This Article
Right arrow Full Text
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Eslava, C.
Right arrow Articles by Nataro, J. P.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Eslava, C.
Right arrow Articles by Nataro, J. P.

 Previous Article  |  Next Article 

Infect Immun, July 1998, p. 3155-3163, Vol. 66, No. 7
0019-9567/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.

Pet, an Autotransporter Enterotoxin from Enteroaggregative Escherichia coli

Carlos Eslava,1,* Fernando Navarro-García,1,2 John R. Czeczulin,2 Ian R. Henderson,2 Alejandro Cravioto,1 and James P. Nataro2

Department of Public Health, Faculty of Medicine, UNAM, 04510 Mexico DF, Mexico,1 and Center for Vaccine Development, Department of Pediatrics, University of Maryland School of Medicine, Baltimore, Maryland 212012

Received 9 February 1998/Returned for modification 25 March 1998/Accepted 20 April 1998

Enteroaggregative Escherichia coli (EAEC) is an emerging cause of diarrheal illness. Clinical data suggest that diarrhea caused by EAEC is predominantly secretory in nature, but the responsible enterotoxin has not been described. Work from our laboratories has implicated a ca. 108-kDa protein as a heat-labile enterotoxin and cytotoxin, as evidenced by rises in short-circuit current and falls in tissue resistance in rat jejunal tissue mounted in an Ussing chamber. Here we report the genetic cloning, sequencing, and characterization of this high-molecular-weight heat-labile toxin. The toxin (designated the plasmid-encoded toxin [Pet]) is encoded on the 65-MDa adherence-related plasmid of EAEC strain 042. Nucleotide sequence analysis suggests that the toxin is a member of the autotransporter class of proteins, characterized by the presence of a conserved C-terminal domain which forms a beta -barrel pore in the bacterial outer membrane and through which the mature protein is transported. The Pet toxin is highly homologous to the EspP protease of enterohemorrhagic E. coli and to EspC of enteropathogenic E. coli, an as yet cryptic protein. In addition to its potential role in EAEC infection, Pet represents the first enterotoxin within the autotransporter class of secreted proteins. We hypothesize that other closely related members of this class may also produce enterotoxic effects.


* Corresponding author. Mailing address: Department of Public Health, Faculty of Medicine, UNAM, Ap. Postal 70-443, 04510 Mexico DF, Mexico. Phone: (525) 616-1162. Fax: (525) 616-1616. E-mail: eslava{at}servidor.unam.mx.


Infect Immun, July 1998, p. 3155-3163, Vol. 66, No. 7
0019-9567/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.



This article has been cited by other articles:

