{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,2]],"date-time":"2026-06-02T13:11:41Z","timestamp":1780405901673,"version":"3.54.1"},"reference-count":80,"publisher":"MDPI AG","issue":"18","license":[{"start":{"date-parts":[[2024,9,20]],"date-time":"2024-09-20T00:00:00Z","timestamp":1726790400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Russian Science Foundation","award":["23-45-10026"],"award-info":[{"award-number":["23-45-10026"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>Adhesive-invasive E. coli has been suggested to be associated with the development of Crohn\u2019s disease (CD). It is assumed that they can provoke the onset of the inflammatory process as a result of the invasion of intestinal epithelial cells and then, due to survival inside macrophages and dendritic cells, stimulate chronic inflammation. In previous reports, we have shown that passage of the CD isolate ZvL2 on minimal medium M9 supplemented with sodium propionate (PA) as a carbon source stimulates and inhibits the adherent-invasive properties and the ability to survive in macrophages. This effect was reversible and not observed for the laboratory strain K12 MG1655. We were able to compare the isogenic strain AIEC in two phenotypes\u2014virulent (ZvL2-PA) and non-virulent (ZvL2-GLU). Unlike ZvL2-GLU, ZvL2-PA activates the production of ROS and cytokines when interacting with neutrophils. The laboratory strain does not cause a similar effect. To activate neutrophils, bacterial opsonization is necessary. Differences in neutrophil NADH oxidase activation and \u03b6-potential for ZvL2-GLU and ZvL2-PA are associated with changes in membrane protein abundance, as demonstrated by differential 2D electrophoresis and LC-MS. The increase in ROS and cytokine production during the interaction of ZvL2-PA with neutrophils is associated with a rearrangement of the abundance of membrane proteins, which leads to the activation of Rcs and PhoP\/Q signaling pathways and changes in the composition and\/or modification of LPS. Certain isoforms of OmpA may play a role in the formation of the virulent phenotype of ZvL2-PA and participate in the activation of NADPH oxidase in neutrophils.<\/jats:p>","DOI":"10.3390\/ijms251810118","type":"journal-article","created":{"date-parts":[[2024,9,20]],"date-time":"2024-09-20T07:38:57Z","timestamp":1726817937000},"page":"10118","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":4,"title":["The Role of Propionate-Induced Rearrangement of Membrane Proteins in the Formation of the Virulent Phenotype of Crohn\u2019s Disease-Associated Adherent-Invasive Escherichia coli"],"prefix":"10.3390","volume":"25","author":[{"given":"Olga V.","family":"Pobeguts","sequence":"first","affiliation":[{"name":"Lopukhin Federal Research and Clinical Center of Physical-Chemical Medicine of Federal Medical Biological Agency, Malaya Pirogovskaya 1a, 119435 Moscow, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Maria A.","family":"Galyamina","sequence":"additional","affiliation":[{"name":"Lopukhin Federal Research and Clinical Center of Physical-Chemical Medicine of Federal Medical Biological Agency, Malaya Pirogovskaya 1a, 119435 Moscow, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Elena V.","family":"Mikhalchik","sequence":"additional","affiliation":[{"name":"Lopukhin Federal Research and Clinical Center of Physical-Chemical Medicine of Federal Medical Biological Agency, Malaya Pirogovskaya 1a, 119435 Moscow, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sergey I.","family":"Kovalchuk","sequence":"additional","affiliation":[{"name":"Shemyakin-Ovchinnikov Institute of Bioorganic Chemistry, Ulitsa Mikluho-Maklaya, 16\/10, 117997 Moscow, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Igor P.","family":"Smirnov","sequence":"additional","affiliation":[{"name":"Lopukhin Federal Research and Clinical Center of Physical-Chemical Medicine of Federal Medical Biological Agency, Malaya Pirogovskaya 1a, 119435 Moscow, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alena V.","family":"Lee","sequence":"additional","affiliation":[{"name":"Lopukhin Federal Research and Clinical Center of Physical-Chemical Medicine of Federal Medical Biological Agency, Malaya Pirogovskaya 1a, 119435 Moscow, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lyubov