SslE Elicits Functional Antibodies That Impair In Vitro Mucinase Activity and In Vivo Colonization by Both Intestinal and Extraintestinal Escherichia coli Strains
Open accessAbstract
SslE, the Secreted and surface-associated lipoprotein from Escherichia coli, has recently been associated to the M60-like extracellular zinc-metalloprotease sub-family which is implicated in glycan recognition and processing. SslE can be divided into two main variants and we recently proposed it as a potential vaccine candidate. By applying a number of in vitro bioassays and comparing wild type, knockout mutant and complemented strains, we have now demonstrated that SslE specifically contributes to degradation of mucin substrates, typically present in the intestine and bladder. Mutation of the zinc metallopeptidase motif of SslE dramatically impaired E. coli mucinase activity, confirming the specificity of the phenotype observed. Moreover, antibodies raised against variant I SslE, cloned from strain IHE3034 (SslEIHE3034), are able to inhibit translocation of E. coli strains expressing different variants through a mucin-based matrix, suggesting that SslE induces cross-reactive functional antibodies that affect the metallopeptidase activity. To test this hypothesis, we used well-established animal models and demonstrated that immunization with SslEIHE3034 significantly reduced gut, kidney and spleen colonization by strains producing variant II SslE and belonging to different pathotypes. Taken together, these data strongly support the importance of SslE in E. coli colonization of mucosal surfaces and reinforce the use of this antigen as a component of a broadly protective vaccine against pathogenic E. coli species.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The zinc metalloproteases StcE and SslE secreted by E. coli EHEC and EPEC/ETEC respectively contribute to intimate adherence of these bacteria to host cells, a process essential for colonization.
“Finally, the zinc metalloproteases StcE and SslE secreted by E. coli EHEC and EPEC/ETEC respectively, contribute to intimate adherence of these bacteria to host cells, a process that is essential for colonization.73–78”
From The emerging roles of bacterial proteases in intestinal diseases (2023) · cites this paper as [78]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) Software Version 4.0
Tamura, K., Dudley, J. T., Nei, M., & Kumar, S. (2007) · Molecular Biology and Evolution · doi:10.1093/molbev/msm092 · Cited by 28,734 · see citing works
Kaper, J. B., Nataro, J. P., & Mobley, H. L. T. (2004) · Nature Reviews Microbiology · doi:10.1038/nrmicro818 · Cited by 5,583 · see citing works
Self-citationRecent Advances in Understanding Enteric Pathogenic Escherichia coli
Croxen, M. A., Law, R. J., Scholz, R., Keeney, K. M., Wlodarska, M., & Finlay, B. B. (2013) · Clinical Microbiology Reviews · doi:10.1128/cmr.00022-13 · Cited by 1,578 · see citing works
Immune adaptations that maintain homeostasis with the intestinal microbiota
Hooper, L. V., & Macpherson, A. J. (2010) · Nature reviews. Immunology · doi:10.1038/nri2710 · Cited by 1,455 · see citing works
Mucins in the mucosal barrier to infection
Lindén, S. K., SUTTON, P. R. N., Karlsson, N. G., Korolik, V., & McGuckin, M. A. (2008) · Mucosal Immunology · doi:10.1038/mi.2008.5 · Cited by 1,241 · see citing works
The type II secretion system: biogenesis, molecular architecture and mechanism
Korotkov, K. V., Sandkvist, M., & Hol, W. G. J. (2012) · Nature Reviews Microbiology · doi:10.1038/nrmicro2762 · Cited by 553 · see citing works
A unique signature identifies a family of zinc‐dependent metallopeptidases
Jongeneel, C. V., Bouvier, J., & Bairoch, A. (1989) · FEBS Letters · doi:10.1016/0014-5793(89)80471-5 · Cited by 462 · see citing works
