Characterization of Saa, a Novel Autoagglutinating Adhesin Produced by Locus of Enterocyte Effacement-Negative Shiga-Toxigenic Escherichia coli Strains That Are Virulent for Humans

doi:10.1128/IAI.69.11.6999-7009.2001

This Article

	Full Text
	Full Text (PDF)
	Alert me when this article is cited
	Alert me if a correction is posted

Services

	Similar articles in this journal
	Similar articles in PubMed
	Alert me to new issues of the journal
	Download to citation manager
	Reprints and Permissions
	Copyright Information
	Books from ASM Press
	MicrobeWorld

Citing Articles

	Citing Articles via HighWire
	Citing Articles via Google Scholar

Google Scholar

	Articles by Paton, A. W.
	Articles by Paton, J. C.
	Search for Related Content

PubMed

	PubMed Citation
	Articles by Paton, A. W.
	Articles by Paton, J. C.

Previous Article | Next Article

Infection and Immunity, November 2001, p. 6999-7009, Vol. 69, No. 11
0019-9567/01/$04.00+0 DOI: 10.1128/IAI.69.11.6999-7009.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.

Characterization of Saa, a Novel Autoagglutinating Adhesin Produced by Locus of Enterocyte Effacement-Negative Shiga-Toxigenic Escherichia coli Strains That Are Virulent for Humans

Adrienne W. Paton, Potjanee Srimanote, Matthew C. Woodrow, and James C. Paton^*

Department of Molecular Biosciences, Adelaide University, Adelaide, South Australia 5005, Australia

Received 8 May 2001/Returned for modification 19 July 2001/Accepted 17 August 2001

The capacity of Shiga toxigenic Escherichia coli (STEC) to adhere to the intestinal mucosa undoubtedly contributes to pathogenesisof human disease. The majority of STEC strains isolated from severecases produce attaching and effacing lesions on the intestinalmucosa, a property mediated by the locus of enterocyte effacement(LEE) pathogenicity island. This element is not essential forpathogenesis, as some cases of severe disease, including hemolyticuremic syndrome (HUS), are caused by LEE-negative STEC strains,but the mechanism whereby these adhere to the intestinal mucosais not understood. We have isolated a gene from the megaplasmidof a LEE-negative O113:H21 STEC strain (98NK2) responsible foran outbreak of HUS, which encodes an auto-agglutinating adhesindesignated Saa (STEC autoagglutinating adhesin). Introductionof saa cloned in pBC results in a 9.7-fold increase in adherenceof E. coli JM109 to HEp-2 cells and a semilocalized adherencepattern. Mutagenesis of saa in 98NK2, or curing the wild-typestrain of its megaplasmid, resulted in a significant reductionin adherence. Homologues of saa were found in several unrelatedLEE-negative STEC serotypes, including O48:H21 (strain 94CR) andO91:H21 (strain B2F1), which were also isolated from patientswith HUS. Saa exhibits a low degree of similarity (25% amino acid[aa] identity) with YadA of Yersinia enterocolitica and Eib, arecently described phage-encoded immunoglobulin binding proteinfrom E. coli. Saa produced by 98NK2 is 516 aa long and includesfour copies of a 37-aa direct repeat sequence. Interestingly,Saa produced by other STEC strains ranges in size from 460 to534 aa as a consequence of variation in the number of repeatsand/or other insertions or deletions immediately proximal to therepeatdomain.

^* Corresponding author. Mailing address: Department of Molecular Biosciences, Adelaide University, Adelaide, S.A. 5005, Australia.Phone: 61-8-83035929. Fax: 61-8-83033262. E-mail: james.paton{at}adelaide.edu.au.