Yu.","family":"Filatova","sequence":"additional","affiliation":[{"name":"Department of Chemistry, Lomonosov Moscow State University, Leninskiye Gory 1\u20133, 119991 Moscow, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0009-0771-3488","authenticated-orcid":false,"given":"Kirill V.","family":"Sikamov","sequence":"additional","affiliation":[{"name":"Lopukhin Federal Research and Clinical Center of Physical-Chemical Medicine of Federal Medical Biological Agency, Malaya Pirogovskaya 1a, 119435 Moscow, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5245-2285","authenticated-orcid":false,"given":"Oleg M.","family":"Panasenko","sequence":"additional","affiliation":[{"name":"Lopukhin Federal Research and Clinical Center of Physical-Chemical Medicine of Federal Medical Biological Agency, Malaya Pirogovskaya 1a, 119435 Moscow, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2743-5835","authenticated-orcid":false,"given":"Alexey Yu.","family":"Gorbachev","sequence":"additional","affiliation":[{"name":"Lopukhin Federal Research and Clinical Center of Physical-Chemical Medicine of Federal Medical Biological Agency, Malaya Pirogovskaya 1a, 119435 Moscow, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2024,9,20]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"4499","DOI":"10.1128\/IAI.67.9.4499-4509.1999","article-title":"Invasive ability of Escherichia coli strains isolated from ileal mucosa in Crohn\u2019s disease","volume":"67","author":"Boudeau","year":"1999","journal-title":"Infect. Immun."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"412","DOI":"10.1053\/j.gastro.2004.04.061","article-title":"High prevalence of adherent-invasive Escherichia coli associated with ileal mucosa in Crohn\u2019s disease","volume":"127","author":"Boudeau","year":"2004","journal-title":"Gastroenterology"},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"Dunne, K.A., Allam, A., McIntosh, A., Houston, S.A., Cerovic, V., Goodyear, C.S., Roe, A.J., Scott ABeatson, S.A., Milling, S.W., and Walker, D. (2013). Increased S-nitrosylation and proteasomal degradation of caspase-3 during infection contribute to the persistence of adherent invasive Escherichia coli (AIEC) in immune cells. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0068386"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"2380064","DOI":"10.1080\/19490976.2024.2380064","article-title":"AIEC-dependent pathogenic Th17 cell transdifferentiation in Crohn\u2019s disease is suppressed by rfaP and ybaT deletion","volume":"16","author":"Leccese","year":"2024","journal-title":"Gut Microbes"},{"key":"ref_5","doi-asserted-by":"crossref","unstructured":"Nash, J.H., Villegas, A., Kropinski, A.M., Aguilar-Valenzuela, R., Konczy, P., Mascarenhas, M., Ziebell, K., Torres, A.G., Karmali, M.A., and Coombes, B.K. (2010). Genome sequence of adherent-invasive Escherichia coli and comparative genomic analysis with other E. coli pathotypes. BMC Genomics., 11.","DOI":"10.1186\/1471-2164-11-667"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"426","DOI":"10.1139\/w2012-007","article-title":"A potential role of Escherichia coli pathobionts in the pathogenesis of pediatric inflammatory bowel disease","volume":"58","author":"Schippa","year":"2012","journal-title":"Can. J. Microbiol."},{"key":"ref_7","doi-asserted-by":"crossref","unstructured":"Conte, M.P., Longhi, C., Marazzato, M., Conte, A.L., Aleandri, M., Lepanto, M.S., Zagaglia, C., Nicoletti, M., Aloi, M., and Totino, V. (2014). Adherent-invasive Escherichia coli (AIEC) in pediatric Crohn\u2019s disease patients: Phenotypic and genetic pathogenic features. BMC Res. Notes, 7.","DOI":"10.1186\/1756-0500-7-748"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"159","DOI":"10.1093\/ilar\/ilv007","article-title":"Pathogens, commensal symbionts, and pathobionts: Discovery and functional effects on the host","volume":"56","author":"Hornef","year":"2015","journal-title":"Ilar. J."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"1","DOI":"10.4331\/wjbc.v11.i1.1","article-title":"Why the discovery of adherent-invasive Escherichia coli molecular markers is so challenging?","volume":"11","year":"2020","journal-title":"World J. Biol. Chem."