  • Regua-Mangia, A. H., Gomes, T. A. T., Vieira, M. A. M., Irino, K., Teixeira, L. M. (2009). Molecular typing and virulence of enteroaggregative Escherichia coli strains isolated from children with and without diarrhoea in Rio de Janeiro city, Brazil. J Med Microbiol 58: 414-422 [Abstract] [Full Text]  
  • Boisen, N., Ruiz-Perez, F., Scheutz, F., Krogfelt, K. A., Nataro, J. P. (2009). High Prevalence of Serine Protease Autotransporter Cytotoxins among Strains of Enteroaggregative Escherichia coli. Am J Trop Med Hyg 80: 294-301 [Abstract] [Full Text]  
  • Boisen, N., Struve, C., Scheutz, F., Krogfelt, K. A., Nataro, J. P. (2008). New Adhesin of Enteroaggregative Escherichia coli Related to the Afa/Dr/AAF Family. Infect. Immun. 76: 3281-3292 [Abstract] [Full Text]  
  • Imuta, N., Nishi, J., Tokuda, K., Fujiyama, R., Manago, K., Iwashita, M., Sarantuya, J., Kawano, Y. (2008). The Escherichia coli Efflux Pump TolC Promotes Aggregation of Enteroaggregative E. coli 042. Infect. Immun. 76: 1247-1256 [Abstract] [Full Text]  
  • Navarro-Garcia, F., Canizalez-Roman, A., Vidal, J. E., Salazar, Ma. I. (2007). Intoxication of epithelial cells by plasmid-encoded toxin requires clathrin-mediated endocytosis. Microbiology 153: 2828-2838 [Abstract] [Full Text]  
  • Samie, A., Obi, C. L., Dillingham, R., Pinkerton, R. C., Guerrant, R. L. (2007). Enteroaggregative Escherichia coli in Venda, South Africa: Distribution of Virulence-Related Genes by Multiplex Polymerase Chain Reaction in Stool Samples of Human Immunodeficiency Virus (HIV)-Positive and HIV-Negative Individuals and Primary School Children. Am J Trop Med Hyg 77: 142-150 [Abstract] [Full Text]  
  • Navarro-Garcia, F., Canizalez-Roman, A., Burlingame, K. E., Teter, K., Vidal, J. E. (2007). Pet, a Non-AB Toxin, Is Transported and Translocated into Epithelial Cells by a Retrograde Trafficking Pathway. Infect. Immun. 75: 2101-2109 [Abstract] [Full Text]  
  • Ashgar, S. S. A., Oldfield, N. J., Wooldridge, K. G., Jones, M. A., Irving, G. J., Turner, D. P. J., Ala'Aldeen, D. A. A. (2007). CapA, an Autotransporter Protein of Campylobacter jejuni, Mediates Association with Human Epithelial Cells and Colonization of the Chicken Gut. J. Bacteriol. 189: 1856-1865 [Abstract] [Full Text]  
  • Restieri, C., Garriss, G., Locas, M.-C., Dozois, C. M. (2007). Autotransporter-Encoding Sequences Are Phylogenetically Distributed among Escherichia coli Clinical Isolates and Reference Strains. Appl. Environ. Microbiol. 73: 1553-1562 [Abstract] [Full Text]  
  • Desvaux, M., Scott-Tucker, A., Turner, S. M., Cooper, L. M., Huber, D., Nataro, J. P., Henderson, I. R. (2007). A conserved extended signal peptide region directs posttranslational protein translocation via a novel mechanism. Microbiology 153: 59-70 [Abstract] [Full Text]  
  • Weintraub, A. (2007). Enteroaggregative Escherichia coli: epidemiology, virulence and detection. J Med Microbiol 56: 4-8 [Abstract] [Full Text]  
  • Maroncle, N. M., Sivick, K. E., Brady, R., Stokes, F.-E., Mobley, H. L. T. (2006). Protease Activity, Secretion, Cell Entry, Cytotoxicity, and Cellular Targets of Secreted Autotransporter Toxin of Uropathogenic Escherichia coli. Infect. Immun. 74: 6124-6134 [Abstract] [Full Text]  
