Bacterial serine proteases secreted by the autotransporter pathway: classification, specificity, and role in virulence

Ruiz-Perez, Fernando; Nataro, James P.

doi:10.1007/s00018-013-1355-8

Cited by 149Escherichia coli research studiesBacterial Genetics and BiotechnologyBiochemical and Structural Characterization

Bacterial serine proteases secreted by the autotransporter pathway: classification, specificity, and role in virulence

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Ruiz-Perez, Fernando, Nataro, James P.·2014·Cellular and Molecular Life Sciences

DOI 10.1007/s00018-013-1355-8PMC PMC3871983

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Abstract

Serine proteases exist in eukaryotic and prokaryotic organisms and have emerged during evolution as the most abundant and functionally diverse group. In Gram-negative bacteria, there is a growing family of high molecular weight serine proteases secreted to the external milieu by a fascinating and widely employed bacterial secretion mechanism, known as the autotransporter pathway. They were initially found in Neisseria, Shigella, and pathogenic Escherichia coli, but have now also been identified in Citrobacter rodentium, Salmonella, and Edwardsiella species. Here, we focus on proteins belonging to the serine protease autotransporter of Enterobacteriaceae (SPATEs) family. Recent findings regarding the predilection of serine proteases to host intracellular or extracellular protein-substrates involved in numerous biological functions, such as those implicated in cytoskeleton stability, autophagy or innate and adaptive immunity, have helped provide a better understanding of SPATEs' contributions in pathogenesis. Here, we discuss their classification, substrate specificity, and potential roles in pathogenesis.

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Class-1 serine protease autotransporters from enterobacteriaceae target intracellular substrates, eliciting cytotoxic and endotoxin effects on the host.
“Class-1 SPATEs target intracellular substrates, eliciting cytotoxic and endotoxin effects on the host.67”
From The emerging roles of bacterial proteases in intestinal diseases (2023) · cites this paper as [67]
Serine protease autotransporters from enterobacteriaceae degrade host intracellular or extracellular substrates, which trigger a variety of adverse effects on host cells.
“Several findings suggest that SPATEs degrade host intracellular or extracellular substrates, which trigger a variety of adverse effects on host cells.67”
From The emerging roles of bacterial proteases in intestinal diseases (2023) · cites this paper as [67]