Six widespread bacterial clones among Escherichia coli K1 isolates
Achtman, M., Mercer, A. A., Kušećek, B., Pohl, A., Heuzenroeder, M. W., Aaronson, W., Sutton, A., & Silver, R. P. (1983) · Infection and Immunity · doi:10.1128/iai.39.1.315-335.1983 · Cited by 447 · see citing works
Lane, M. C., Alteri, C. J., Smith, S. N., & Mobley, H. L. T. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0607898104 · Cited by 406 · see citing works
Self-citationBień, J., Sokolova, O. V., & Bozko, P. M. (2012) · International Journal of Nephrology · doi:10.1155/2012/681473 · Cited by 363 · see citing works
Hagberg, L., Engberg, I., Freter, R. R., Lam, J. S., Olling, S., & Edén, C. S. (1983) · Infection and Immunity · doi:10.1128/iai.40.1.273-283.1983 · Cited by 362 · see citing works
Iguchi, A., Thomson, N. R., Ogura, Y., Saunders, D., Ooka, T., Henderson, I. R., Harris, D. E., Asadulghani, M., Kurokawa, K., Dean, P., et al. (2008) · Journal of Bacteriology · doi:10.1128/jb.01238-08 · Cited by 333 · see citing works
Klock, H. E., & Lesley, S. A. (2008) · Methods in molecular biology · doi:10.1007/978-1-59745-196-3_6 · Cited by 308 · see citing works
An intestinal mucin is the target substrate for a baculovirus enhancin
Wang, P., & Granados, R. R. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.13.6977 · Cited by 275 · see citing works
Abrupt Emergence of a Single Dominant Multidrug-Resistant Strain of Escherichia coli
Johnson, J. R., Tchesnokova, V. L., Johnston, B., Clabots, C., Roberts, P. L., Billig, M., Riddell, K., Rogers, P., Qin, X. G., Butler‐Wu, S. M., et al. (2013) · The Journal of Infectious Diseases · doi:10.1093/infdis/jis933 · Cited by 267 · see citing works
Moriel, D. G., Bertoldi, I., Spagnuolo, A., Marchi, S., Rosini, R., Nesta, B., Pastorello, I., Corea, V. A. M., Torricelli, G., Cartocci, E., et al. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0915077107 · Cited by 261 · see citing works
Self-citationA novel dispersin protein in enteroaggregative Escherichia coli
Sheikh, J., Czeczulin, J. R., Harrington, S. M., Hicks, S., Henderson, I. R., Bouguénec, C. L., Gounon, P., Phillips, A. D., & Nataro, J. P. (2002) · Journal of Clinical Investigation · doi:10.1172/jci16172 · Cited by 255 · see citing works
Emergence of Metallo-β-Lactamase NDM-1-Producing Multidrug-Resistant Escherichia coli in Australia
Poirel, L., Lagrutta, E., Taylor, P. C., Pham, J., & Nordmann, P. (2010) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.00878-10 · Cited by 243 · see citing works
The Evolution of Mutualism in Gut Microbiota Via Host Epithelial Selection
Schlüter, J., & Foster, K. R. (2012) · PLoS Biology · doi:10.1371/journal.pbio.1001424 · Cited by 228 · see citing works
Preventing urinary tract infection: progress toward an effective Escherichia coli vaccine
Brumbaugh, A. R., & Mobley, H. L. T. (2012) · Expert Review of Vaccines · doi:10.1586/erv.12.36 · Cited by 204 · see citing works
Self-citationZhou, J. S., Gopal, P. K., & Gill, H. S. (2001) · International Journal of Food Microbiology · doi:10.1016/s0168-1605(00)00398-6 · Cited by 178 · see citing works
Mucosal penetration primes Vibrio cholerae for host colonization by repressing quorum sensing
Liu, Z., Miyashiro, T., Tsou, A. M., Hsiao, A., Goulian, M., & Zhu, J. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0802241105 · Cited by 166 · see citing works
Evidence for degradation of gastrointestinal mucin by Candida albicans secretory aspartyl proteinase
Colina, A. R., Aumont, F., Deslauriers, N., Belhumeur, P., & de Repentigny, L. (1996) · Infection and Immunity · doi:10.1128/iai.64.11.4514-4519.1996 · Cited by 161 · see citing works
Nesta, B., Spraggon, G., Alteri, C. J., Moriel, D. G., Rosini, R., Veggi, D., Smith, S. N., Bertoldi, I., Pastorello, I., Ferlenghi, I., et al. (2012) · mBio · doi:10.1128/mbio.00010-12 · Cited by 143 · see citing works