  • Huang, D. B., Mohanty, A., DuPont, H. L., Okhuysen, P. C., Chiang, T. (2006). A review of an emerging enteric pathogen: enteroaggregative Escherichia coli.. J Med Microbiol 55: 1303-1311 [Abstract] [Full Text]  
  • Kostakioti, M., Stathopoulos, C. (2006). Role of the {alpha}-Helical Linker of the C-Terminal Translocator in the Biogenesis of the Serine Protease Subfamily of Autotransporters. Infect. Immun. 74: 4961-4969 [Abstract] [Full Text]  
  • Diemert, D. J. (2006). Prevention and Self-Treatment of Traveler's Diarrhea. Clin. Microbiol. Rev. 19: 583-594 [Abstract] [Full Text]  
  • Dudley, E. G., Abe, C., Ghigo, J.-M., Latour-Lambert, P., Hormazabal, J. C., Nataro, J. P. (2006). An IncI1 Plasmid Contributes to the Adherence of the Atypical Enteroaggregative Escherichia coli Strain C1096 to Cultured Cells and Abiotic Surfaces. Infect. Immun. 74: 2102-2114 [Abstract] [Full Text]  
  • Parham, N. J., Pollard, S. J., Desvaux, M., Scott-Tucker, A., Liu, C., Fivian, A., Henderson, I. R. (2005). Distribution of the Serine Protease Autotransporters of the Enterobacteriaceae among Extraintestinal Clinical Isolates of Escherichia coli. J. Clin. Microbiol. 43: 4076-4082 [Abstract] [Full Text]  
  • Otto, B. R., Sijbrandi, R., Luirink, J., Oudega, B., Heddle, J. G., Mizutani, K., Park, S.-Y., Tame, J. R. H. (2005). Crystal Structure of Hemoglobin Protease, a Heme Binding Autotransporter Protein from Pathogenic Escherichia coli. J. Biol. Chem. 280: 17339-17345 [Abstract] [Full Text]  
  • Henderson, I. R., Navarro-Garcia, F., Desvaux, M., Fernandez, R. C., Ala'Aldeen, D. (2004). Type V Protein Secretion Pathway: the Autotransporter Story. Microbiol. Mol. Biol. Rev. 68: 692-744 [Abstract] [Full Text]  
  • Kostakioti, M., Stathopoulos, C. (2004). Functional Analysis of the Tsh Autotransporter from an Avian Pathogenic Escherichia coli Strain. Infect. Immun. 72: 5548-5554 [Abstract] [Full Text]  
  • Kahali, S., Sarkar, B., Rajendran, K., Khanam, J., Yamasaki, S., Nandy, R. K., Bhattacharya, S. K., Ramamurthy, T. (2004). Virulence Characteristics and Molecular Epidemiology of Enteroaggregative Escherichia coli Isolates from Hospitalized Diarrheal Patients in Kolkata, India. J. Clin. Microbiol. 42: 4111-4120 [Abstract] [Full Text]  
  • Navarro-Garcia, F., Canizalez-Roman, A., Sui, B. Q., Nataro, J. P., Azamar, Y. (2004). 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. Infect. Immun. 72: 3609-3621 [Abstract] [Full Text]  
  • Zamboni, A., Fabbricotti, S. H., Fagundes-Neto, U., Scaletsky, I. C.A. (2004). Enteroaggregative Escherichia coli Virulence Factors Are Found To Be Associated with Infantile Diarrhea in Brazil. J. Clin. Microbiol. 42: 1058-1063 [Abstract] [Full Text]  
  • Schmidt, H., Hensel, M. (2004). Pathogenicity Islands in Bacterial Pathogenesis. Clin. Microbiol. Rev. 17: 14-56 [Abstract] [Full Text]  
  • Sarantuya, J., Nishi, J., Wakimoto, N., Erdene, S., Nataro, J. P., Sheikh, J., Iwashita, M., Manago, K., Tokuda, K., Yoshinaga, M., Miyata, K., Kawano, Y. (2004). Typical Enteroaggregative Escherichia coli Is the Most Prevalent Pathotype among E. coli Strains Causing Diarrhea in Mongolian Children. J. Clin. Microbiol. 42: 133-139 [Abstract] [Full Text]  
  • Nishi, J., Sheikh, J., Mizuguchi, K., Luisi, B., Burland, V., Boutin, A., Rose, D. J., Blattner, F. R., Nataro, J. P. (2003). The Export of Coat Protein from Enteroaggregative Escherichia coli by a Specific ATP-binding Cassette Transporter System. J. Biol. Chem. 278: 45680-45689 [Abstract] [Full Text]  