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Guindon, S., Dufayard, J.-F., Lefort, V., Anisimova, M., Hordijk, W., & Gascuel, O. (2010) · Systematic Biology · doi:10.1093/sysbio/syq010 · Cited by 18,376 · see citing works
Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega
Sievers, F., Wilm, A., Dineen, D., Gibson, T., Karplus, K., Li, W.-Z., Lopez, R., McWilliam, H., Remmert, M., Söding, J., et al. (2011) · Molecular Systems Biology · doi:10.1038/msb.2011.75 · Cited by 15,576 · see citing works
SignalP 4.0: discriminating signal peptides from transmembrane regions
Petersen, T. N., Brunak, S., von Heijne, G., & Nielsen, H. (2011) · Nature Methods · doi:10.1038/nmeth.1701 · Cited by 8,847 · see citing works
The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling
Arnold, K., Bordoli, L., Kopp, J., & Schwede, T. F. (2005) · Bioinformatics · doi:10.1093/bioinformatics/bti770 · Cited by 6,951 · see citing works
Pathogenic Escherichia coli
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-citation
Phylogeny.fr: robust phylogenetic analysis for the non-specialist
Dereeper, A., Guignon, V., Blanc, G., Audic, S., Buffet, S., Chevenet, F., Dufayard, J.-F., Guindon, S., Lefort, V., Lescot, M., et al. (2008) · Nucleic Acids Research · doi:10.1093/nar/gkn180 · Cited by 4,700 · see citing works
The SWISS-MODEL Repository and associated resources
Kiefer, F., Arnold, K., Künzli, M., Bordoli, L., & Schwede, T. F. (2008) · Nucleic Acids Research · doi:10.1093/nar/gkn750 · Cited by 2,003 · see citing works
Mammalian autophagy: core molecular machinery and signaling regulation
Yang, Z., & Klionsky, D. J. (2010) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2009.11.014 · Cited by 1,956 · see citing works
CX 3 CR1-Mediated Dendritic Cell Access to the Intestinal Lumen and Bacterial Clearance
Niess, J. H., Brand, S., Gu, X., Landsman, L., Jung, S., McCormick, B. A., Vyas, J. M., Boes, M. L., Ploegh, H. L., Fox, J. G., et al. (2005) · Science · doi:10.1126/science.1102901 · Cited by 1,609 · see citing works
MEROPS: the database of proteolytic enzymes, their substrates and inhibitors
Rawlings, N. D., Barrett, A. J., & Bateman, A. G. (2011) · Nucleic Acids Research · doi:10.1093/nar/gkr987 · Cited by 1,539 · see citing works
Global burden of Shigella infections: implications for vaccine development and implementation of control strategies.
Kotloff, K. L., Winickoff, J. P., Ivanoff, B., Clemens, J. D., Swerdlow, D. L., Sansonetti, P. J., Adak, G. K., & Levine, M. M. (1999) · Europe PMC (PubMed Central) · Cited by 1,242 · see citing works
TreeDyn: towards dynamic graphics and annotations for analyses of trees
Chevenet, F., Brun, C., Bañuls, A., Jacq, B., & Christen, R. (2006) · BMC Bioinformatics · doi:10.1186/1471-2105-7-439 · Cited by 1,061 · see citing works
CD44: Structure, Function and Association with the Malignant Process
Naor, D., Sionov, R. V., & Ish‐Shalom, D. (1997) · Advances in cancer research · doi:10.1016/s0065-230x(08)60101-3 · Cited by 1,020 · see citing works
MEROPS: the peptidase database
Rawlings, N. D., Barrett, A. J., & Bateman, A. G. (2009) · Nucleic Acids Research · doi:10.1093/nar/gkp971 · Cited by 974 · see citing works
MatGAT: An application that generates similarity/identity matrices using protein or DNA sequences
Campanella, J. J., Bitincka, L., & Smalley, J. V. (2003) · BMC Bioinformatics · doi:10.1186/1471-2105-4-29 · Cited by 857 · see citing works
Origins of the E. coli Strain Causing an Outbreak of Hemolytic–Uremic Syndrome in Germany
Rasko, D. A., Webster, D. R., Sahl, J. W., Bashir, A., Boisen, N., Scheutz, F., Paxinos, E. E., Sebra, R., Chin, C.-S., Iliopoulos, D., et al. (2011) · New England Journal of Medicine · doi:10.1056/nejmoa1106920 · Cited by 825 · see citing works
Self-citation
Gene structure and extracellular secretion of Neisseria gonorrhoeae IgA protease
Pohlner, J., Halter, R., Beyreuther, K. T., & Meyer, T. F. (1987) · Nature · doi:10.1038/325458a0 · Cited by 635 · see citing works
TIM genes: a family of cell surface phosphatidylserine receptors that regulate innate and adaptive immunity
Freeman, G. J., Casasnovas, J. M., Umetsu, D. T., & DeKruyff, R. H. (2010) · Immunological Reviews · doi:10.1111/j.0105-2896.2010.00903.x · Cited by 613 · see citing works
The great escape: structure and function of the autotransporter proteins
Henderson, I. R., Navarro‐García, F., & Nataro, J. P. (1998) · Trends in Microbiology · doi:10.1016/s0966-842x(98)01318-3 · Cited by 556 · see citing works
Self-citation
Citrobacter rodentium of mice and man
Mundy, R., Macdonald, T., Dougan, G., Frankel, G., & Wiles, S. (2005) · Cellular Microbiology · doi:10.1111/j.1462-5822.2005.00625.x · Cited by 545 · see citing works
Serine peptidases: Classification, structure and function
Page, M. J., & Di, E. (2008) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-008-7565-9 · Cited by 441 · see citing works
Complete Genome Sequence and Comparative Genomics ofShigella flexneriSerotype 2a Strain 2457T
Wei, J., Goldberg, M. B., Burland, V., Venkatesan, M. M., Deng, W., Fournier, G. P., Mayhew, G. F., Plunkett, G., Rose, D. J., Darling, A. E., et al. (2003) · Infection and Immunity · doi:10.1128/iai.71.5.2775-2786.2003 · Cited by 424 · see citing works
Genome dynamics and diversity of Shigella species, the etiologic agents of bacillary dysentery
Yang, F. (2005) · Nucleic Acids Research · doi:10.1093/nar/gki954 · Cited by 415 · see citing works
EspP, a novel extracellular serine protease of enterohaemorrhagic Escherichia coli O157:H7 cleaves human coagulation factor V
Brunder, W., Schmidt, H., & Karch, H. (1997) · Molecular Microbiology · doi:10.1046/j.1365-2958.1997.3871751.x · Cited by 381 · see citing works
Clinical trials of Shigella vaccines: two steps forward and one step back on a long, hard road
Levine, M. M., Kotloff, K. L., Barry, E. M., et al. (2007) · Nature Reviews Microbiology · doi:10.1038/nrmicro1662 · Cited by 375 · see citing works
Characterization of Pic, a Secreted Protease of Shigella flexneri and Enteroaggregative Escherichia coli
Henderson, I. R., Czeczulin, J., Eslava, C., Noriega, F., & Nataro, J. P. (1999) · Infection and Immunity · doi:10.1128/iai.67.11.5587-5596.1999 · Cited by 357 · see citing works
Self-citation
Secretion and subcellular localizations of bacterial proteins: a semantic awareness issue
Desvaux, M., Hébraud, M., Talon, R., & Henderson, I. R. (2009) · Trends in Microbiology · doi:10.1016/j.tim.2009.01.004 · Cited by 347 · see citing works
CX3CR1 regulates intestinal macrophage homeostasis, bacterial translocation, and colitogenic Th17 responses in mice
Contreras, O. M., Geem, D., Laur, O., Williams, I. R., Lira, S. A., Nusrat, A., Parkos, C. A., & Denning, T. L. (2011) · Journal of Clinical Investigation · doi:10.1172/jci59150 · Cited by 325 · see citing works
Structure of Bordetella pertussis virulence factor P.69 pertactin
Emsley, P., Charles, I. G., Fairweather, N. F., & Isaacs, N. W. (1996) · Nature · doi:10.1038/381090a0 · Cited by 318 · see citing works
Trimeric autotransporter adhesins: variable structure, common function
Linke, D., Riess, T. M., Autenrieth, I. B., Lupas, A. N., & Kempf, V. A. J. (2006) · Trends in Microbiology · doi:10.1016/j.tim.2006.04.005 · Cited by 308 · see citing works
Protein Secretion in Gram-Negative Bacteria via the Autotransporter Pathway
Dautin, N., & Bernstein, H. D. (2007) · Annual Review of Microbiology · doi:10.1146/annurev.micro.61.080706.093233 · Cited by 298 · see citing works