},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"Rakitina, D.V., Manolov, A.I., Kanygina, A.V., Garushyants, S.K., Baikova, J.P., Alexeev, D.G., Ladygina, V.G., Kostryukova, E.S., Larin, A.K., and Semashko, T.A. (2017). Genome analysis of E. coli isolated from Crohn\u2019s disease patients. BMC Genomics., 18.","DOI":"10.1186\/s12864-017-3917-x"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"5813","DOI":"10.1128\/AEM.02614-10","article-title":"Adherent-Invasive Escherichia coli Phenotype Displayed by Intestinal Pathogenic E. coli Strains from Cats, Dogs, and Swine","volume":"77","author":"Barnich","year":"2011","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Camprub\u00ed-Font, C., Ewers, C., Lopez-Siles, M., and Martinez-Medina, M. (2019). Genetic and Phenotypic Features to Screen for Putative Adherent-Invasive Escherichia coli. Front. Microbiol., 10.","DOI":"10.3389\/fmicb.2019.00108"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"68","DOI":"10.1097\/MIB.0000000000000609","article-title":"GipA Factor Supports Colonization of Peyer\u2019s Patches by Crohn\u2019s Disease-associated Escherichia Coli","volume":"22","author":"Vazeille","year":"2016","journal-title":"Inflamm. Bowel Dis."},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Dogan, B., Belcher-Timme, H.F., Dogan, E.I., Jiang, Z.D., DuPont, H.L., Snyder, N., Yang, S., Chandler, B., Scherl, E.J., and Simpson, K.W. (2018). Evaluation of Escherichia coli pathotypes associated with irritable bowel syndrome. FEMS Microbiol. Lett., 365.","DOI":"10.1093\/femsle\/fny249"},{"key":"ref_15","doi-asserted-by":"crossref","unstructured":"C\u00e9spedes, S., Saitz, W., Del Canto, F., De la Fuente, M., Quera, R., Hermoso, M., Mu\u00f1oz, R., Ginard, D., Khorrami, S., and Gir\u00f3n, J. (2017). Genetic Diversity and Virulence Determinants of Escherichia coli Strains Isolated from Patients with Crohn\u2019s Disease in Spain and Chile. Front. Microbiol., 8.","DOI":"10.3389\/fmicb.2017.00639"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"1919","DOI":"10.1097\/MIB.0000000000000183","article-title":"Inflammation-associated adherent-invasive Escherichia coli are enriched in pathways for use of propanediol and iron and M-cell translocation","volume":"20","author":"Dogan","year":"2014","journal-title":"Inflamm. Bowel Dis."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"1566","DOI":"10.1172\/JCI30504","article-title":"CEACAM6 acts as a receptor for adherent-invasive E. coli, supporting ileal mucosa colonization in Crohn disease","volume":"117","author":"Barnich","year":"2007","journal-title":"J. Clin. Invest."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"1355","DOI":"10.1136\/gut.2010.207456","article-title":"Abnormally expressed ER stress response chaperone Gp96 in CD favours adherent-invasive Escherichia coli invasion","volume":"9","author":"Rolhion","year":"2010","journal-title":"Gut"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"602","DOI":"10.1053\/j.gastro.2013.05.017","article-title":"Chitin-binding domains of Escherichia coli ChiA mediate interactions with intestinal epithelial cells in mice with colitis","volume":"145","author":"Low","year":"2013","journal-title":"Gastroenterology"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"213","DOI":"10.4291\/wjgp.v5.i3.213","article-title":"Escherichia coli in chronic inflammatory bowel diseases: An update on adherent invasive Escherichia coli pathogenicity","volume":"5","year":"2014","journal-title":"World J. Gastrointest. Pathophysiol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"781","DOI":"10.1046\/j.1365-2958.2003.03468.x","article-title":"Regulatory and functional co-operation of flagella and type 1 pili in adhesive and invasive abilities of AIEC strain LF82 isolated from a patient with Crohn\u2019s disease","volume":"48","author":"Barnich","year":"2003","journal-title":"Mol. Microbiol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"1051","DOI":"10.1002\/ibd.20423","article-title":"Crohn\u2019s disease-associated Escherichia coli LF82 aggravates colitis in injured mouse colon via signaling by flagellin","volume":"14","author":"Carvalho","year":"2008","journal-title":"Inflamm. Bowel Dis."