This article has been cited by other articles:

Moreira, F. C., Vieira, M. A. M., Ferreira, A. J. P., Girao, D. M., Vaz, T. M. I., Rosa, A. C. P., Knobl, T., Irino, K., Freymuller, E., Gomes, T. A. T. (2008). Escherichia coli Strains of Serotype O51:H40 Comprise Typical and Atypical Enteropathogenic E. coli Strains and Are Potentially Diarrheagenic. J. Clin. Microbiol. 46: 1462-1465 [Abstract] [Full Text]
Tarr, C. L., Nelson, A. M., Beutin, L., Olsen, K. E. P., Whittam, T. S. (2008). Molecular Characterization Reveals Similar Virulence Gene Content in Unrelated Clonal Groups of Escherichia coli of Serogroup O174 (OX3). J. Bacteriol. 190: 1344-1349 [Abstract] [Full Text]
Oliveira, M. G., Feitosa Brito, J. R., Carvalho, R. R., Guth, B. E. C., Gomes, T. A. T., Vieira, M. A. M., Kato, M. A. M. F., Ramos, I. I., Vaz, T. M. I., Irino, K. (2007). Water Buffaloes (Bubalus bubalis) Identified as an Important Reservoir of Shiga Toxin-Producing Escherichia coli in Brazil. Appl. Environ. Microbiol. 73: 5945-5948 [Abstract] [Full Text]
Ishii, S., Meyer, K. P., Sadowsky, M. J. (2007). Relationship between Phylogenetic Groups, Genotypic Clusters, and Virulence Gene Profiles of Escherichia coli Strains from Diverse Human and Animal Sources. Appl. Environ. Microbiol. 73: 5703-5710 [Abstract] [Full Text]
Rendon, M. A., Saldana, Z., Erdem, A. L., Monteiro-Neto, V., Vazquez, A., Kaper, J. B., Puente, J. L., Giron, J. A. (2007). Commensal and pathogenic Escherichia coli use a common pilus adherence factor for epithelial cell colonization. Proc. Natl. Acad. Sci. USA 104: 10637-10642 [Abstract] [Full Text]
dos Santos, L. F., Goncalves, E. M., Vaz, T. M. I., Irino, K., Guth, B. E. C. (2007). Distinct Pathotypes of O113 Escherichia coli Strains Isolated from Humans and Animals in Brazil. J. Clin. Microbiol. 45: 2028-2030 [Abstract] [Full Text]
Gyles, C. L. (2007). Shiga toxin-producing Escherichia coli: An overview. J ANIM SCI 85: E45-E62 [Abstract] [Full Text]
Lu, Y., Iyoda, S., Satou, H., Satou, H., Itoh, K., Saitoh, T., Watanabe, H. (2006). A New Immunoglobulin-Binding Protein, EibG, Is Responsible for the Chain-Like Adhesion Phenotype of Locus of Enterocyte Effacement-Negative, Shiga Toxin-Producing Escherichia coli.. Infect. Immun. 74: 5747-5755 [Abstract] [Full Text]
Loukiadis, E., Kerouredan, M., Beutin, L., Oswald, E., Brugere, H. (2006). Characterization of Shiga Toxin Gene (stx)-Positive and Intimin Gene (eae)-Positive Escherichia coli Isolates from Wastewater of Slaughterhouses in France.. Appl. Environ. Microbiol. 72: 3245-3251 [Abstract] [Full Text]
Sonntag, A.-K., Bielaszewska, M., Mellmann, A., Dierksen, N., Schierack, P., Wieler, L. H., Schmidt, M. A., Karch, H. (2005). Shiga Toxin 2e-Producing Escherichia coli Isolates from Humans and Pigs Differ in Their Virulence Profiles and Interactions with Intestinal Epithelial Cells. Appl. Environ. Microbiol. 71: 8855-8863 [Abstract] [Full Text]
Talbot, U. M., Paton, J. C., Paton, A. W. (2005). Protective Immunization of Mice with an Active-Site Mutant of Subtilase Cytotoxin of Shiga Toxin-Producing Escherichia coli. Infect. Immun. 73: 4432-4436 [Abstract] [Full Text]
Paton, A. W., Paton, J. C. (2005). Multiplex PCR for Direct Detection of Shiga Toxigenic Escherichia coli Strains Producing the Novel Subtilase Cytotoxin. J. Clin. Microbiol. 43: 2944-2947 [Abstract] [Full Text]