A millennium update on pediatric diarrheal illness in the developing world.
O’Ryan, M., Prado, V., & Pickering, L. K. (2005) · Seminars in Pediatric Infectious Diseases · doi:10.1053/j.spid.2005.12.008 · Cited by 283 · see citing works
Type V secretion: mechanism(s) of autotransport through the bacterial outer membrane
Leo, J. C., Grin, I., & Linke, D. (2012) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2011.0208 · Cited by 269 · see citing works
Identification of protective and broadly conserved vaccine antigens from the genome of extraintestinal pathogenic Escherichia coli
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
Two‐partner secretion in Gram‐negative bacteria: a thrifty, specific pathway for large virulence proteins
Jacob‐Dubuisson, F., Locht, C., & Antoine, R. (2001) · Molecular Microbiology · doi:10.1046/j.1365-2958.2001.02278.x · Cited by 261 · see citing works
Protein secretion by enteropathogenic Escherichia coli is essential for transducing signals to epithelial cells.
Kenny, B., & Finlay, B. B. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.17.7991 · Cited by 250 · see citing works
Pet, an Autotransporter Enterotoxin from Enteroaggregative Escherichia coli
Eslava, C. A., Navarro‐García, F., Czeczulin, J. R., et al. (1998) · Infection and Immunity · doi:10.1128/iai.66.7.3155-3163.1998 · Cited by 250 · see citing works
Relationship between the Tsh Autotransporter and Pathogenicity of Avian Escherichia coli and Localization and Analysis of the tsh Genetic Region
Dozois, C. M., Dho-Moulin, M., Brée, A., Fairbrother, J. M., Désautels, C., & Curtiss, R. (2000) · Infection and Immunity · doi:10.1128/iai.68.7.4145-4154.2000 · Cited by 247 · see citing works
Discovery of an archetypal protein transport system in bacterial outer membranes
Selkrig, J., Mosbahi, K., Webb, C. T., Belousoff, M. J., Perry, A., Wells, T. J., Morris, F. C., Leyton, D. L., Totsika, M., Phan, M., et al. (2012) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2261 · Cited by 223 · see citing works
Identification of Sat, an autotransporter toxin produced by uropathogenic Escherichia coli
Guyer, D. M., Henderson, I. R., Nataro, J. P., et al. (2000) · Molecular Microbiology · doi:10.1046/j.1365-2958.2000.02110.x · Cited by 219 · see citing works
Self-citation
Isolation and characterization of a gene involved in hemagglutination by an avian pathogenic Escherichia coli strain
Provence, D. L., & Curtiss, R. (1994) · Infection and Immunity · doi:10.1128/iai.62.4.1369-1380.1994 · Cited by 217 · see citing works
From self sufficiency to dependence: mechanisms and factors important for autotransporter biogenesis
Leyton, D. L., Rossiter, A. E., & Henderson, I. R. (2012) · Nature Reviews Microbiology · doi:10.1038/nrmicro2733 · Cited by 216 · see citing works
Salmonella bongori Provides Insights into the Evolution of the Salmonellae
Fookes, M. C., Schroeder, G. N., Langridge, G. C., Blondel, C. J., Mammina, C., Connor, T. R., Seth-Smith, H. M. B., Vernikos, G. S., Robinson, K. S., Sanders, M. J., et al. (2011) · PLoS Pathogens · doi:10.1371/journal.ppat.1002191 · Cited by 212 · see citing works
Pertactin β-helix folding mechanism suggests common themes for the secretion and folding of autotransporter proteins
Junker, M., Schuster, C. C., McDonnell, A. V., Sorg, K. A., Finn, M. C., Berger, B., & Clark, P. L. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0507923103 · Cited by 208 · see citing works
Sat, the Secreted Autotransporter Toxin of Uropathogenic Escherichia coli , Is a Vacuolating Cytotoxin for Bladder and Kidney Epithelial Cells
Guyer, D. M., Radulović, S., Jones, F.-E., et al. (2002) · Infection and Immunity · doi:10.1128/iai.70.8.4539-4546.2002 · Cited by 207 · see citing works
Protein-translocating outer membrane porins of Gram-negative bacteria
Yen, M., Peabody, C. R., Partovi, S. M., Zhai, Y., Tseng, Y., & Saier, M. H. (2002) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/s0005-2736(02)00359-0 · Cited by 202 · see citing works
Genomic Characterization of Enteroaggregative Escherichia coli From Children in Mali
Boisen, N., Scheutz, F., Rasko, D. A., Redman, J. C., Persson, S., Simon, J. K., Kotloff, K. L., Levine, M. M., Sow, S. O., Tamboura, B., et al. (2011) · The Journal of Infectious Diseases · doi:10.1093/infdis/jir757 · Cited by 189 · see citing works
Self-citation
SepA, the major extracellular protein of Shigella flexneri: autonomous secretion and involvement in tissue invasion
Benjelloun‐Touimi, Z., Sansonetti, P. J., & Parsot, C. (1995) · Molecular Microbiology · doi:10.1111/j.1365-2958.1995.mmi_17010123.x · Cited by 189 · see citing works
Complete Genome Sequence and Comparative Metabolic Profiling of the Prototypical Enteroaggregative Escherichia coli Strain 042
Chaudhuri, R. R., Sebaihia, M., Hobman, J. L., Webber, M. A., Leyton, D. L., Goldberg, M. D., Cunningham, A. F., Scott-Tucker, A., Ferguson, P., Thomas, C. M., et al. (2010) · PLoS ONE · doi:10.1371/journal.pone.0008801 · Cited by 187 · see citing works
Self-citation
Interaction of an autotransporter passenger domain with BamA during its translocation across the bacterial outer membrane
Ieva, R., & Bernstein, H. D. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0907912106 · Cited by 186 · see citing works
Genomic analysis of secretion systems
Pallen, M. J., Chaudhuri, R. R., & Henderson, I. R. (2003) · Current Opinion in Microbiology · doi:10.1016/j.mib.2003.09.005 · Cited by 184 · see citing works
Functional Comparison of Serine Protease Autotransporters of Enterobacteriaceae
Dutta, P. R., Cappello, R. E., Navarro‐García, F., & Nataro, J. P. (2002) · Infection and Immunity · doi:10.1128/iai.70.12.7105-7113.2002 · Cited by 182 · see citing works
Self-citation
Crystal Structure of Hemoglobin Protease, a Heme Binding Autotransporter Protein from Pathogenic Escherichia coli
Otto, B. R., Sijbrandi, R., Luirink, J., Oudega, B., Heddle, J. G., Mizutani, K., Park, S., & Tame, J. R. H. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m412885200 · Cited by 180 · see citing works
PSGL‐1 function in immunity and steady state homeostasis
Carlow, D. A., Gossens, K., Naus, S., Veerman, K. M., Seo, W., & Ziltener, H. J. (2009) · Immunological Reviews · doi:10.1111/j.1600-065x.2009.00797.x · Cited by 180 · see citing works
Protein secretion through autotransporter and two-partner pathways
Jacob‐Dubuisson, F., Fernandez, R. C., & Coutte, L. (2004) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2004.03.008 · Cited by 177 · see citing works
Identification and Characterization of a Novel Genomic Island Integrated at selC in Locus of Enterocyte Effacement-Negative, Shiga Toxin-Producing Escherichia coli
Schmidt, H., Zhang, W.-L., Hemmrich, U., et al. (2001) · Infection and Immunity · doi:10.1128/iai.69.11.6863-6873.2001 · Cited by 162 · see citing works
Crystal Structure of a Full-Length Autotransporter
van den Berg, B. (2010) · Journal of Molecular Biology · doi:10.1016/j.jmb.2009.12.061 · Cited by 161 · see citing works
Crystal structure of the Helicobacter pylori vacuolating toxin p55 domain
Gangwer, K. A., Mushrush, D. J., Stauff, D. L., et al. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0707447104 · Cited by 161 · see citing works
The Pic Protease of Enteroaggregative Escherichia coli Promotes Intestinal Colonization and Growth in the Presence of Mucin
Harrington, S. M., Sheikh, J., Henderson, I. R., Ruiz-Perez, F., Cohen, P. S., & Nataro, J. P. (2009) · Infection and Immunity · doi:10.1128/iai.01494-08 · Cited by 156 · see citing works