},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Pobeguts, O.V., Ladygina, V.G., Evsyutina, D.V., Eremeev, A.V., Zubov, A.I., Matyushkina, D.S., Scherbakov, P.L., Rakitina, D.V., and Fisunov, G.Y. (2020). Propionate Induces Virulent Properties of Crohn\u2019s Disease-Associated Escherichia coli. Front. Microbiol., 11.","DOI":"10.3389\/fmicb.2020.01460"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1904","DOI":"10.1128\/IAI.03003-14","article-title":"The IbeA invasin of adherent-invasive Escherichia coli mediates nteraction with intestinal epithelia and macrophages","volume":"83","author":"Cieza","year":"2015","journal-title":"Infect. Immun."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1128\/microbiolspec.MBP-0008-2014","article-title":"The Roles of Inflammation, Nutrient Availability and the Commensal Microbiota in Enteric Pathogen Infection","volume":"3","author":"Stecher","year":"2015","journal-title":"Microbiol. Spectr."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"1020","DOI":"10.1099\/mic.0.078105-0","article-title":"From food to cell: Nutrient exploitation strategies of enteropathogens","volume":"160","author":"Staib","year":"2014","journal-title":"Microbiology"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"993","DOI":"10.1111\/cmi.12300","article-title":"The enteric two-step: Nutritional strategies of bacterial pathogens within the gut","volume":"16","author":"Ferreyra","year":"2014","journal-title":"Cell Microbiol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"325","DOI":"10.1016\/j.ebiom.2019.03.071","article-title":"Inflammation associated ethanolamine facilitates infection by Crohn\u2019s disease-linked adherent-invasive Escherichia Coli","volume":"43","author":"Ormsby","year":"2019","journal-title":"EBioMedicine"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"251","DOI":"10.1111\/cei.13226","article-title":"Recruitment of activated neutrophils correlates with disease severity in adult Crohn\u2019s disease","volume":"195","author":"Therrien","year":"2019","journal-title":"Clin. Exp. Immunol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"543","DOI":"10.1189\/jlb.70.4.543","article-title":"Identification and comparison of residues critical for cell-adhesion activities of two neutrophil CD66 antigens, CEACAM6 and CEACAM8","volume":"70","author":"Kuroki","year":"2001","journal-title":"J. Leukoc. Biol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"903","DOI":"10.1515\/CCLM.2009.224","article-title":"Neutrophil CD64: A diagnostic marker for infection and sepsis","volume":"47","author":"Hoffmann","year":"2009","journal-title":"Clin. Chem. Lab. Med."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"3087","DOI":"10.1039\/c1mb05193h","article-title":"Outer membrane proteome and its regulatory network in response to changes in glucose concentration in Escherichia coli","volume":"7","author":"Yang","year":"2011","journal-title":"Mol. Biosist."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"e00721-20","DOI":"10.1128\/IAI.00721-20","article-title":"The role of OmpX, an outer membrane protein, in virulence and flagellar expression in uropathogenic Escherichia coli","volume":"89","author":"Hirakawa","year":"2021","journal-title":"Infect. Immun."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"15822","DOI":"10.1073\/pnas.1108999108","article-title":"The bacterial actin MreB rotates, and rotation depends on cell-wall assembly","volume":"108","author":"Wang","year":"2011","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"Harvey, K.L., Jarocki, V.M., Charles, I.G., and Djordjevic, S.P. (2019). The Diverse Functional Roles of Elongation Factor Tu (EF-Tu) in Microbial Pathogenesis. Front. Microbiol., 10.","DOI":"10.3389\/fmicb.2019.02351"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"180","DOI":"10.1002\/2211-5463.12770","article-title":"Mucin adsorbed by E. coli can affect neutrophil activation in vitro","volume":"10","author":"Mikhalchik","year":"2020","journal-title":"FEBS Open Bio."