an Escherichia coli sequence type 69 (\u201cclonal group A\u201d) cystitis isolate in murine models of urinary tract infection and sepsis","volume":"120","author":"JR Johnson","year":"2018","journal-title":"Microb Pathog"},{"issue":"6","key":"pone.0326251.ref092","doi-asserted-by":"crossref","first-page":"2773","DOI":"10.1007\/s00253-019-09653-x","article-title":"Antibacterial effects of iron oxide (Fe3O4) nanoparticles: distinguishing concentration-dependent effects with different bacterial cells growth and membrane-associated mechanisms","volume":"103","author":"L Gabrielyan","year":"2019","journal-title":"Appl Microbiol Biotechnol"},{"issue":"3","key":"pone.0326251.ref093","doi-asserted-by":"crossref","first-page":"917","DOI":"10.1016\/j.intimp.2013.09.020","article-title":"Sertraline decreases serum level of interleukin-6 (IL-6) in hemodialysis patients with depression: results of a randomized double-blind, placebo-controlled clinical trial","volume":"17","author":"M Taraz","year":"2013","journal-title":"Int Immunopharmacol"},{"issue":"9","key":"pone.0326251.ref094","doi-asserted-by":"crossref","first-page":"401","DOI":"10.1093\/intimm\/dxx031","article-title":"Hyperferritinemia and inflammation","volume":"29","author":"KF Kernan","year":"2017","journal-title":"Int Immunol"},{"key":"pone.0326251.ref095","doi-asserted-by":"crossref","first-page":"329","DOI":"10.5604\/17322693.1199716","article-title":"KIM-1 and NGAL as potential biomarkers for the diagnosis and cancer progression","volume":"70","author":"Z Marchewka","year":"2016","journal-title":"Postepy Hig Med Dosw (Online)"},{"issue":"1","key":"pone.0326251.ref096","doi-asserted-by":"crossref","first-page":"10","DOI":"10.1016\/j.canlet.2009.05.027","article-title":"Neutrophil gelatinase-associated lipocalin (NGAL) in human neoplasias: a new protein enters the scene","volume":"288","author":"D Bolignano","year":"2010","journal-title":"Cancer Lett"},{"issue":"5","key":"pone.0326251.ref097","doi-asserted-by":"crossref","first-page":"57","DOI":"10.4331\/wjbc.v12.i5.57","article-title":"Proteomics: Concepts and applications in human medicine","volume":"12","author":"S Al-Amrani","year":"2021","journal-title":"World J Biol Chem"},{"key":"pone.0326251.ref098","doi-asserted-by":"crossref","first-page":"126790","DOI":"10.1016\/j.micres.2021.126790","article-title":"Siderophores: Importance in bacterial pathogenesis and applications in medicine and industry","volume":"250","author":"B Khasheii","year":"2021","journal-title":"Microbiol Res"},{"issue":"2","key":"pone.0326251.ref099","doi-asserted-by":"crossref","first-page":"273","DOI":"10.1093\/femsre\/fuv049","article-title":"Bacterial ferrous iron transport: the Feo system","volume":"40","author":"CKY Lau","year":"2016","journal-title":"FEMS Microbiol Rev"},{"key":"pone.0326251.ref100","doi-asserted-by":"crossref","first-page":"90","DOI":"10.3389\/fcimb.2013.00090","article-title":"Iron, copper, zinc, and manganese transport and regulation in pathogenic Enterobacteria: correlations between strains, site of infection and the relative importance of the different metal transport systems for virulence","volume":"3","author":"G Porcheron","year":"2013","journal-title":"Front Cell Infect Microbiol"},{"key":"pone.0326251.ref101","doi-asserted-by":"crossref","first-page":"26","DOI":"10.3389\/fmicb.2020.00026","article-title":"Nitrate Metabolism Modulates Biosynthesis of Biofilm Components in Uropathogenic Escherichia coli and Acts as a Fitness Factor During Experimental Urinary Tract Infection","volume":"11","author":"AJ Mart\u00edn-Rodr\u00edguez","year":"2020","journal-title":"Front Microbiol"},{"key":"pone.0326251.ref102","doi-asserted-by":"crossref","first-page":"177","DOI":"10.1016\/j.jprot.2015.11.001","article-title":"Comparative proteomics of uropathogenic Escherichia coli during growth in human urine identify UCA-like (UCL) fimbriae as an adherence factor involved in biofilm formation and binding to uroepithelial cells","volume":"131","author":"DJ Wurpel","year":"2016","journal-title":"J Proteomics"},{"issue":"3","key":"pone.0326251.ref103","doi-asserted-by":"crossref","first-page":"1400","DOI":"10.1128\/IAI.68.3.1400-1407.2000","article-title":"Iha: a novel Escherichia coli O157:H7 adherence-conferring molecule encoded on a recently acquired chromosomal island of conserved structure","volume":"68","author":"PI Tarr","year":"2000","journal-title":"Infect Immun"},{"issue":"10","key":"pone.0326251.ref104","doi-asserted-by":"crossref","first-page":"6209","DOI":"10.1128\/IAI.69.10.6209-6216.2001","article-title":"Identification of a new iron-regulated virulence 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