Luck, S. N., Bennett-Wood, V., Poon, R., Robins-Browne, R. M., Hartland, E. L. (2005). Invasion of Epithelial Cells by Locus of Enterocyte Effacement-Negative Enterohemorrhagic Escherichia coli. Infect. Immun. 73: 3063-3071 [Abstract] [Full Text]
Jordan, D. M., Booher, S. L., Moon, H. W. (2005). Escherichia coli O157:H7 Does Not Require Intimin To Persist in Pigs. Infect. Immun. 73: 1865-1867 [Full Text]
Torres, A. G., Zhou, X., Kaper, J. B. (2005). Adherence of Diarrheagenic Escherichia coli Strains to Epithelial Cells. Infect. Immun. 73: 18-29 [Full Text]
Bielaszewska, M., Sinha, B., Kuczius, T., Karch, H. (2005). Cytolethal Distending Toxin from Shiga Toxin-Producing Escherichia coli O157 Causes Irreversible G2/M Arrest, Inhibition of Proliferation, and Death of Human Endothelial Cells. Infect. Immun. 73: 552-562 [Abstract] [Full Text]
Paton, A. W., Srimanote, P., Talbot, U. M., Wang, H., Paton, J. C. (2004). A New Family of Potent AB5 Cytotoxins Produced by Shiga Toxigenic Escherichia coli. J. Exp. Med. 0: jem.20040392--C12 [Abstract] [Full Text]
Toma, C., Martinez Espinosa, E., Song, T., Miliwebsky, E., Chinen, I., Iyoda, S., Iwanaga, M., Rivas, M. (2004). Distribution of Putative Adhesins in Different Seropathotypes of Shiga Toxin-Producing Escherichia coli. J. Clin. Microbiol. 42: 4937-4946 [Abstract] [Full Text]
Shima, K., Terajima, J., Sato, T., Nishimura, K., Tamura, K., Watanabe, H., Takeda, Y., Yamasaki, S. (2004). Development of a PCR-Restriction Fragment Length Polymorphism Assay for the Epidemiological Analysis of Shiga Toxin-Producing Escherichia coli. J. Clin. Microbiol. 42: 5205-5213 [Abstract] [Full Text]
Dziva, F., van Diemen, P. M., Stevens, M. P., Smith, A. J., Wallis, T. S. (2004). Identification of Escherichia coli O157 : H7 genes influencing colonization of the bovine gastrointestinal tract using signature-tagged mutagenesis. Microbiology 150: 3631-3645 [Abstract] [Full Text]
Tyler, J. S., Friedman, D. I. (2004). Characterization of a Eukaryotic-Like Tyrosine Protein Kinase Expressed by the Shiga Toxin-Encoding Bacteriophage 933W. J. Bacteriol. 186: 3472-3479 [Abstract] [Full Text]
Shen, S., Mascarenhas, M., Rahn, K., Kaper, J. B., Karmal, M. A. (2004). Evidence for a Hybrid Genomic Island in Verocytotoxin-Producing Escherichia coli CL3 (Serotype O113:H21) Containing Segments of EDL933 (Serotype O157:H7) O Islands 122 and 48. Infect. Immun. 72: 1496-1503 [Abstract] [Full Text]
Beutin, L., Krause, G., Zimmermann, S., Kaulfuss, S., Gleier, K. (2004). Characterization of Shiga Toxin-Producing Escherichia coli Strains Isolated from Human Patients in Germany over a 3-Year Period. J. Clin. Microbiol. 42: 1099-1108 [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]
Dean-Nystrom, E. A., Melton-Celsa, A. R., Pohlenz, J. F. L., Moon, H. W., O'Brien, A. D. (2003). Comparative Pathogenicity of Escherichia coli O157 and Intimin-Negative Non-O157 Shiga Toxin-Producing E. coli Strains in Neonatal Pigs. Infect. Immun. 71: 6526-6533 [Abstract] [Full Text]
Jenkins, C., Willshaw, G. A., Evans, J., Cheasty, T., Chart, H., Shaw, D. J., Dougan, G., Frankel, G., Smith, H. R. (2003). Subtyping of virulence genes in verocytotoxin-producing Escherichia coli (VTEC) other than serogroup O157 associated with disease in the United Kingdom. J Med Microbiol 52: 941-947 [Abstract] [Full Text]