  • Leyton, D. L., Sloan, J., Hill, R. E., Doughty, S., Hartland, E. L. (2003). Transfer Region of pO113 from Enterohemorrhagic Escherichia coli: Similarity with R64 and Identification of a Novel Plasmid-Encoded Autotransporter, EpeA. Infect. Immun. 71: 6307-6319 [Abstract] [Full Text]  
  • Dutta, P. R., Sui, B. Q., Nataro, J. P. (2003). Structure-Function Analysis of the Enteroaggregative Escherichia coli Plasmid-encoded Toxin Autotransporter Using Scanning Linker Mutagenesis. J. Biol. Chem. 278: 39912-39920 [Abstract] [Full Text]  
  • PRESTERL, E., ZWICK, R. H., REICHMANN, S., AICHELBURG, A., WINKLER, S., KREMSNER, P. G., GRANINGER, W. (2003). FREQUENCY AND VIRULENCE PROPERTIES OF DIARRHEAGENIC ESCHERICHIA COLI IN CHILDREN WITH DIARRHEA IN GABON. Am J Trop Med Hyg 69: 406-410 [Abstract] [Full Text]  
  • Parreira, V. R., Gyles, C. L. (2003). A Novel Pathogenicity Island Integrated Adjacent to the thrW tRNA Gene of Avian Pathogenic Escherichia coli Encodes a Vacuolating Autotransporter Toxin. Infect. Immun. 71: 5087-5096 [Abstract] [Full Text]  
  • Sui, B. Q., Dutta, P. R., Nataro, J. P. (2003). Intracellular Expression of the Plasmid-Encoded Toxin from Enteroaggregative Escherichia coli. Infect. Immun. 71: 5364-5370 [Abstract] [Full Text]  
  • Cerna, J. F., Nataro, J. P., Estrada-Garcia, T. (2003). Multiplex PCR for Detection of Three Plasmid-Borne Genes of Enteroaggregative Escherichia coli Strains. J. Clin. Microbiol. 41: 2138-2140 [Abstract] [Full Text]  
  • Dutta, P. R., Cappello, R., Navarro-Garcia, F., Nataro, J. P. (2002). Functional Comparison of Serine Protease Autotransporters of Enterobacteriaceae. Infect. Immun. 70: 7105-7113 [Abstract] [Full Text]  
  • Turner, D. P. J., Wooldridge, K. G., Ala'Aldeen, D. A. A. (2002). Autotransported Serine Protease A of Neisseria meningitidis: an Immunogenic, Surface-Exposed Outer Membrane, and Secreted Protein. Infect. Immun. 70: 4447-4461 [Abstract] [Full Text]  
  • Guyer, D. M., Radulovic, S., Jones, F.-E., Mobley, H. L. T. (2002). Sat, the Secreted Autotransporter Toxin of Uropathogenic Escherichia coli, Is a Vacuolating Cytotoxin for Bladder and Kidney Epithelial Cells. Infect. Immun. 70: 4539-4546 [Abstract] [Full Text]  
  • Yatsuyanagi, J., Saito, S., Sato, H., Miyajima, Y., Amano, K.-I., Enomoto, K. (2002). Characterization of Enteropathogenic and Enteroaggregative Escherichia coli Isolated from Diarrheal Outbreaks. J. Clin. Microbiol. 40: 294-297 [Abstract] [Full Text]  
  • Okeke, I. N., Steinruck, H., Kanack, K. J., Elliott, S. J., Sundstrom, L., Kaper, J. B., Lamikanra, A. (2002). Antibiotic-Resistant Cell-Detaching Escherichia coli Strains from Nigerian Children. J. Clin. Microbiol. 40: 301-305 [Abstract] [Full Text]  
  • Fink, D. L., Cope, L. D., Hansen, E. J., Geme, J. W. St. III (2001). The Hemophilus influenzae Hap Autotransporter Is a Chymotrypsin Clan Serine Protease and Undergoes Autoproteolysis via an Intermolecular Mechanism. J. Biol. Chem. 276: 39492-39500 [Abstract] [Full Text]  
  • Henderson, I. R., Nataro, J. P. (2001). Virulence Functions of Autotransporter Proteins. Infect. Immun. 69: 1231-1243 [Full Text]  