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"531","DOI":"10.1038\/nature03239","article-title":"Interaction network containing conserved and essential protein complexes in Escherichia coli","volume":"433","author":"Butland","year":"2005","journal-title":"Nature"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"1715","DOI":"10.1016\/j.jmb.2015.01.025","article-title":"Translation elongation factor EF-Tu modulates filament formation of actin-like MreB protein in vitro","volume":"427","author":"Reimold","year":"2015","journal-title":"J. Mol. Biol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"1537","DOI":"10.1016\/j.jmb.2015.02.002","article-title":"A first line of stress defense: Small heat shock proteins and their function in protein homeostasis","volume":"427","author":"Haslbeck","year":"2015","journal-title":"J. Mol. Biol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"985","DOI":"10.1111\/mmi.12609","article-title":"Polar localization of Escherichia coli chemoreceptors requires an intact Tol-Pal complex","volume":"92","author":"Santos","year":"2014","journal-title":"Mol. Microbiol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"16080","DOI":"10.1016\/S0021-9258(17)36204-X","article-title":"Isolation and characterization of eight A precursors from a 3-deoxy-D-manno-octylosonic acis-deficient mutant of Salmonella typhimurium","volume":"260","author":"Raetz","year":"1985","journal-title":"J. Biol. Chem."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"1029","DOI":"10.1111\/j.1365-2958.2004.04040.x","article-title":"Proteomic screening and identification of differentially distributed membrane proteins in Escherichia coli","volume":"52","author":"Lai","year":"2004","journal-title":"Mol. Microbiol."},{"key":"ref_43","doi-asserted-by":"crossref","unstructured":"Liao, C., Liang, X., Yang, F., Soupir, M.L., Howe, A.C., Thompson, M.L., and Jarboe, L.R. (2017). Allelic Variation in Outer Membrane Protein A and Its Influence on Attachment of Escherichia coli to Corn Stover. Front. Microbiol., 8.","DOI":"10.3389\/fmicb.2017.00708"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"6701","DOI":"10.1021\/bi047278e","article-title":"Kinetics of folding of Escherichia coli OmpA from narrow to large pore conformation in a planar bilayer","volume":"44","author":"Zakharian","year":"2005","journal-title":"Biochemistry"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"373","DOI":"10.1016\/j.ijmm.2004.08.004","article-title":"OmpA of a septicemic Escherichia coli O78 secretion and convergent evolution","volume":"294","author":"Gophna","year":"2004","journal-title":"Int. J. Med. Microbiol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"623","DOI":"10.1128\/jb.131.2.623-630.1977","article-title":"Influence of osmolarity of the growth medium on the outer membrane protein pattern of Escherichia coli","volume":"131","author":"Lugtenberg","year":"1977","journal-title":"J. Bacteriol."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"4696","DOI":"10.1128\/jb.177.16.4696-4702.1995","article-title":"Modulation of flagellar expression in Escherichia coli by acetyl phosphate and the osmoregulator OmpR","volume":"177","author":"Shin","year":"1995","journal-title":"J. Bacteriol."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"639","DOI":"10.1046\/j.1365-2958.2003.03594.x","article-title":"Complex regulation of csgD promoter activity by global regulatory proteins","volume":"49","author":"Gerstel","year":"2003","journal-title":"Mol. Microbiol."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"7213","DOI":"10.1128\/JB.183.24.7213-7223.2001","article-title":"Complex Regulatory Network Controls Initial Adhesion and Biofilm Formation in Escherichia coli via Regulation of the csgD Gene","volume":"183","author":"Brombacher","year":"2001","journal-title":"J. Bacteriol."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"2442","DOI":"10.1128\/JB.180.9.2442-2449.1998","article-title":"Isolation of an Escherichia coli K-12 mutant strain able to form biofilms on inert surfaces: Involvement of a new ompR allele that increases curli expression","volume":"180","author":"Vidal","year":"1998","journal-title":"J. Bacteriol."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"e00407-22","DOI":"10.1128\/jb.00407-22","article-title":"NlpE is an OmpA-associated outer membrane sensor of the Cpx 11 envelope stress response","volume":"205","author":"Cho","year":"2023","journal-title":"J. Bacteriol."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"537","DOI":"10.1128\/IAI.00881-15","article-title":"The Surface Sensor NlpE of Enterohemorrhagic Escherichia coli Contributes to Regulation of the Type III Secretion System and Flagella by the Cpx Response to Adhesion","volume":"84","author":"Shimizu","year":"2015","journal-title":"Infect. Immun."