Self-citation
Use of a novel approach, termed island probing, identifies the Shigella flexneri she pathogenicity island which encodes a homolog of the immunoglobulin A protease-like family of proteins
Rajakumar, K., Sasakawa, C., & Adler, B. (1997) · Infection and Immunity · doi:10.1128/iai.65.11.4606-4614.1997 · Cited by 154 · see citing works
A conserved region within the Bordetella pertussis autotransporter BrkA is necessary for folding of its passenger domain
Oliver, D. C., Huang, G. H., Nodel, E., Pleasance, S., & Fernandez, R. C. (2003) · Molecular Microbiology · doi:10.1046/j.1365-2958.2003.03377.x · Cited by 149 · see citing works
Sequential and spatially restricted interactions of assembly factors with an autotransporter β domain
Ieva, R., Tian, P., Peterson, J. H., et al. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1103827108 · Cited by 145 · see citing works
espC Pathogenicity Island of Enteropathogenic Escherichia coli Encodes an Enterotoxin
Mellies, J. L., Navarro‐García, F., Okeke, I. N., et al. (2001) · Infection and Immunity · doi:10.1128/iai.69.1.315-324.2001 · Cited by 143 · see citing works
Characterization of a Hemoglobin Protease Secreted by the Pathogenic Escherichia coli Strain EB1
Otto, B. R., van Dooren, S. J. M., Nuijens, J. H., Luirink, J., & Oudega, B. (1998) · The Journal of Experimental Medicine · doi:10.1084/jem.188.6.1091 · Cited by 139 · see citing works
An unusual signal peptide facilitates late steps in the biogenesis of a bacterial autotransporter
Szabady, R. L., Peterson, J. H., Skillman, K. M., & Bernstein, H. D. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0406055102 · Cited by 137 · see citing works
A Novel Pathogenicity Island Integrated Adjacent to the thrW tRNA Gene of Avian Pathogenic Escherichia coli Encodes a Vacuolating Autotransporter Toxin
Parreira, V. R., & Gyles, C. L. (2003) · Infection and Immunity · doi:10.1128/iai.71.9.5087-5096.2003 · Cited by 136 · see citing works
The Bam (Omp85) complex is involved in secretion of the autotransporter haemoglobin protease
Saurı́, A., Soprova, Z., Wickström, D., Gier, J. D., van der Schors, R. C., Smit, A. B., Jong, W. S. P., & Luirink, J. (2009) · Microbiology · doi:10.1099/mic.0.034991-0 · Cited by 135 · see citing works
Vectorial transport and folding of an autotransporter virulence protein during outer membrane secretion
Junker, M., Besingi, R. N., & Clark, P. L. (2009) · Molecular Microbiology · doi:10.1111/j.1365-2958.2009.06607.x · Cited by 135 · see citing works
High Prevalence of Serine Protease Autotransporter Cytotoxins among Strains of Enteroaggregative Escherichia coli
Boisen, N., Ruı́z-Pérez, F., Scheutz, F., et al. (2009) · American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.2009.80.294 · Cited by 133 · see citing works
Signal Recognition Particle (SRP)-mediated Targeting and Sec-dependent Translocation of an Extracellular Escherichia coli Protein*
Sijbrandi, R., Urbanus, M., ten Hagen-Jongman, C. T., Bernstein, H., Oudega, B., Otto, B., & Luirink, J. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m211630200 · Cited by 130 · see citing works
Autotransporter-Encoding Sequences Are Phylogenetically Distributed amongEscherichia coliClinical Isolates and Reference Strains
Restieri, C., Garriss, G., Locas, M., & Dozois, C. M. (2007) · Applied and Environmental Microbiology · doi:10.1128/aem.01542-06 · Cited by 130 · see citing works
Roles of Periplasmic Chaperone Proteins in the Biogenesis of Serine Protease Autotransporters of Enterobacteriaceae
Ruı́z-Pérez, F., Henderson, I. R., Leyton, D. L., Rossiter, A. E., Zhang, Y., & Nataro, J. P. (2009) · Journal of Bacteriology · doi:10.1128/jb.00754-09 · Cited by 129 · see citing works
Self-citation
The sigA Gene Which Is Borne on the she Pathogenicity Island of Shigella flexneri 2a Encodes an Exported Cytopathic Protease Involved in Intestinal Fluid Accumulation
Al‐Hasani, K., Henderson, I. R., Sakellaris, H., et al. (2000) · Infection and Immunity · doi:10.1128/iai.68.5.2457-2463.2000 · Cited by 127 · see citing works
IcsA Surface Presentation in Shigella flexneri Requires the Periplasmic Chaperones DegP, Skp, and SurA
Purdy, G. E., Fisher, C. R., & Payne, S. M. (2007) · Journal of Bacteriology · doi:10.1128/jb.00483-07 · Cited by 123 · see citing works
Cleavage of a bacterial autotransporter by an evolutionarily convergent autocatalytic mechanism
Dautin, N., Barnard, T. J., Anderson, D. E., & Bernstein, H. D. (2007) · The EMBO Journal · doi:10.1038/sj.emboj.7601638 · Cited by 122 · see citing works
Identification and Molecular Characterization of EatA, an Autotransporter Protein of Enterotoxigenic Escherichia coli
Patel, S. K., Dotson, J., Allen, K. P., et al. (2004) · Infection and Immunity · doi:10.1128/iai.72.3.1786-1794.2004 · Cited by 121 · see citing works
Cytoskeletal Effects Induced by Pet, the Serine Protease Enterotoxin of Enteroaggregative Escherichia coli
Navarro‐García, F., Sears, C. L., Eslava, C. A., et al. (1999) · Infection and Immunity · doi:10.1128/iai.67.5.2184-2192.1999 · Cited by 121 · see citing works
Requirement for YaeT in the Outer Membrane Assembly of Autotransporter Proteins
Jain, S., & Goldberg, M. B. (2007) · Journal of Bacteriology · doi:10.1128/jb.00228-07 · Cited by 115 · see citing works
Serine Protease Autotransporters of Enterobacteriaceae (SPATEs): Biogenesis and Function
Dautin, N. (2010) · Toxins · doi:10.3390/toxins2061179 · Cited by 113 · see citing works
Autotransporter Genes pic and tsh Are Associated with Escherichia coli Strains That Cause Acute Pyelonephritis and Are Expressed during Urinary Tract Infection
Heimer, S. R., Rasko, D. A., Lockatell, C. V., Johnson, D. E., & Mobley, H. L. T. (2003) · Infection and Immunity · doi:10.1128/iai.72.1.593-597.2004 · Cited by 110 · see citing works
Self-associating autotransporters, SAATs: functional and structural similarities
Klemm, P., Vejborg, R. M., & Sherlock, O. (2006) · International Journal of Medical Microbiology · doi:10.1016/j.ijmm.2005.10.002 · Cited by 109 · see citing works
Identification of Enterohemorrhagic Escherichia coli O26:H − Genes Required for Intestinal Colonization in Calves
van Diemen, P. M., Dziva, F., Stevens, M. P., et al. (2005) · Infection and Immunity · doi:10.1128/iai.73.3.1735-1743.2005 · Cited by 109 · see citing works
Serine protease autotransporters from Shigella flexneri and pathogenic Escherichia coli target a broad range of leukocyte glycoproteins
Ruı́z-Pérez, F., Wahid, R., Faherty, C. S., Kolappaswamy, K., Rodriguez, L., Santiago, A. E., Murphy, E., Cross, A. S., Sztein, M. B., & Nataro, J. P. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1101006108 · Cited by 107 · see citing works
Self-citation
Pic, an Autotransporter Protein Secreted by Different Pathogens in theEnterobacteriaceaeFamily, Is a Potent Mucus Secretagogue
Navarro‐García, F., Gutiérrez-Jiménez, J., García-Tovar, C. G., Castro‐Sánchez, L., Salazar-González, H., & Cordova, V. (2010) · Infection and Immunity · doi:10.1128/iai.00523-10 · Cited by 104 · see citing works
Secretion of a bacterial virulence factor is driven by the folding of a C-terminal segment
Peterson, J. H., Tian, P., Ieva, R., Dautin, N., & Bernstein, H. D. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1009491107 · Cited by 101 · see citing works
Involvement of the Enteroaggregative Escherichia coli Plasmid-Encoded Toxin in Causing Human Intestinal Damage