Self-citationVaccines against enterotoxigenicEscherichia coli
Svennerholm, A.-M., & Tobias, J. (2008) · Expert Review of Vaccines · doi:10.1586/14760584.7.6.795 · Cited by 117 · see citing works
Nakjang, S., Ndeh, D. A., Wipat, A., Bolam, D. N., & Hirt, R. P. (2012) · PLoS ONE · doi:10.1371/journal.pone.0030287 · Cited by 116 · see citing works
Progress and hurdles in the development of vaccines against enterotoxigenicEscherichia coliin humans
Zhang, W., & Sack, D. A. (2012) · Expert Review of Vaccines · doi:10.1586/erv.12.37 · Cited by 114 · see citing works
Smith, S. N., Hagan, E. C., Lane, M. C., & Mobley, H. L. T. (2010) · mBio · doi:10.1128/mbio.00262-10 · Cited by 110 · see citing works
Self-citationVaccines Against Enterotoxigenic Escherichia coli
Svennerholm, A.-M., & Glenn, G. (2016) · CRC Press eBooks · doi:10.3109/9781420060744-69 · Cited by 105 · see citing works
Vibrio cholerae virulence regulator-coordinated evasion of host immunity
Hsiao, A., Liu, Z., Joelsson, A., & Zhu, J. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0604650103 · Cited by 100 · see citing works
Contribution of Hemagglutinin/Protease and Motility to the Pathogenesis of El Tor Biotype Cholera
Silva, A. J., Leitch, G. J., Camilli, A., & Benítez, J. A. (2006) · Infection and Immunity · doi:10.1128/iai.74.4.2072-2079.2006 · Cited by 100 · see citing works
Baldi, D. L., Higginson, E. E., Hocking, D. M., Praszkier, J., Cavaliere, R., James, C. E., Bennett-Wood, V. R., Azzopardi, K. I., Turnbull, L., Lithgow, T. J., et al. (2012) · Infection and Immunity · doi:10.1128/iai.06160-11 · Cited by 98 · see citing works
Wieser, A., Romann, E., Magistro, G., Hoffmann, C., Nörenberg, D., Weinert, K., & Schubert, S. (2010) · Infection and Immunity · doi:10.1128/iai.00174-10 · Cited by 92 · see citing works
Enteropathogenic and enterohemorrhagic E. coli: ecology, pathogenesis, and evolution
Hartland, E. L., & Leong, J. M. (2013) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2013.00015 · Cited by 87 · see citing works
Vaccines for preventing enterotoxigenic Escherichia coli (ETEC) diarrhoea
Ahmed, T., Bhuiyan, T. R., Zaman, K., Sinclair, D., & Qadri, F. (2013) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd009029.pub2 · Cited by 77 · see citing works
Vigil, P. D., Stapleton, A. E., Johnson, J. R., Hooton, T. M., Hodges, A. P., He, Y. O., & Mobley, H. L. T. (2011) · mBio · doi:10.1128/mbio.00066-11 · Cited by 59 · see citing works
Self-citationRol, N., Favre, L., Benyacoub, J., & Corthésy, B. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.405001 · Cited by 57 · see citing works
Rhee, K., Cheng, H., Harris, A., Morin, C. E., Kaper, J. B., & Hecht, G. A. (2011) · Gut Microbes · doi:10.4161/gmic.2.1.14882 · Cited by 53 · see citing works
Yang, J. W., Baldi, D. L., Tauschek, M., Strugnell, R. A., & Robins-Browne, R. M. (2006) · Journal of Bacteriology · doi:10.1128/jb.01115-06 · Cited by 50 · see citing works
Strozen, T. G., Li, G., & Howard, S. P. (2012) · Infection and Immunity · doi:10.1128/iai.06394-11 · Cited by 47 · see citing works
Hernandes, R. T., la Cruz, M. Á. D., Yamamoto, D., Girón, J. A., & Gomes, T. A. T. (2013) · Infection and Immunity · doi:10.1128/iai.00620-13 · Cited by 44 · see citing works
Nicklasson, M., Sjöling, Å., von Mentzer, A., Qadri, F., & Svennerholm, A. (2012) · PLoS ONE · doi:10.1371/journal.pone.0035827 · Cited by 42 · see citing works
Escherichia coli: Great Diversity around a Common Core
Moriel, D. G., Rosini, R., Seib, K. L., Serino, L., Pizza, M., & Rappuoli, R. (2012) · mBio · doi:10.1128/mbio.00118-12 · Cited by 41 · see citing works
Self-citationIdentification of a mucin layerin the urinary bladder
Grist, M., & Chakraborty, J. (1994) · Urology · doi:10.1016/s0090-4295(94)80005-7 · Cited by 38 · see citing works