Rogers, T. J., Paton, A. W., McColl, S. R., Paton, J. C. (2003). Enhanced CXC Chemokine Responses of Human Colonic Epithelial Cells to Locus of Enterocyte Effacement-Negative Shiga-Toxigenic Escherichia coli. Infect. Immun. 71: 5623-5632 [Abstract] [Full Text]
Torres, A. G., Kaper, J. B. (2003). Multiple Elements Controlling Adherence of Enterohemorrhagic Escherichia coli O157:H7 to HeLa Cells. Infect. Immun. 71: 4985-4995 [Abstract] [Full Text]
Nielsen, E. M., Andersen, M. T. (2003). Detection and Characterization of Verocytotoxin-Producing Escherichia coli by Automated 5' Nuclease PCR Assay. J. Clin. Microbiol. 41: 2884-2893 [Abstract] [Full Text]
Friedrich, A. W., Borell, J., Bielaszewska, M., Fruth, A., Tschape, H., Karch, H. (2003). Shiga Toxin 1c-Producing Escherichia coli Strains: Phenotypic and Genetic Characterization and Association with Human Disease. J. Clin. Microbiol. 41: 2448-2453 [Abstract] [Full Text]
Jenkins, C., Perry, N. T., Cheasty, T., Shaw, D. J., Frankel, G., Dougan, G., Gunn, G. J., Smith, H. R., Paton, A. W., Paton, J. C. (2003). Distribution of the saa Gene in Strains of Shiga Toxin-Producing Escherichia coli of Human and Bovine Origins. J. Clin. Microbiol. 41: 1775-1778 [Abstract] [Full Text]
Bettelheim, K. A. (2003). Non-O157 Verotoxin-Producing Escherichia coli: A Problem, Paradox, and Paradigm. Exp. Biol. Med. 228: 333-344 [Abstract] [Full Text]
Brett, K. N., Ramachandran, V., Hornitzky, M. A., Bettelheim, K. A., Walker, M. J., Djordjevic, S. P. (2003). stx1c Is the Most Common Shiga Toxin 1 Subtype among Shiga Toxin-Producing Escherichia coli Isolates from Sheep but Not among Isolates from Cattle. J. Clin. Microbiol. 41: 926-936 [Abstract] [Full Text]
Hornitzky, M. A., Vanselow, B. A., Walker, K., Bettelheim, K. A., Corney, B., Gill, P., Bailey, G., Djordjevic, S. P. (2002). Virulence Properties and Serotypes of Shiga Toxin-Producing Escherichia coli from Healthy Australian Cattle. Appl. Environ. Microbiol. 68: 6439-6445 [Abstract] [Full Text]
Doughty, S., Sloan, J., Bennett-Wood, V., Robertson, M., Robins-Browne, R. M., Hartland, E. L. (2002). Identification of a Novel Fimbrial Gene Cluster Related to Long Polar Fimbriae in Locus of Enterocyte Effacement-Negative Strains of Enterohemorrhagic Escherichia coli. Infect. Immun. 70: 6761-6769 [Abstract] [Full Text]
Stevens, M. P., van Diemen, P. M., Dziva, F., Jones, P. W., Wallis, T. S. (2002). Options for the control of enterohaemorrhagic Escherichia coli in ruminants. Microbiology 148: 3767-3778 [Full Text]
Arthur, T. M., Barkocy-Gallagher, G. A., Rivera-Betancourt, M., Koohmaraie, M. (2002). Prevalence and Characterization of Non-O157 Shiga Toxin-Producing Escherichia coli on Carcasses in Commercial Beef Cattle Processing Plants. Appl. Environ. Microbiol. 68: 4847-4852 [Abstract] [Full Text]
Srimanote, P., Paton, A. W., Paton, J. C. (2002). Characterization of a Novel Type IV Pilus Locus Encoded on the Large Plasmid of Locus of Enterocyte Effacement-Negative Shiga-Toxigenic Escherichia coli Strains That Are Virulent for Humans. Infect. Immun. 70: 3094-3100 [Abstract] [Full Text]
Paton, A. W., Paton, J. C. (2002). Direct Detection and Characterization of Shiga Toxigenic Escherichia coli by Multiplex PCR for stx1, stx2, eae, ehxA, and saa. J. Clin. Microbiol. 40: 271-274 [Abstract] [Full Text]

J. Bacteriol.	J. Virol.	Eukaryot. Cell

Microbiol. Mol. Biol. Rev.	Clin. Vaccine Immunol.	All ASM Journals