{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,10,27]],"date-time":"2025-10-27T16:04:31Z","timestamp":1761581071010},"reference-count":42,"publisher":"American Society for Microbiology","issue":"5","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Clin. Vaccine Immunol."],"published-print":{"date-parts":[[2013,5]]},"abstract":"<jats:title>ABSTRACT<\/jats:title><jats:p><jats:named-content content-type=\"genus-species\">Salmonella enterica<\/jats:named-content>serotype Paratyphi A is a human-restricted pathogen and the cause of paratyphoid A fever. Using a high-throughput immunoscreening technique,<jats:italic>in vivo<\/jats:italic>-induced antigen technology (IVIAT), we identified 20 immunogenic bacterial proteins expressed in humans who were bacteremic with<jats:italic>S<\/jats:italic>. Paratyphi A but not those expressed in<jats:italic>S<\/jats:italic>. Paratyphi A grown under standard laboratory conditions. The majority of these proteins have known or potential roles in the pathogenesis of<jats:named-content content-type=\"genus-species\">S. enterica<\/jats:named-content>. These include proteins implicated in cell adhesion, fimbrial structure, adaptation to atypical conditions, oxidoreductase activity, proteolysis, antimicrobial resistance, and ion transport. Of particular interest among these<jats:italic>in vivo<\/jats:italic>-expressed proteins were<jats:italic>S<\/jats:italic>. Paratyphi A (SPA)2397, SPA2612, and SPA1604. SPA2397 and SPA2612 are prophage related, and SPA1604 is in<jats:named-content content-type=\"genus-species\">Salmonella<\/jats:named-content>pathogenicity island 11 (SPI-11). Using real-time quantitative PCR (RT-qPCR), we confirmed increased levels of mRNA expressed by genes identified by IVIAT in a comparison of mRNA levels in organisms in the blood of bacteremic patients to those in<jats:italic>in vitro<\/jats:italic>cultures. Comparing convalescent- to acute-phase samples, we also detected a significant increase in the reaction of convalescent-phase antibodies with two proteins identified by IVIAT: SPA2397 and SPA0489. SPA2397 is a phage-related lysozyme, Gp19, and SPA0489 encodes a protein containing NlpC\/P60 and cysteine, histidine-dependent amidohydrolase\/peptidase (CHAP) domains. In a previous study utilizing a different approach, we found that transcripts for 11 and 7 of the genes identified by IVIAT were detectable in organisms in the blood of humans in Bangladesh who were bacteremic with<jats:italic>S<\/jats:italic>. Paratyphi A and<jats:named-content content-type=\"genus-species\">Salmonella enterica<\/jats:named-content>serovar Typhi, respectively.<jats:italic>S.<\/jats:italic>Paratyphi A antigens identified by IVIAT warrant further evaluation for their contributions to pathogenesis and might have diagnostic, therapeutic, or preventive relevance.<\/jats:p>","DOI":"10.1128\/cvi.00054-13","type":"journal-article","created":{"date-parts":[[2013,3,14]],"date-time":"2013-03-14T05:24:16Z","timestamp":1363238656000},"page":"712-719","source":"Crossref","is-referenced-by-count":13,"title":["Identification of<i>In Vivo<\/i>-Induced Bacterial Proteins during Human Infection with Salmonella enterica Serotype Paratyphi A"],"prefix":"10.1128","volume":"20","author":[{"given":"Mohammad Murshid","family":"Alam","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Lillian L.","family":"Tsai","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Sean M.","family":"Rollins","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Alaullah","family":"Sheikh","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Farhana","family":"Khanam","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Meagan Kelly","family":"Bufano","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yanan","family":"Yu","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Ying","family":"Wu-Freeman","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Anuj","family":"Kalsy","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Tania","family":"Sultana","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"M. 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Travel Med."},{"key":"key20180919073651_B2","first-page":"346","article-title":"The global burden of typhoid fever","volume":"82","author":"Crump","year":"2004","journal-title":"Bull. World Health Organ."