Gibson, J. S., Cobbold, R. N., & Trott, D. J. (2010) · Journal of Medical Microbiology · doi:10.1099/jmm.0.018002-0 · Cited by 28 · see citing works
Pastorello, I., Paccani, S. R., Rosini, R., Mattera, R., Ferrer‐Navarro, M., Urosev, D., Nesta, B., Surdo, P. L., Vecchio, M. D., Rippa, V., et al. (2013) · mBio · doi:10.1128/mbio.00206-13 · Cited by 28 · see citing works
Self-citationTorres, A. G., Cieza, R. J., Rojas-López, M., Blumentritt, C. A., Souza, C. S., Johnston, R., Strockbine, N., Kaper, J. B., Sbrana, E., & Popov, V. L. (2012) · BMC Microbiology · doi:10.1186/1471-2180-12-112 · Cited by 26 · see citing works
van der Donk, C. F. M., Schols, J. M. G. A., Driessen, C., Hagenouw, R. G. P., Meulendijks, A. M., & Stobberingh, E. E. (2012) · Journal of the American Medical Directors Association · doi:10.1016/j.jamda.2012.09.026 · Cited by 25 · see citing works
Lenart, A., Dudkiewicz, M., Grynberg, M., & Pawłowski, K. (2013) · PLoS ONE · doi:10.1371/journal.pone.0062272 · Cited by 23 · see citing works
DeCanio, M. S., Landick, R. C., & Haft, R. J. F. (2013) · BMC Microbiology · doi:10.1186/1471-2180-13-130 · Cited by 23 · see citing works
Carrington, S. D., Irwin, J. A., Liu, L., Rudd, P. M., Matthews, E., & Corfield, A. P. (2011) · Methods in molecular biology · doi:10.1007/978-1-61779-513-8_11 · Cited by 12 · see citing works
van der Donk, C. F. M., van de Bovenkamp, J. H. B., Bamelis, H., Driessen, C., Feldhoff, K., Kalka-Moll, W. M., Magerman, K., & Stobberingh, E. E. (2013) · Future Microbiology · doi:10.2217/fmb.13.61 · Cited by 10 · see citing works
Techniques for Assessment of Interactions of Mucins with Microbes and Parasites In Vitro and In Vivo
Sheng, Y., Hasnain, S. Z., Png, C. W., McGuckin, M. A., & Lindén, S. K. (2011) · Methods in molecular biology · doi:10.1007/978-1-61779-513-8_18 · Cited by 7 · see citing works
Emergence of VIM-1 Metallo-β-Lactamase-Producing Escherichia coli in a Neonatal Intensive Care Unit
Papadimitriou, M., Voulgari, E., Ranellou, K., Koemtzidou, E., Lebessi, E., & Tsakris, A. (2010) · Microbial Drug Resistance · doi:10.1089/mdr.2010.0097 · Cited by 5 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Pathogenicity Factors of Genomic Islands in Intestinal and Extraintestinal Escherichia coli
Desvaux, M., Dalmasso, G., Beyrouthy, R., Barnich, N., Delmas, J., & Bonnet, R. (2020) · Frontiers in Microbiology · doi:10.3389/fmicb.2020.02065 · Cited by 186 · see citing works
Experimental models to study intestinal microbes–mucus interactions in health and disease
Etienne‐Mesmin, L., Chassaing, B., Desvaux, M., Paepe, K. D., Gresse, R., Sauvaitre, T., Forano, É., de Wiele, T. V., Schüller, S., Juge, N., et al. (2019) · FEMS Microbiology Reviews · doi:10.1093/femsre/fuz013 · Cited by 178 · see citing works
Evolutionary conservation of the antimicrobial function of mucus: a first defence against infection
Bakshani, C. R., Morales‐Garcia, A. L., Althaus, M., Wilcox, M. D., Pearson, J. P., Bythell, J. C., & Burgess, J. G. (2018) · npj Biofilms and Microbiomes · doi:10.1038/s41522-018-0057-2 · Cited by 160 · see citing works
Drug and Vaccine Development for the Treatment and Prevention of Urinary Tract Infections
O'Brien, V. P., Hannan, T. J., Nielsen, H. V., & Hultgren, S. J. (2016) · Microbiology Spectrum · doi:10.1128/microbiolspec.uti-0013-2012 · Cited by 157 · see citing works
Intestinal Pathogenic Escherichia coli: Insights for Vaccine Development
Rojas-López, M., Monteiro, R., Pizza, M., Desvaux, M., & Rosini, R. (2018) · Frontiers in Microbiology · doi:10.3389/fmicb.2018.00440 · Cited by 123 · see citing works
Self-citationRecognition of protein-linked glycans as a determinant of peptidase activity