Henderson, I. R., Hicks, S., Navarro‐García, F., et al. (1999) · Infection and Immunity · doi:10.1128/iai.67.10.5338-5344.1999 · Cited by 100 · see citing works
Characterization of the Neisseria Igaβ-core
Klauser, T., Krämer, J., Otzelberger, K., Pohlner, J., & Meyer, T. F. (1993) · Journal of Molecular Biology · doi:10.1006/jmbi.1993.1613 · Cited by 99 · see citing works
The Pseudomonas aeruginosa patatin‐like protein PlpD is the archetype of a novel Type V secretion system
Salacha, R., Kovačić, F., Brochier‐Armanet, C., et al. (2010) · Environmental Microbiology · doi:10.1111/j.1462-2920.2010.02174.x · Cited by 97 · see citing works
The secreted autotransporter toxin, Sat, functions as a virulence factor in Afa/Dr diffusely adhering Escherichia coli by promoting lesions in tight junction of polarized epithelial cells
Guignot, J., Chaplais, C., Coconnier, M. H., & Servin, A. L. (2006) · Cellular Microbiology · doi:10.1111/j.1462-5822.2006.00782.x · Cited by 97 · see citing works
PicU, a second serine protease autotransporter of uropathogenic Escherichia coli
Parham, N. J., Srinivasan, U., Desvaux, M., Foxman, B., Marrs, C. F., & Henderson, I. R. (2003) · FEMS Microbiology Letters · doi:10.1016/s0378-1097(03)00862-0 · Cited by 97 · see citing works
Characterization of an exported protease from Shiga toxin‐producing Escherichia coli
Djafari, S., Ebel, F., Deibel, C., et al. (1997) · Molecular Microbiology · doi:10.1046/j.1365-2958.1997.5141874.x · Cited by 95 · see citing works
Characterization of the Avian PathogenicEscherichia coliHemagglutinin Tsh, a Member of the Immunoglobulin A Protease-Type Family of Autotransporters
Stathopoulos, C., Provence, D. L., & Curtiss, R. (1999) · Infection and Immunity · doi:10.1128/iai.67.2.772-781.1999 · Cited by 91 · see citing works
Genetic organization of the she pathogenicity island in Shigella flexneri 2a
Al‐Hasani, K., Rajakumar, K., Bulach, D., et al. (2001) · Microbial Pathogenesis · doi:10.1006/mpat.2000.0404 · Cited by 86 · see citing works
A Bioinformatic Strategy for the Detection, Classification and Analysis of Bacterial Autotransporters
Celik, N., Webb, C. T., Leyton, D. L., Holt, K. E., Heinz, E., Gorrell, R. J., Kwok, T., Naderer, T., Strugnell, R. A., Speed, T. P., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0043245 · Cited by 86 · see citing works
Transfer Region of pO113 from Enterohemorrhagic Escherichia coli : Similarity with R64 and Identification of a Novel Plasmid-Encoded Autotransporter, EpeA
Leyton, D. L., Sloan, J., Hill, R., Doughty, S., & Hartland, E. L. (2003) · Infection and Immunity · doi:10.1128/iai.71.11.6307-6319.2003 · Cited by 86 · see citing works
CD45 ligation induces programmed cell death in T and B lymphocytes
Klaus, S. J., Sidorenko, S. P., & Clark, E. A. (1996) · The Journal of Immunology · doi:10.4049/jimmunol.156.8.2743 · Cited by 84 · see citing works
EspP, a Type V-secreted serine protease of enterohaemorrhagicEscherichia coliO157:H7, influences intestinal colonization of calves and adherence to bovine primary intestinal epithelial cells
Dziva, F., Mahajan, A., Cameron, P., Currie, C., McKendrick, I. J., Wallis, T. S., Smith, D. G., & Stevens, M. P. (2007) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.2007.00724.x · Cited by 83 · see citing works
Shigella are versatile mucosal pathogens that circumvent the host innate immune system
Ashida, H., Ogawa, M., Mimuro, H., Kobayashi, T., Sanada, T., & Sasakawa, C. (2011) · Current Opinion in Immunology · doi:10.1016/j.coi.2011.06.001 · Cited by 83 · see citing works
The Essential β-Barrel Assembly Machinery Complex Components BamD and BamA Are Required for Autotransporter Biogenesis
Rossiter, A. E., Leyton, D. L., Tveen‐Jensen, K., et al. (2011) · Journal of Bacteriology · doi:10.1128/jb.00192-11 · Cited by 81 · see citing works
EspP, a Serine Protease of EnterohemorrhagicEscherichia coli, Impairs Complement Activation by Cleaving Complement Factors C3/C3b and C5
Orth‐Höller, D., Ehrlenbach, S., Brockmeyer, J., Khan, A. B., Huber, G. C., Karch, H., Sarg, B., Lindner, H. H., & Würzner, R. (2010) · Infection and Immunity · doi:10.1128/iai.00488-10 · Cited by 81 · see citing works
Four Different Genes Responsible for Nonimmune Immunoglobulin-Binding Activities within a Single Strain of Escherichia coli
Sandt, C. H., & Hill, C. W. L. (2000) · Infection and Immunity · doi:10.1128/iai.68.4.2205-2214.2000 · Cited by 80 · see citing works
CD43, a molecule with multiple functions
Rosenstein, Y., Santana, A., & Pedraza‐Alva, G. (1999) · Immunologic Research · doi:10.1007/bf02786465 · Cited by 79 · see citing works
Pet Toxin from Enteroaggregative Escherichia coli Produces Cellular Damage Associated with Fodrin Disruption
Villaseca, J. M., Navarro‐García, F., Mendoza‐Hernández, G., et al. (2000) · Infection and Immunity · doi:10.1128/iai.68.10.5920-5927.2000 · Cited by 79 · see citing works
Genome-Wide Transposon Mutagenesis Reveals a Role for pO157 Genes in Biofilm Development in Escherichia coli O157:H7 EDL933
Puttamreddy, S., Cornick, N. A., & Minion, F. C. (2010) · Infection and Immunity · doi:10.1128/iai.00156-10 · Cited by 78 · see citing works
A Novel Intein-Like Autoproteolytic Mechanism in Autotransporter Proteins
Tajima, N., Kawai, F., Park, S., et al. (2010) · Journal of Molecular Biology · doi:10.1016/j.jmb.2010.06.068 · Cited by 77 · see citing works
Crystal structure of the Haemophilus influenzae Hap adhesin reveals an intercellular oligomerization mechanism for bacterial aggregation
Meng, G., Spahich, N., Kenjale, R., Waksman, G., & St Geme, J. W. (2011) · The EMBO Journal · doi:10.1038/emboj.2011.279 · Cited by 76 · see citing works
Phenotypic and genotypic characterization of virulence factors of Escherichia coli isolated from broiler chickens with simultaneous occurrence of cellulitis and other colibacillosis lesions.
Gomis, S. M., Riddell, C., Potter, A. A., et al. (2001) · PubMed · Cited by 75 · see citing works
Size and Conformation Limits to Secretion of Disulfide-bonded Loops in Autotransporter Proteins
Leyton, D. L., Sevastsyanovich, Y. R., Browning, D. F., Rossiter, A. E., Wells, T. J., Fitzpatrick, R. E., Overduin, M., Cunningham, A. F., & Henderson, I. R. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.306118 · Cited by 75 · see citing works
Virulence Properties of Escherichia coli 83972, a Prototype Strain Associated with Asymptomatic Bacteriuria
Hull, R. A., Rudy, D. C., Donovan, W. H., et al. (1999) · Infection and Immunity · doi:10.1128/iai.67.1.429-432.1999 · Cited by 75 · see citing works
The Serine Protease Motif of EspC from Enteropathogenic Escherichia coli Produces Epithelial Damage by a Mechanism Different from That of Pet Toxin from Enteroaggregative E. coli
Navarro‐García, F., Canizalez‐Román, A., Sui, B. Q., et al. (2004) · Infection and Immunity · doi:10.1128/iai.72.6.3609-3621.2004 · Cited by 75 · see citing works
Active-Site Gating Regulates Substrate Selectivity in a Chymotrypsin-Like Serine Protease
Johnson, T. A., Qiu, J., Plaut, A. G., & Holyoak, T. (2009) · Journal of Molecular Biology · doi:10.1016/j.jmb.2009.04.041 · Cited by 74 · see citing works
Functional Analysis of the Tsh Autotransporter from an Avian Pathogenic Escherichia coli Strain
Kostakioti, M., & Stathopoulos, C. (2004) · Infection and Immunity · doi:10.1128/iai.72.10.5548-5554.2004 · Cited by 74 · see citing works
Escherichia coli Hemoglobin Protease Autotransporter Contributes to Synergistic Abscess Formation and Heme-Dependent Growth of Bacteroides fragilis