  • Navarro-Garcia, F., Canizalez-Roman, A., Luna, J., Sears, C., Nataro, J. P. (2001). Plasmid-Encoded Toxin of Enteroaggregative Escherichia coli is Internalized by Epithelial Cells. Infect. Immun. 69: 1053-1060 [Abstract] [Full Text]  
  • Mellies, J. L., Navarro-Garcia, F., Okeke, I., Frederickson, J., Nataro, J. P., Kaper, J. B. (2001). espC Pathogenicity Island of Enteropathogenic Escherichia coli Encodes an Enterotoxin. Infect. Immun. 69: 315-324 [Abstract] [Full Text]  
  • St. Geme, J. W. III, Cutter, D. (2000). The Haemophilus influenzae Hia Adhesin Is an Autotransporter Protein That Remains Uncleaved at the C Terminus and Fully Cell Associated. J. Bacteriol. 182: 6005-6013 [Abstract] [Full Text]  
  • Villaseca, J. M., Navarro-Garcia, F., Mendoza-Hernandez, G., Nataro, J. P., Cravioto, A., Eslava, C. (2000). Pet Toxin from Enteroaggregative Escherichia coli Produces Cellular Damage Associated with Fodrin Disruption. Infect. Immun. 68: 5920-5927 [Abstract] [Full Text]  
  • Manjarrez-Hernandez, H. A., Gavilanes-Parra, S., Chavez-Berrocal, E., Navarro-Ocana, A., Cravioto, A. (2000). Antigen Detection in Enteropathogenic Escherichia coli Using Secretory Immunoglobulin A Antibodies Isolated from Human Breast Milk. Infect. Immun. 68: 5030-5036 [Abstract] [Full Text]  
  • Dozois, C. M., Dho-Moulin, M., Bree, A., Fairbrother, J. M., Desautels, C., Curtiss, R. III (2000). Relationship between the Tsh Autotransporter and Pathogenicity of Avian Escherichia coli and Localization and Analysis of the tsh Genetic Region. Infect. Immun. 68: 4145-4154 [Abstract] [Full Text]  
  • Al-Hasani, K., Henderson, I. R., Sakellaris, H., Rajakumar, K., Grant, T., Nataro, J. P., Robins-Browne, R., Adler, B. (2000). 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. Infect. Immun. 68: 2457-2463 [Abstract] [Full Text]  
  • Sandt, C. H., Hill, C. W. (2000). Four Different Genes Responsible for Nonimmune Immunoglobulin-Binding Activities within a Single Strain of Escherichia coli. Infect. Immun. 68: 2205-2214 [Abstract] [Full Text]  
  • Henderson, I. R., Czeczulin, J., Eslava, C., Noriega, F., Nataro, J. P. (1999). Characterization of Pic, a Secreted Protease of Shigella flexneri and Enteroaggregative Escherichia coli. Infect. Immun. 67: 5587-5596 [Abstract] [Full Text]  
  • Henderson, I. R., Hicks, S., Navarro-Garcia, F., Elias, W. P., Philips, A. D., Nataro, J. P. (1999). Involvement of the Enteroaggregative Escherichia coli Plasmid-Encoded Toxin in Causing Human Intestinal Damage. Infect. Immun. 67: 5338-5344 [Abstract] [Full Text]  
  • Czeczulin, J. R., Whittam, T. S., Henderson, I. R., Navarro-Garcia, F., Nataro, J. P. (1999). Phylogenetic Analysis of Enteroaggregative and Diffusely Adherent Escherichia coli. Infect. Immun. 67: 2692-2699 [Abstract] [Full Text]  
  • Navarro-Garcia, F., Sears, C., Eslava, C., Cravioto, A., Nataro, J. P. (1999). Cytoskeletal Effects Induced by Pet, the Serine Protease Enterotoxin of Enteroaggregative Escherichia coli. Infect. Immun. 67: 2184-2192 [Abstract] [Full Text]  
  • Elias, W. P. Jr., Czeczulin, J. R., Henderson, I. R., Trabulsi, L. R., Nataro, J. P. (1999). Organization of Biogenesis Genes for Aggregative Adherence Fimbria II Defines a Virulence Gene Cluster in Enteroaggregative Escherichia coli. J. Bacteriol. 181: 1779-1785 [Abstract] [Full Text]