Noach, I., Ficko-Blean, E., Pluvinage, B., Stuart, C., Jenkins, M. L., Brochu, D., Buenbrazo, N., Wakarchuk, W., Burke, J. E., Gilbert, M., et al. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1615141114 · Cited by 89 · see citing works
The emerging roles of bacterial proteases in intestinal diseases
Caminero, A., Guzman, M., Libertucci, J., & Lomax, A. E. (2023) · Gut Microbes · doi:10.1080/19490976.2023.2181922 · Cited by 92 · see citing works
GMMA Is a Versatile Platform to Design Effective Multivalent Combination Vaccines
Micoli, F., Alfini, R., Benedetto, R. D., Necchi, F., Schiavo, F., Mancini, F., Carducci, M., Palmieri, E., Balocchi, C., Gasperini, G., et al. (2020) · Vaccines · doi:10.3390/vaccines8030540 · Cited by 85 · see citing works
Foxo1 controls gut homeostasis and commensalism by regulating mucus secretion
Chen, Z., Luo, J., Li, J., Kim, G., Chen, E. S., Xiao, S., Snapper, S. B., Bao, B., An, D., Blumberg, R. S., et al. (2021) · The Journal of Experimental Medicine · doi:10.1084/jem.20210324 · Cited by 81 · see citing works
Hews, C. L., Tran, S.-L., Wegmann, U., Brett, B., Walsham, A. D. S., Kavanaugh, D., Ward, N. J., Juge, N., & Schüller, S. (2017) · Cellular Microbiology · doi:10.1111/cmi.12717 · Cited by 77 · see citing works
Classification, structural biology, and applications of mucin domain-targeting proteases
Shon, D. J., Kuo, A., Ferracane, M. J., & Malaker, S. A. (2021) · Biochemical Journal · doi:10.1042/bcj20200607 · Cited by 72 · see citing works
Chakraborty, S., Randall, A. Z., Vickers, T. J., Molina, D., Harro, C. D., DeNearing, B., Brubaker, J., Sack, D. A., Bourgeois, A. L., Felgner, P. L., et al. (2018) · The Journal of Infectious Diseases · doi:10.1093/infdis/jiy312 · Cited by 64 · see citing works
Wurpel, D. J., Totsika, M., Allsopp, L. P., Webb, R. I., Moriel, D. G., & Schembri, M. A. (2015) · Journal of Proteomics · doi:10.1016/j.jprot.2015.11.001 · Cited by 63 · see citing works
Genome-Wide Investigation of Biofilm Formation in Bacillus cereus
Yan, F., Yu, Y., Gozzi, K., Chen, Y., Guo, J.-H., & Chai, Y. (2017) · Applied and Environmental Microbiology · doi:10.1128/aem.00561-17 · Cited by 63 · see citing works
Ageorges, V., Monteiro, R., Léroy, S., Burgess, C. M., Pizza, M., Chaucheyras‐Durand, F., & Desvaux, M. (2020) · FEMS Microbiology Reviews · doi:10.1093/femsre/fuaa008 · Cited by 60 · see citing works
Self-citationValeri, M., Paccani, S. R., Kasendra, M. J., Nesta, B., Serino, L., Pizza, M., & Soriani, M. (2015) · PLoS ONE · doi:10.1371/journal.pone.0117486 · Cited by 60 · see citing works
Self-citationDrug and Vaccine Development for the Treatment and Prevention of Urinary Tract Infections
O'Brien, V. P., Hannan, T. J., Nielsen, H. V., & Hultgren, S. J. (2016) · ASM Press eBooks · doi:10.1128/9781555817404.ch24 · Cited by 59 · see citing works
Haurat, M. F., Scott, N. E., Venanzio, G. D., Lopez, J., Pluvinage, B., Boraston, A. B., Ferracane, M. J., & Feldman, M. F. (2020) · mBio · doi:10.1128/mbio.02033-20 · Cited by 53 · see citing works
Hay, I. D., Belousoff, M. J., Dunstan, R. A., Bamert, R. S., & Lithgow, T. J. (2017) · Journal of Bacteriology · doi:10.1128/jb.00521-17 · Cited by 43 · see citing works
Vaccines for Protecting Infants from Bacterial Causes of Diarrheal Disease
Walker, R. I., Kaminski, R. W., Porter, C. K., Choy, R. K. M., White, J. A., Fleckenstein, J. M., Cassels, F., & Bourgeois, L. (2021) · Microorganisms · doi:10.3390/microorganisms9071382 · Cited by 42 · see citing works
Glycoconjugate vaccines against antimicrobial resistant pathogens
Sorieul, C., Dolce, M., Romano, M. R., Codée, J. D. C., & Adamo, R. (2023) · Expert Review of Vaccines · doi:10.1080/14760584.2023.2274955 · Cited by 42 · see citing works
A Novel Protective Vaccine Antigen from the Core Escherichia coli Genome
Moriel, D. G., Tan, L., Goh, K., Phan, M., Ipe, D., Lo, A. W., Peters, K. M., Ulett, G., Beatson, S., & Schembri, M. (2016) · Msphere · doi:10.1128/msphere.00326-16 · Cited by 40 · see citing works