Otto, B. R., van Dooren, S. J. M., Dozois, C. M., Luirink, J., & Oudega, B. (2002) · Infection and Immunity · doi:10.1128/iai.70.1.5-10.2002 · Cited by 74 · see citing works
Apoptosis of human hematopoietic progenitor cells induced by crosslinking of surface CD43, the major sialoglycoprotein of leukocytes
Bažil, V., Brandt, J., Tsukamoto, A. S., et al. (1995) · Blood · doi:10.1182/blood.v86.2.502.bloodjournal862502 · Cited by 69 · see citing works
Common themes and variations in serine protease autotransporters
Yen, Y. T., Kostakioti, M., Henderson, I. R., & Stathopoulos, C. (2008) · Trends in Microbiology · doi:10.1016/j.tim.2008.05.003 · Cited by 69 · see citing works
Genome of Multidrug-Resistant Uropathogenic Escherichia coli Strain NA114 from India
Avasthi, T. S., Kumar, N., Baddam, R., et al. (2011) · Journal of Bacteriology · doi:10.1128/jb.05413-11 · Cited by 68 · see citing works
Species Specificity of In Vitro Escherichia coli Adherence to Host Intestinal Cell Membranes and Its Correlation with In Vitro Colonization and Infectivity
Cheney, C. P., Schad, P. A., Formal, S. B., & Boedeker, E. C. (1980) · Infection and Immunity · doi:10.1128/iai.28.3.1019-1027.1980 · Cited by 65 · see citing works
Mucin-type O-glycans and leukosialin
Fukuda, M., & Tsuboi, S. (1999) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/s0925-4439(99)00067-8 · Cited by 65 · see citing works
Fodrin CaM‐binding domain cleavage by Pet from enteroaggregative Escherichia coli leads to actin cytoskeletal disruption
Canizalez‐Román, A., & Navarro‐García, F. (2003) · Molecular Microbiology · doi:10.1046/j.1365-2958.2003.03492.x · Cited by 64 · see citing works
Intimin and Invasin Export Their C-Terminus to the Bacterial Cell Surface Using an Inverse Mechanism Compared to Classical Autotransport
Oberhettinger, P., Schütz, M. S., Leo, J. C., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0047069 · Cited by 63 · see citing works
SepA, the 110 kDa protein secreted by Shigella flexneri: two-domain structure and proteolytic activity
Benjelloun‐Touimi, Z., Si‐Tahar, M., Montecucco, C., et al. (1998) · Microbiology · doi:10.1099/00221287-144-7-1815 · Cited by 62 · see citing works
Protease Activity, Secretion, Cell Entry, Cytotoxicity, and Cellular Targets of Secreted Autotransporter Toxin of Uropathogenic Escherichia coli
Maroncle, N., Sivick, K. E., Brady, R. A., Stokes, F.-E., & Mobley, H. L. T. (2006) · Infection and Immunity · doi:10.1128/iai.01086-06 · Cited by 62 · see citing works
Distribution of the Serine Protease Autotransporters of the Enterobacteriaceae among Extraintestinal Clinical Isolates of Escherichia coli
Parham, N. J., Pollard, S. J., Desvaux, M., et al. (2005) · Journal of Clinical Microbiology · doi:10.1128/jcm.43.8.4076-4082.2005 · Cited by 62 · see citing works
Subtypes of the Plasmid-Encoded Serine Protease EspP in Shiga Toxin-Producing Escherichia coli : Distribution, Secretion, and Proteolytic Activity
Brockmeyer, J., Bielaszewska, M., Fruth, A., Bonn, M. L., Mellmann, A., Humpf, H., & Karch, H. (2007) · Applied and Environmental Microbiology · doi:10.1128/aem.00920-07 · Cited by 60 · see citing works
Are bacterial ‘autotransporters’ really transporters?
Bernstein, H. D. (2007) · Trends in Microbiology · doi:10.1016/j.tim.2007.09.007 · Cited by 59 · see citing works
RegA, an AraC-Like Protein, Is a Global Transcriptional Regulator That Controls Virulence Gene Expression in Citrobacter rodentium
Hart, E. J., Yang, J. W., Tauschek, M., Kelly, M., Wakefield, M. J., Frankel, G. M., Hartland, E. L., & Robins-Browne, R. M. (2008) · Infection and Immunity · doi:10.1128/iai.00770-08 · Cited by 59 · see citing works
EspC translocation into epithelial cells by enteropathogenicEscherichia colirequires a concerted participation of type V and III secretion systems
Vidal, J. E., & Navarro‐García, F. (2008) · Cellular Microbiology · doi:10.1111/j.1462-5822.2008.01181.x · Cited by 57 · see citing works
Bacterial Macroscopic Rope-like Fibers with Cytopathic and Adhesive Properties*
Xicohtencatl-Cortes, J., Saldaña, Z., Deng, W., Castañeda, E., Freer, E., Tarr, P., Finlay, B., Puente, J. L., & Girón, J. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.162248 · Cited by 56 · see citing works
The Immunogenic SigA Enterotoxin of Shigella flexneri 2a Binds to HEp-2 Cells and Induces Fodrin Redistribution in Intoxicated Epithelial Cells
Al‐Hasani, K., Navarro‐García, F., Huerta, J., et al. (2009) · PLoS ONE · doi:10.1371/journal.pone.0008223 · Cited by 56 · see citing works
The serine protease motif of Pic mediates a dose-dependent mucolytic activity after binding to sugar constituents of the mucin substrate
Gutiérrez-Jiménez, J., Arciniega-Martínez, I. M., & Navarro‐García, F. (2008) · Microbial Pathogenesis · doi:10.1016/j.micpath.2008.04.006 · Cited by 55 · see citing works
Complete Genome Sequence of the Wild-Type Commensal Escherichia coli Strain SE15, Belonging to Phylogenetic Group B2
Toh, H., Oshima, K., Toyoda, A., Ogura, Y., Ooka, T., Sasamoto, H., Park, S.-H., Iyoda, S., Kurokawa, K., Morita, H., et al. (2009) · Journal of Bacteriology · doi:10.1128/jb.01543-09 · Cited by 53 · see citing works
Interaction of FkpA, a peptidyl-prolylcis/transisomerase with EspP autotransporter protein
Ruı́z-Pérez, F., Henderson, I. R., & Nataro, J. P. (2010) · Gut Microbes · doi:10.4161/gmic.1.5.13436 · Cited by 53 · see citing works
Self-citation
Evolution of an Autotransporter: Domain Shuffling and Lateral Transfer from Pathogenic Haemophilus to Neisseria
Davis, J., Smith, A. L., Hughes, W. R., et al. (2001) · Journal of Bacteriology · doi:10.1128/jb.183.15.000-000.2001 · Cited by 51 · see citing works
CD44 ligation induces caspase-independent cell death via a novel calpain/AIF pathway in human erythroleukemia cells
Artus, C., Maquarre, E., Moubarak, R. S., Delettre, C., Jasmin, C., Susín, S. A., & Robert-Lézénès, J. (2006) · Oncogene · doi:10.1038/sj.onc.1209581 · Cited by 50 · see citing works
Complete Genome Sequence of the Crohn's Disease-Associated Adherent-Invasive Escherichia coliStrain HM605
Clarke, D. J., Chaudhuri, R. R., Martin, H., et al. (2011) · Journal of Bacteriology · doi:10.1128/jb.05374-11 · Cited by 50 · see citing works
Renaming protein secretion in the Gram-negative bacteria
Henderson, I. R., Nataro, J. P., Kaper, J. B., Meyer, T. F., Farrand, S. K., Burns, D., Finlay, B. B., & Geme, J. W. S. (2000) · Trends in Microbiology · doi:10.1016/s0966-842x(00)01814-x · Cited by 48 · see citing works
Self-citation
ATP-Independent Control of Autotransporter Virulence Protein Transport via the Folding Properties of the Secreted Protein
Renn, J. P., Junker, M., Besingi, R. N., Braselmann, E., & Clark, P. L. (2011) · Chemistry & Biology · doi:10.1016/j.chembiol.2011.11.009 · Cited by 48 · see citing works
Molecular Basis for the Activation of a Catalytic Asparagine Residue in a Self-Cleaving Bacterial Autotransporter
Barnard, T. J., Gumbart, J. C., Peterson, J. H., et al. (2011) · Journal of Molecular Biology · doi:10.1016/j.jmb.2011.10.049 · Cited by 48 · see citing works
Crystal Structure of the Passenger Domain of the Escherichia coli Autotransporter EspP
Khan, S., Mian, H. S., Sandercock, L. E., et al. (2011) · Journal of Molecular Biology · doi:10.1016/j.jmb.2011.09.028 · Cited by 47 · see citing works
Adhesin Degradation Accelerates Delivery of Heat-labile Toxin by Enterotoxigenic Escherichia coli