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"441","DOI":"10.1016\/j.chom.2015.03.003","article-title":"Delivery of cardiolipins to the Salmonella outer membrane is necessary for survival within host tissues and virulence","volume":"17","author":"Dalebroux","year":"2015","journal-title":"Cell Host Microbe."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"53","DOI":"10.1038\/nrmicro1788","article-title":"Salmonellae interplay with host cells","volume":"6","author":"Haraga","year":"2008","journal-title":"Nat. Rev. Microbiol."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"389","DOI":"10.1016\/0923-2508(94)90086-8","article-title":"Regulation of capsule synthesis includes interactions of the RcsC\/RcsB regulatory pair","volume":"145","author":"Stout","year":"1994","journal-title":"Res. Microbiol."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"4264","DOI":"10.1128\/JB.00004-06","article-title":"RcsF is an outer membrane lipoprotein involved in the RcsCDB phosphorelay signaling pathway in Escherichia coli","volume":"188","author":"Cam","year":"2006","journal-title":"J. Bacteriol."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"3219","DOI":"10.1002\/j.1460-2075.1996.tb00686.x","article-title":"Bacterial defense against aging: Role of the Escherichia coli ArcA regulator in gene expression, readjusted energy flux and survival during stasis","volume":"15","author":"Nystrom","year":"1996","journal-title":"Embo J."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"12588","DOI":"10.1074\/jbc.M313454200","article-title":"Probing the ArcA-P modulon of Escherichia coli by whole genome transcriptional analysis and sequence recognition profiling","volume":"279","author":"Liu","year":"2004","journal-title":"J. Biol. Chem."},{"key":"ref_59","doi-asserted-by":"crossref","unstructured":"Loui, C., Chang, A.C., and Lu, S. (2009). Role of the ArcAB two-component system in the resistance of Escherichia coli to reactive oxygen stress. BMC Microbiol., 9.","DOI":"10.1186\/1471-2180-9-183"},{"key":"ref_60","doi-asserted-by":"crossref","unstructured":"Valvano, M.A. (2022). Remodelling of the Gram-negative bacterial Kdo2-lipid A and its functional implications. Microbiology, 168.","DOI":"10.1099\/mic.0.001159"},{"key":"ref_61","doi-asserted-by":"crossref","unstructured":"Panda, G., Dash, S., and Sahu, S.K. (2022). Harnessing the Role of Bacterial Plasma Membrane Modifications for the Development of Sustainable Membranotropic Phytotherapeutics. Membranes, 12.","DOI":"10.3390\/membranes12100914"},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"1604","DOI":"10.1111\/mmi.14240","article-title":"Colistin heteroresistance in Enterobacter cloacae is regulated by PhoPQ-dependent 4-amino-4-deoxy-l-arabinose addition to lipid A","volume":"111","author":"Kang","year":"2019","journal-title":"Mol. Microbiol."},{"key":"ref_63","doi-asserted-by":"crossref","unstructured":"MacRae, M.R., Puvanendran, D., Haase, M.A.B., Coudray, N., Kolich, L., Lam, J., Baek, M., Bhabha, G., and Ekiert, D.C. (2023). Protein-protein interactions in the Mla lipid transport system probed by computational structure prediction and deep mutational scanning. J. Biol. Chem., 24.","DOI":"10.1101\/2022.12.09.519820"},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"1327","DOI":"10.1534\/genetics.107.081836","article-title":"Genetic interaction between the Escherichia coli AcpT phosphopantetheinyl transferase and the YejM inner membrane protein","volume":"178","author":"Cronan","year":"2008","journal-title":"Genetics"},{"key":"ref_65","doi-asserted-by":"crossref","unstructured":"Chervy, M., Barnich, N., and Denizot, J. (2020). Adherent-Invasive E. coli: Update on the Lifestyle of a Troublemaker in Crohn\u2019s Disease. Int. J. Mol. Sci., 21.","DOI":"10.3390\/ijms21103734"},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"317","DOI":"10.1007\/s12275-023-00030-y","article-title":"Envelope-Stress Sensing Mechanism of Rcs and Cpx Signaling Pathways in Gram-Negative Bacteria","volume":"61","author":"Cho","year":"2023","journal-title":"J. Microbiol."