Confronting Challenges to Enterotoxigenic Escherichia coli Vaccine Development
Fleckenstein, J. M. (2021) · Frontiers in Tropical Diseases · doi:10.3389/fitd.2021.709907 · Cited by 39 · see citing works
Vaccines Against Escherichia coli
Nesta, B., & Pizza, M. (2018) · Current topics in microbiology and immunology · doi:10.1007/82_2018_111 · Cited by 36 · see citing works
Self-citationLabourel, A., Parrou, J., Deraison, C., Mercier‐Bonin, M., Lajus, S., & Potocki-Véronèse, G. (2023) · Essays in Biochemistry · doi:10.1042/ebc20220153 · Cited by 35 · see citing works
Chakraborty, S., Randall, A. Z., Vickers, T. J., Molina, D., Harro, C. D., DeNearing, B., Brubaker, J., Sack, D. A., Bourgeois, A. L., Felgner, P. L., et al. (2019) · npj Vaccines · doi:10.1038/s41541-019-0131-7 · Cited by 34 · see citing works
Mycobacterium tuberculosis Zinc Metalloprotease-1 Assists Mycobacterial Dissemination in Zebrafish
Vemula, M. H., Medishetti, R., Ganji, R., Jakkala, K., Sankati, S., Chatti, K., & Banerjee, S. (2016) · Frontiers in Microbiology · doi:10.3389/fmicb.2016.01347 · Cited by 30 · see citing works
Secreted proteases: A new insight in the pathogenesis of extraintestinal pathogenic Escherichia coli
Tapader, R., Basu, S., & Pal, A. (2019) · International Journal of Medical Microbiology · doi:10.1016/j.ijmm.2019.03.002 · Cited by 28 · see citing works
‘Omic’ Approaches to Study Uropathogenic Escherichia coli Virulence
Lo, A. W. H., Moriel, D. G., Phan, M., Schulz, B. L., Kidd, T. J., Beatson, S. A., & Schembri, M. A. (2017) · Trends in Microbiology · doi:10.1016/j.tim.2017.04.006 · Cited by 26 · see citing works
Ma, J.-L., Sun, M.-X., Pan, Z.-H., Song, W., Lu, C.-P., & Yao, H. (2018) · Emerging Microbes and Infections · doi:10.1038/s41426-018-0042-0 · Cited by 25 · see citing works
Murine Model of Chemotherapy-Induced Extraintestinal Pathogenic Escherichia coli Translocation
Green, S. I., Ajami, N. J., Ma, L. M., Poole, N. M., Price, R. E., Petrosino, J. F., & Maresso, A. W. (2015) · Infection and Immunity · doi:10.1128/iai.00684-15 · Cited by 24 · see citing works
Molecular and cellular insight into Escherichia coli SslE and its role during biofilm maturation
Corsini, P. M., Wang, S.-Y., Rehman, S., Fenn, K., Sagar, A., Sirovica, S., Cleaver, L., Edwards-Gayle, C., Mastroianni, G., Dorgan, B., et al. (2021) · bioRxiv · doi:10.1038/s41522-022-00272-5 · Cited by 17 · see citing works
Implications of enterotoxigenicEscherichia coligenomics for vaccine development
Sjöling, Å., von Mentzer, A., & Svennerholm, A. (2014) · Expert Review of Vaccines · doi:10.1586/14760584.2015.996553 · Cited by 20 · see citing works
Novel Simple Conjugation Chemistries for Decoration of GMMA with Heterologous Antigens
Benedetto, R. D., Alfini, R., Carducci, M., Aruta, M. G., Lanzilao, L., Acquaviva, A., Palmieri, E., Giannelli, C., Necchi, F., Saul, A. J., et al. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms221910180 · Cited by 19 · see citing works
Tapader, R., Bose, D., Dutta, P., Das, S., & Pal, A. (2018) · Infection and Immunity · doi:10.1128/iai.00399-18 · Cited by 19 · see citing works
Singh, S., & Koo, O. K. (2024) · Pathogens · doi:10.3390/pathogens13080642 · Cited by 15 · see citing works
Tao, J., Sang, Y., Teng, Q., Ni, J., Yang, Y., Tsui, S. K., & Yao, Y. (2015) · Frontiers in Microbiology · doi:10.3389/fmicb.2015.00051 · Cited by 16 · see citing works
Modern vaccine development via reverse vaccinology to combat antimicrobial resistance
Tobuse, A. J., Wei, A. C., & Yeong, K. Y. (2022) · Life Sciences · doi:10.1016/j.lfs.2022.120660 · Cited by 14 · see citing works
Naïli, I., Vinot, J., Baudner, B. C., Bernalier‐Donadille, A., Pizza, M., Desvaux, M., Jubelin, G., D’Oro, U., & Buonsanti, C. (2018) · Vaccine · doi:10.1016/j.vaccine.2018.10.008 · Cited by 12 · see citing works