Roy, K., Kansal, R. G., Bartels, S. R., et al. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.251546 · Cited by 44 · see citing works
Secreted autotransporter toxin (Sat) triggers autophagy in epithelial cells that relies on cell detachment
Moal, V. L.-L., Comenge, Y., Ruby, V., Amsellem, R., Nicolas, V., & Servin, A. L. (2011) · Cellular Microbiology · doi:10.1111/j.1462-5822.2011.01595.x · Cited by 40 · see citing works
Prevalence of the sat, set and sen genes among diverse serotypes of Shigella flexneri strains isolated from patients with acute diarrhoea
Niyogi, S. K., Vargas, M., & Vilà, J. (2004) · Clinical Microbiology and Infection · doi:10.1111/j.1469-0691.2004.00897.x · Cited by 40 · see citing works
Characterisation of Early Mucosal and Neuronal Lesions Following Shigella flexneri Infection in Human Colon
Coron, E., Flamant, M., Aubert, P., Wedel, T., Pédron, T., Letessier, E., Galmiche, J. P., Sansonetti, P. J., & Neunlist, M. (2009) · PLoS ONE · doi:10.1371/journal.pone.0004713 · Cited by 39 · see citing works
Structure-Function Analysis of the Enteroaggregative Escherichia coli Plasmid-encoded Toxin Autotransporter Using Scanning Linker Mutagenesis
Dutta, P. R., Sui, B. Q., & Nataro, J. P. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m303595200 · Cited by 37 · see citing works
Self-citation
Secreted autotransporter toxin produced by a diffusely adheringEscherichia colistrain causes intestinal damage in animal model assays
Taddei, C. R., Fasano, A., Ferreira, A. J. P., et al. (2005) · FEMS Microbiology Letters · doi:10.1016/j.femsle.2005.07.013 · Cited by 37 · see citing works
EspC, an autotransporter protein secreted by enteropathogenic Escherichia coli (EPEC), displays protease activity on human hemoglobin
Drago-Serrano, M. E., Parra, S. G., & Manjarrez-HernÃ¡ndez, H. A. (2006) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.2006.00463.x · Cited by 35 · see citing works
Pet, a Non-AB Toxin, Is Transported and Translocated into Epithelial Cells by a Retrograde Trafficking Pathway
Navarro‐García, F., Canizalez‐Román, A., Burlingame, K. E., et al. (2007) · Infection and Immunity · doi:10.1128/iai.01515-06 · Cited by 35 · see citing works
YidC Is Involved in the Biogenesis of the Secreted Autotransporter Hemoglobin Protease
Jong, W. S. P., ten Hagen‐Jongman, C. M., Ruijter, E., Orrù, R. V. A., Genevaux, P., & Luirink, J. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.167650 · Cited by 31 · see citing works
Efficient Translocation of EspC into Epithelial Cells Depends on Enteropathogenic Escherichia coli and Host Cell Contact
Vidal, J. E., & Navarro‐García, F. (2006) · Infection and Immunity · doi:10.1128/iai.74.4.2293-2303.2006 · Cited by 31 · see citing works
VirK Is a Periplasmic Protein Required for Efficient Secretion of Plasmid-Encoded Toxin from Enteroaggregative Escherichia coli
Tapia-Pastrana, G., Chávez‐Dueñas, L., Lanz‐Mendoza, H., et al. (2012) · Infection and Immunity · doi:10.1128/iai.00167-12 · Cited by 31 · see citing works
Intoxication of epithelial cells by plasmid-encoded toxin requires clathrin-mediated endocytosis
Navarro‐García, F., Canizalez‐Román, A., Vidal, J. E., et al. (2007) · Microbiology · doi:10.1099/mic.0.2007/007088-0 · Cited by 30 · see citing works
Host-Toxin Interactions Involving EspC and Pet, Two Serine Protease Autotransporters of the Enterobacteriaceae
Navarro‐García, F., Sonnested, M., & Teter, K. (2010) · Toxins · doi:10.3390/toxins2051134 · Cited by 28 · see citing works
Autotransporter proteins, evolution and redefining protein secretion: Response
Henderson, I. R., Cappello, R. E., & Nataro, J. P. (2000) · Trends in Microbiology · doi:10.1016/s0966-842x(00)01884-9 · Cited by 26 · see citing works
Self-citation
Cross-linking of P-selectin glycoprotein ligand-1 induces death of activated T cells
Chen, S.-C., Huang, C.-C., Chien, C. L., Jeng, C., Su, H.-T., Chiang, E. F.-L., Liu, M.-R., Wu, C.-K., Chang, C.-N., & Lin, R. (2004) · Blood · doi:10.1182/blood-2003-05-1679 · Cited by 25 · see citing works
Genome Sequence of a Porcine Extraintestinal Pathogenic Escherichia coli Strain
Tan, C., Xu, Z., Zheng, H., et al. (2011) · Journal of Bacteriology · doi:10.1128/jb.05551-11 · Cited by 25 · see citing works
Serine protease espP subtype α, but not β or γ, of Shiga toxin-producing Escherichia coli is associated with highly pathogenic serogroups
Khan, A. B., Naim, A., Orth‐Höller, D., et al. (2008) · International Journal of Medical Microbiology · doi:10.1016/j.ijmm.2008.08.006 · Cited by 23 · see citing works
Prevalence, Biogenesis, and Functionality of the Serine Protease Autotransporter EspP
Weiss, A., & Brockmeyer, J. (2012) · Toxins · doi:10.3390/toxins5010025 · Cited by 22 · see citing works
CD34 mediates intestinal inflammation in Salmonella-infected mice
Graßl, G. A., Faustmann, M., Gill, N., Zbytnuik, L. D., Merkens, H., So, L., Rossi, F. M. V., McNagny, K. M., & Finlay, B. B. (2010) · Cellular Microbiology · doi:10.1111/j.1462-5822.2010.01488.x · Cited by 20 · see citing works
Lack of Functional P-Selectin Ligand Exacerbates Salmonella Serovar Typhimurium Infection
Kum, W. W. S., Lee, S., Graßl, G. A., Bidshahri, R., Hsu, K., Ziltener, H. J., & Finlay, B. B. (2009) · The Journal of Immunology · doi:10.4049/jimmunol.0802536 · Cited by 17 · see citing works
Intracellular Expression of the Plasmid-Encoded Toxin from Enteroaggregative Escherichia coli
Sui, B. Q., Dutta, P. R., & Nataro, J. P. (2003) · Infection and Immunity · doi:10.1128/iai.71.9.5364-5370.2003 · Cited by 17 · see citing works
Self-citation
Contribution of a Novel Gene, rpeA , Encoding a Putative Autotransporter Adhesin to Intestinal Colonization by Rabbit-Specific Enteropathogenic Escherichia coli
Leyton, D. L., Adams, L. M., Kelly, M., et al. (2007) · Infection and Immunity · doi:10.1128/iai.00972-06 · Cited by 16 · see citing works
Role of domains within the autotransporter Hbp/Tsh
Nishimura, K., Yoon, Y.-H., Kurihara, A., Unzai, S., Luirink, J., Park, S., & Tame, J. R. H. (2010) · Acta Crystallographica Section D Biological Crystallography · doi:10.1107/s0907444910036966 · Cited by 15 · see citing works
Outbreak of Hemolytic-Uremic Syndrome Linked to Shiga Toxin-Producing Enteroaggregative Escherichia coli O104:H4
Nataro, J. P. (2011) · Pediatric Research · doi:10.1203/pdr.0b013e31822d5ce9 · Cited by 12 · see citing works
Self-citation
Effects of the plasmid-encoded toxin of enteroaggregativeEscherichia colion focal adhesion complexes
Cappello, R. E., Estrada‐Gutiérrez, G., Irles, C., et al. (2010) · FEMS Immunology & Medical Microbiology · doi:10.1111/j.1574-695x.2010.00776.x · Cited by 9 · see citing works
Impaired innate immune response and enhanced pathology during Citrobacter rodentium infection in mice lacking functional P-selectin
Kum, W. W. S., Lo, B. C., Deng, W., Ziltener, H. J., & Finlay, B. B. (2010) · Cellular Microbiology · doi:10.1111/j.1462-5822.2010.01466.x · Cited by 9 · see citing works
A host-specific factor is necessary for efficient folding of the autotransporter plasmid-encoded toxin☆
Nemec, K. N., Scaglione, P., Navarro‐García, F., et al. (2009) · Biochimie · doi:10.1016/j.biochi.2009.11.006 · Cited by 8 · see citing works
Identification and Mechanism of Evolution of New Alleles Coding for the AIDA-I Autotransporter of Porcine Pathogenic Escherichia coli
Côté, J., Berthiaume, F., Houle, S., Fairbrother, J. M., Dozois, C. M., & Mourez, M. (2012) · Applied and Environmental Microbiology · doi:10.1128/aem.00906-12 · Cited by 4 · see citing works