},{"key":"ref_67","doi-asserted-by":"crossref","unstructured":"Lach, S.R., Kumar, S., Kim, S., Im, W., and Konovalova, A. (2023). Conformational rearrangements in the sensory RcsF\/OMP complex mediate signal transduction across the bacterial cell envelope. PLoS Genetics., 19.","DOI":"10.1371\/journal.pgen.1010601"},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"823","DOI":"10.1046\/j.1365-2958.2003.03601.x","article-title":"RcsCDB His-Asp phosphorelay system negatively regulates the flhDC operon in Escherichia coli","volume":"49","author":"Laugel","year":"2003","journal-title":"Mol. Microbiol."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"106","DOI":"10.1016\/j.mib.2013.12.005","article-title":"Salmonellae PhoPQ regulation of the outer membrane to resist innate immunity","volume":"17","author":"Dalebroux","year":"2014","journal-title":"Curr. Opin. Microbiol."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"1963","DOI":"10.1073\/pnas.1316901111","article-title":"PhoPQ regulates acidic glycerophospholipid content of the Salmonella Typhimurium outer membrane","volume":"111","author":"Dalebroux","year":"2014","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"635","DOI":"10.1146\/annurev.biochem.71.110601.135414","article-title":"Lipopolysaccharide endotoxins","volume":"71","author":"Raetz","year":"2002","journal-title":"Annu. Rev. Biochem."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"251","DOI":"10.1099\/mic.0.000604","article-title":"Loving the poison: The methylcitrate cycle and bacterial pathogenesis","volume":"164","author":"Dolan","year":"2018","journal-title":"Microbiology"},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"396","DOI":"10.1006\/bbrc.2002.6657","article-title":"The function of OmpA in Escherichia coli","volume":"292","author":"Wang","year":"2002","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"6352","DOI":"10.4049\/jimmunol.169.11.6352","article-title":"A novel interaction of outer membrane protein A with C4b binding protein mediates serum resistance of Escherichia coli K1","volume":"169","author":"Prasadarao","year":"2002","journal-title":"J. Immunol."},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"6012","DOI":"10.1128\/IAI.72.10.6012-6022.2004","article-title":"Inhibition of apoptosis by Escherichia coli K1 is accompanied by increased expression of BclXL and blockade of mitochondrial cytochrome c release in macrophages","volume":"72","author":"Sukumaran","year":"2004","journal-title":"Infect. Immun."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"4269","DOI":"10.1002\/pmic.200600193","article-title":"Proteomic analysis of Escherichia coli biofilms reveals the overexpression of the outer membrane protein OmpA","volume":"6","author":"Orme","year":"2006","journal-title":"Proteomics"},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"2566","DOI":"10.1128\/IAI.68.5.2566-2572.2000","article-title":"Outer membrane protein A, peptidoglycan-associated lipoprotein, and murein lipoprotein are released by Escherichia coli bacteria into serum","volume":"68","author":"Hellman","year":"2000","journal-title":"Infect. Immun."},{"key":"ref_78","doi-asserted-by":"crossref","unstructured":"Sultan, A., Jers, C., Ganief, T.A., Shi, L., Senissar, M., K\u00f8hler, J.B., Macek, D., and Mijakovic, I. (2021). Phosphoproteome Study of Escherichia coli Devoid of Ser\/Thr Kinase YeaG During the Metabolic Shift From Glucose to Malate. Front. Microbiol., 12.","DOI":"10.3389\/fmicb.2021.657562"},{"key":"ref_79","first-page":"5773","article-title":"Propionylation of lysine, a new mechanism of short-chain fatty acids affecting bacterial virulence","volume":"14","author":"Tang","year":"2022","journal-title":"Am. J. Transl. Res."},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"850","DOI":"10.1021\/ac950914h","article-title":"Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels","volume":"68","author":"Shevchenko","year":"1996","journal-title":"Anal. Chem."}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/25\/18\/10118\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T16:00:55Z","timestamp":1760112055000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/25\/18\/10118"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,9,20]]},"references-count":80,"journal-issue":{"issue":"18","published-online":{"date-parts":[[2024,9]]}},"alternative-id":["ijms251810118"],"URL":"https:\/\/doi.org\/10.3390\/ijms251810118","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,9,20]]}}}