Self-citationNishiyama, K., Sugiyama, M., Yamada, H., Makino, K., Ishihara, S., Takaki, T., Mukai, T., & Okada, N. (2019) · Scientific Reports · doi:10.1038/s41598-019-41151-y · Cited by 12 · see citing works
Yilmaz, C., Rangarajan, A. A., & Schnetz, K. (2020) · Journal of Bacteriology · doi:10.1128/jb.00427-20 · Cited by 12 · see citing works
Tan, L., Moriel, D. G., Totsika, M., Beatson, S. A., & Schembri, M. A. (2016) · PLoS ONE · doi:10.1371/journal.pone.0162391 · Cited by 11 · see citing works
Gu, X., Ma, X., Wu, Q., Tao, Q., Chai, Y., Zhou, X., Han, M., Li, J., Huang, X., Wu, T., et al. (2023) · Veterinary Medicine and Science · doi:10.1002/vms3.1101 · Cited by 9 · see citing works
Krekhno, Z., Woodward, S. E., Serapio-Palacios, A., Peña-Díaz, J., Moon, K. M., Foster, L., & Finlay, B. B. (2024) · Gut Microbes · doi:10.1080/19490976.2024.2308049 · Cited by 9 · see citing works
Bacconi, M., Haag, A. F., Torre, A., Castagnetti, A., Chiarot, E., Delany, I., & Bensi, G. (2015) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-015-7229-2 · Cited by 9 · see citing works
Self-citationLinking inherent O-Linked Protein Glycosylation of YghJ to Increased Antigen Potential
Thorsing, M., Krogh, T. J., Vitved, L., Nawrocki, A., Jakobsen, R., Larsen, M. R., Chakraborty, S., Bourgeois, A. L., Andersen, A. Z., & Boysen, A. (2021) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2021.705468 · Cited by 9 · see citing works
Rojas-López, M., Martinelli, M., Brandi, V., Jubelin, G., Polticelli, F., Soriani, M., Pizza, M., Desvaux, M., & Rosini, R. (2019) · Scientific Reports · doi:10.1038/s41598-019-53197-z · Cited by 7 · see citing works
Self-citationGlycosylation of bacterial antigens changes epitope patterns
Kern, K., Delaroque, N., Boysen, A., Puder, M., Wendt, R. T., Kölsch, A., Ehrentreich‐Förster, E., Stærk, K., Andersen, T. E., Andersen, K., et al. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1258136 · Cited by 7 · see citing works
Micoli, F., Rondini, S., Scorza, F. B., & Adamo, R. (2026) · Expert Review of Vaccines · doi:10.1080/14760584.2026.2622690 · Cited by 6 · see citing works
Reid, C. E., Taylor, R. S., Bissett, A. B., Nowak, B. F., & Bowman, J. P. (2025) · Frontiers in Microbiology · doi:10.3389/fmicb.2025.1564052 · Cited by 5 · see citing works
Riaz, S., Steinsland, H., Andersen, A. Z., Boysen, A., & Hanevik, K. (2024) · Medical Microbiology and Immunology · doi:10.1007/s00430-024-00812-0 · Cited by 5 · see citing works
Oral Vaccines for Enterotoxigenic Escherichia coli
Carlin, N., & Svennerholm, A. (2019) · Elsevier eBooks · doi:10.1016/b978-0-12-811924-2.00032-8 · Cited by 5 · see citing works
Riaz, S., Steinsland, H., Thorsing, M., Andersen, A. Z., Boysen, A., & Hanevik, K. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.760135 · Cited by 5 · see citing works
Deraison, C., Bonnart, C., & Vergnolle, N. (2017) · Wiley-VCH eBooks · doi:10.1002/9783527692156.ch28 · Cited by 4 · see citing works
Trovão, L. O., Vieira, M. A. M., Santos, A. C. D. M., Puño-Sarmiento, J. J., Nunes, P. H. S., Santos, F. F., Rocha, V. G. P., Knöbl, T., Navarro‐García, F., & Gomes, T. A. T. (2024) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2024.1393369 · Cited by 4 · see citing works
Mucin stimulates the growth of Legionella pneumophila
Vargas, A., Kuhlemeier, H., & Cianciotto, N. P. (2026) · Microbiology · doi:10.1099/mic.0.001682 · Cited by 3 · see citing works
Staff, T. P. P. (2015) · PLoS Pathogens · doi:10.1371/journal.ppat.1004773 · Cited by 2 · see citing works
Keizers, M., Mukherjee, K., Berger, M., & Dobrindt, U. (2025) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2025.1603759 · Cited by 1 · see citing works