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[84]Tan C Genome Sequence of a Porcine Extraintestinal Pathogenic Escherichia coli Strain Journal of Bacteriology 2011 193 18 5038 5038 21742868 PMC3165708

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Serine Proteases and Serine Protease Inhibitors
Page, M. J., & Di, E. (2008) · Wiley Encyclopedia of Chemical Biology · doi:10.1002/9780470048672.wecb534 · Cited by 7 · see citing works
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Antão, C. M., & Malcata, F. X. (2005) · Plant Physiology and Biochemistry · doi:10.1016/j.plaphy.2005.05.001 · Cited by 188 · see citing works
Chapter 1 Serine proteases: classification, catalytic mechanism, types, and industrial applications
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Blay, V., & Pei, D. (2019) · ChemTexts · doi:10.1007/s40828-019-0093-4 · Cited by 17 · see citing works

Authors: Ruiz-Perez, F., & Nataro, J. P.
Affiliations: University of Virginia (US)
Venue: Cellular and Molecular Life Sciences
Publisher: Springer Science and Business Media LLC
Published: 2013-05-21
Volume: 71
Issue: 5
Pages: 745-770
ISSN: 1420-682X (ISSN-L)
1420-9071
DOI: 10.1007/s00018-013-1355-8
PMC: PMC3871983
OpenAlex: W2055798634
Cited by: 149
References: 167
Citations by year: 2026: 5 · 2025: 8 · 2024: 11 · 2023: 11 · 2022: 8 · 2021: 16 · 2020: 12 · 2019: 13 · 2018: 11 · 2017: 10 · 2016: 16 · 2015: 11 · 2014: 12 · 2013: 5
FWCI: 1.85
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
Locations: Cellular and Molecular Life Sciences (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: National Institute of Allergy and Infectious Diseases (AI033096, U19AI090873, R01AI033096)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Endocrinology › Escherichia coli research studies
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Biochemical and Structural Characterization
Keywords: serine protease, autotransporters, SPATE, Gram-negative bacteria, bacterial virulence, substrate specificity, protein secretion, host-pathogen interaction, cytoskeleton, autophagy, innate immunity, adaptive immunity, Neisseria, Shigella, Escherichia coli, Citrobacter rodentium, Salmonella, Edwardsiella
MeSH terms: Amino Acid Sequence, Enterobacteriaceae, Models, Molecular, Molecular Sequence Data, Phylogeny, Protein Conformation, Species Specificity, Substrate Specificity, Genetic Variation, Virulence, Sequence Alignment, Evolution, Molecular, Serine Proteases, Immune Evasion, Bacterial Secretion Systems

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Bacterial serine proteases secreted by the autotransporter pathway: classification, specificity, and role in virulence

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