},{"key":"key20180919073651_B3","doi-asserted-by":"crossref","first-page":"1247","DOI":"10.1086\/503033","article-title":"Salmonella enterica serovar Paratyphi A and S. enterica serovar Typhi cause indistinguishable clinical syndromes in Kathmandu, Nepal","volume":"42","author":"Maskey","year":"2006","journal-title":"Clin. Infect. Dis."},{"key":"key20180919073651_B4","first-page":"10","article-title":"An unusually high occurrence of Salmonella enterica serotype Paratyphi A in patients with enteric fever","volume":"117","author":"Tankhiwale","year":"2003","journal-title":"Indian J. Med. 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Microbiol."},{"key":"key20180919073651_B16","doi-asserted-by":"crossref","first-page":"3358","DOI":"10.1128\/IAI.73.6.3358-3366.2005","article-title":"The Salmonella enterica serotype Typhimurium lpf, bcf, stb, stc, std, and sth fimbrial operons are required for intestinal persistence in mice","volume":"73","author":"Weening","year":"2005","journal-title":"Infect. 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Lett."},{"key":"key20180919073651_B20","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1186\/1471-2180-8-37","article-title":"Rapid acid treatment of Escherichia coli: transcriptomic response and recovery","volume":"8","author":"Kannan","year":"2008","journal-title":"BMC Microbiol."},{"key":"key20180919073651_B21","doi-asserted-by":"crossref","first-page":"e6994","DOI":"10.1371\/journal.pone.0006994","article-title":"Comparative proteomic analysis of the PhoP regulon in Salmonella enterica serovar Typhi versus Typhimurium","volume":"4","author":"Charles","year":"2009","journal-title":"PLoS One"},{"key":"key20180919073651_B22","doi-asserted-by":"crossref","first-page":"5040","DOI":"10.1128\/jb.177.17.5040-5047.1995","article-title":"Characterization of the Salmonella Typhimurium pagC\/pagD chromosomal region","volume":"177","author":"Gunn","year":"1995","journal-title":"J. Bacteriol."},{"key":"key20180919073651_B23","doi-asserted-by":"crossref","first-page":"289","DOI":"10.1016\/0022-2836(87)90650-4","article-title":"The use of transposon TnphoA to detect genes for cell envelope proteins subject to a common regulatory stimulus. Analysis of osmotically regulated genes in Escherichia coli","volume":"195","author":"Gutierrez","year":"1987","journal-title":"J. Mol. Biol."},{"key":"key20180919073651_B24","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1006\/jmbi.1997.1308","article-title":"Role of DNA supercoiling and rpoS sigma factor in the osmotic and growth phase-dependent induction of the gene osmE of Escherichia coli K12","volume":"273","author":"Conter","year":"1997","journal-title":"J. Mol. Biol."},{"key":"key20180919073651_B25","doi-asserted-by":"crossref","first-page":"1906","DOI":"10.1073\/pnas.0509183103","article-title":"Transcriptome of Salmonella enterica serovar Typhi within macrophages revealed through the selective capture of transcribed sequences","volume":"103","author":"Faucher","year":"2006","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"key20180919073651_B26","doi-asserted-by":"crossref","first-page":"1110","DOI":"10.1016\/j.cell.2010.11.037","article-title":"Lipoprotein cofactors located in the outer membrane activate bacterial cell wall polymerases","volume":"143","author":"Paradis-Bleau","year":"2010","journal-title":"Cell"},{"key":"key20180919073651_B27","doi-asserted-by":"crossref","first-page":"74","DOI":"10.1007\/BF00272347","article-title":"Cloning and sequencing of the melB gene encoding the melibiose permease of Salmonella Typhimurium LT2","volume":"234","author":"Mizushima","year":"1992","journal-title":"Mol. Gen. Genet."},{"key":"key20180919073651_B28","doi-asserted-by":"crossref","first-page":"6367","DOI":"10.1074\/jbc.M110.206227","article-title":"Mechanism of melibiose\/cation symport of the melibiose permease of Salmonella Typhimurium","volume":"286","author":"Guan","year":"2011","journal-title":"J. Biol. Chem."},{"key":"key20180919073651_B29","doi-asserted-by":"crossref","first-page":"4977","DOI":"10.1128\/jb.179.16.4977-4984.1997","article-title":"A Salmonella Typhimurium genetic locus which confers copper tolerance on copper-sensitive mutants of Escherichia coli","volume":"179","author":"Gupta","year":"1997","journal-title":"J. Bacteriol."