The virulence regulator AbsR in avian pathogenic has pleiotropic effects on bacterial physiology
Zhao, D., Zhang, H., Zhang, X., Jiang, F., Li, Y., Cai, W., & Li, G. (2023) · Journal of Integrative Agriculture · doi:10.1016/j.jia.2023.07.035 · Cited by 1 · see citing works
Walsham, A. D. S. (2016) · UEA Digital Repository (University of East Anglia) · Cited by 1 · see citing works
Tapader, R., & Pal, A. (2019) · Springer eBooks · doi:10.1007/978-981-13-8763-0_19
Active colonisers of the gastrointestinal tract of Atlantic salmon farmed in a warm water regionPreprint
Hall, K., Reid, C. E., Tan, Q. Z., Taylor, R. S., Bissett, A. B., Ruff, N., Nowak, B. F., & Bowman, J. P. (2024) · Research Square · doi:10.21203/rs.3.rs-4361310/v1
Hall, K., Reid, C. E., Hamlett, J., Kaur, D., Tan, Q. Z., Taylor, R. S., Bissett, A. B., Nowak, B. F., & Bowman, J. P. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.11.23.625004
Riaz, S., Steinsland, H., Boysen, A., & Hanevik, K. (2025) · Gut Pathogens · doi:10.1186/s13099-025-00748-7
Talabnin, K., Wendo, W. D., Suyapoh, W., Tangkawattana, S., Sripa, B., & Suttiprapa, S. (2026) · Advances in experimental medicine and biology · doi:10.1007/978-3-032-04153-1_27
Revisiting the type II secretion system: it is more than you might think
Cianciotto, N. P., Mayoral, J., & Garnett, J. A. (2026) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00118-25
Riaz, S., Rim, S., Steinsland, H., Vedøy, O. B., Vickers, T. J., Fleckenstein, J. M., & Hanevik, K. (2026) · European Journal of Immunology · doi:10.1002/eji.70246
- Authors
- Nesta, B., Valeri, M., Spagnuolo, A., Rosini, R., Mora, M., Donato, P., Alteri, C. J., Del Vecchio, M., Buccato, S., Pezzicoli, A., Bertoldi, I., Buzzigoli, L., Tuscano, G., Falduto, M., Rippa, V., Ashhab, Y., Bensi, G., Fontana, M. R., Seib, K. L., Mobley, H. L. T., Pizza, M., Soriani, M., & Serino, L.
- Affiliations
- Novartis (Italy) (IT)
- University of Michigan (US)
- Palestine Polytechnic University (PS)
- Griffith University (AU)
- Corresponding author
- Soriani, Marco
- ORCID
- Venue
- PLoS Pathogens
- Publisher
- Public Library of Science (PLoS)
- Published
- 2014-05-08
- Volume
- 10
- Issue
- 5
- Pages
- e1004124
- ISSN
- 1553-7366 (ISSN-L)
- 1553-7374
- PMC
- PMC4014459
- OpenAlex
- W2039204405
- Cited by
- 68
- References
- 54
- Citations by year
- 2026: 5 · 2025: 3 · 2024: 6 · 2023: 6 · 2022: 2 · 2021: 7 · 2020: 5 · 2019: 8 · 2018: 7 · 2017: 6 · 2016: 6 · 2015: 6 · 2014: 1
- FWCI
- 4.46
- Type
- journal article
- Language
- en
- Update notices
- correction (2015-03-25)
- Open access
- gold
- doi.org
- Locations
- PLoS Pathogens (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Figshare (submittedVersion, cc-by)
- Griffith Research Online (submittedVersion)
- Funders
- Imperial College London
- European Commission (219235)
- National Institutes of Health (AI43363)
- National Institute of Allergy and Infectious Diseases (R01AI043363, R01 AI43363)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Endocrinology › Escherichia coli research studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Biochemical and Structural Characterization
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
- Keywords
- Escherichia coli, mucinase, zinc metallopeptidase, functional antibodies, mucin degradation, bacterial colonization, vaccine candidate, cross-reactive antibodies, extraintestinal Escherichia coli, intestinal colonization, glycan processing
- MeSH terms
- Animals, Antibodies, Bacterial, Antibody Formation, Cells, Cultured, Enzyme Activation, Escherichia coli, Escherichia coli Infections, Female, Intestines, Mice, Inbred CBA, Polysaccharide-Lyases, Animals, Outbred Strains, Escherichia coli Proteins, Virulence Factors, Mice, Enteropathogenic Escherichia coli
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review