},{"key":"key20180919073651_B30","doi-asserted-by":"crossref","first-page":"807","DOI":"10.1016\/j.micinf.2008.04.011","article-title":"Iron-regulated genes of Salmonella enterica serovar Typhimurium in response to norepinephrine and the requirement of fepDGC for norepinephrine-enhanced growth","volume":"10","author":"Bearson","year":"2008","journal-title":"Microbes Infect."},{"key":"key20180919073651_B31","doi-asserted-by":"crossref","first-page":"3840","DOI":"10.1016\/j.vaccine.2005.07.020","article-title":"Catecholate receptor proteins in Salmonella enterica: role in virulence and implications for vaccine development","volume":"24","author":"Williams","year":"2006","journal-title":"Vaccine"},{"key":"key20180919073651_B32","doi-asserted-by":"crossref","first-page":"214","DOI":"10.1016\/j.micpath.2010.03.005","article-title":"The Salmonella enterica serovar Typhimurium QseB response regulator negatively regulates bacterial motility and swine colonization in the absence of the QseC sensor kinase","volume":"48","author":"Bearson","year":"2010","journal-title":"Microb. Pathog."},{"key":"key20180919073651_B33","doi-asserted-by":"crossref","first-page":"6092","DOI":"10.1128\/JB.181.19.6092-6097.1999","article-title":"Characterization of a group of anaerobically induced, fnr-dependent genes of Salmonella Typhimurium","volume":"181","author":"Wei","year":"1999","journal-title":"J. Bacteriol."},{"issue":"Pt 1","key":"key20180919073651_B34","doi-asserted-by":"crossref","first-page":"187","DOI":"10.1099\/00221287-143-1-187","article-title":"The ldhA gene encoding the fermentative lactate dehydrogenase of Escherichia coli","volume":"143","author":"Bunch","year":"1997","journal-title":"Microbiology"},{"key":"key20180919073651_B35","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.bej.2005.05.010","article-title":"Effect of ldhA gene deletion on the metabolism of Escherichia coli based on gene expression, enzyme activities, intracellular metabolite concentrations, and metabolic flux distribution","volume":"26","author":"Kabir","year":"2005","journal-title":"Biochem. Eng. J."},{"key":"key20180919073651_B36","doi-asserted-by":"crossref","first-page":"3336","DOI":"10.1073\/pnas.69.11.3336","article-title":"Mutants of Salmonella Typhimurium and Escherichia coli pleiotropically defective in active transport","volume":"69","author":"Hong","year":"1972","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"key20180919073651_B37","doi-asserted-by":"crossref","first-page":"14","DOI":"10.1007\/s00284-007-9030-7","article-title":"Expression and regulation of the yggG gene of Escherichia coli","volume":"56","author":"Huang","year":"2008","journal-title":"Curr. Microbiol."},{"key":"key20180919073651_B38","doi-asserted-by":"crossref","first-page":"4441","DOI":"10.3390\/ijms12074441","article-title":"Klebsiella pneumoniae yggG gene product: a zinc-dependent metalloprotease","volume":"12","author":"Kuan","year":"2011","journal-title":"Int. J. Mol. Sci."},{"key":"key20180919073651_B39","doi-asserted-by":"crossref","first-page":"8","DOI":"10.1111\/j.1574-6968.2007.00860.x","article-title":"Up-regulation of yggG promotes the survival of Escherichia coli cells containing Era-1 mutant protein","volume":"275","author":"Huang","year":"2007","journal-title":"FEMS Microbiol. Lett."},{"key":"key20180919073651_B40","doi-asserted-by":"crossref","first-page":"R11","DOI":"10.1186\/gb-2003-4-2-r11","article-title":"Evolutionary history, structural features and biochemical diversity of the NlpC\/P60 superfamily of enzymes","volume":"4","author":"Anantharaman","year":"2003","journal-title":"Genome Biol."},{"key":"key20180919073651_B41","doi-asserted-by":"crossref","first-page":"234","DOI":"10.1016\/S0968-0004(03)00061-6","article-title":"The CHAP domain: a large family of amidases including GSP amidase and peptidoglycan hydrolases","volume":"28","author":"Bateman","year":"2003","journal-title":"Trends Biochem. Sci."},{"key":"key20180919073651_B42","doi-asserted-by":"crossref","first-page":"1683","DOI":"10.1128\/JCM.36.6.1683-1687.1998","article-title":"Quantitation of bacteria in blood of typhoid fever patients and relationship between counts and clinical features, transmissibility, and antibiotic resistance","volume":"36","author":"Wain","year":"1998","journal-title":"J. Clin. 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