toxB Gene on pO157 of Enterohemorrhagic Escherichiacoli O157:H7 Is Required for Full Epithelial Cell Adherence Phenotype

doi:10.1128/IAI.69.11.6660-6669.2001

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 Tatsuno, I.
	Articles by Sasakawa, C.
	Search for Related Content

PubMed

	PubMed Citation
	Articles by Tatsuno, I.
	Articles by Sasakawa, C.

Infection and Immunity, November 2001, p. 6660-6669, Vol. 69, No. 11
0019-9567/01/$04.00+0 DOI: 10.1128/IAI.69.11.6660-6669.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.

toxB Gene on pO157 of Enterohemorrhagic Escherichia coli O157:H7 Is Required for Full Epithelial Cell Adherence Phenotype

Ichiro Tatsuno,¹ Masanori Horie,¹ Hiroyuki Abe,¹ Takeyoshi Miki,² Kozo Makino,³ Hideo Shinagawa,³ Haruhiko Taguchi,⁴ Shigeru Kamiya,⁴ Tetsuya Hayashi,⁵ and Chihiro Sasakawa¹^,^*

Department of Microbiology and Immunology, Institute of Medical Science, University of Tokyo, 4-6-1 Shirokanedai, Minato-ku, Tokyo 108-8639,¹ Faculty of Pharmaceutical Science, Kyushu University 3-1-1 Maidashi, Higashi-ku, Fukuoka 812,² Department of Molecular Microbiology, Research Institute for Microbial Diseases, Osaka University, Suita, Osaka 565-0871,³ Department of Microbiology, Kyorin University School of Medicine, 6-20-2 Shinkawa, Mitaka, Tokyo 181,⁴ and Department of Microbiology, Miyazaki Medical College, 5200 Kihara, Kiyotake, Miyazaki 889-1692,⁵ Japan

Received 30 March 2001/Returned for modification 24 July 2001/Accepted 16 August 2001

Adherence of enterohemorrhagic Escherichia coli (EHEC) to the intestinal epithelium is critical for initiation of a bacterialinfection. An in vitro infection study previously indicated thatEHEC bacteria initially adhere diffusely and then proliferateto develop MC, a process that is mediated by various secretedproteins, such as EspA, EspB, EspD, Tir, and intimin, as wellas other putative adherence factors. In the present study, weinvestigated the role of a large 93-kb plasmid (pO157) in theadherence of O157:H7 (O157Sakai) and found the toxB gene to beinvolved in the full adherence phenotype. A pO157-cured strainof O157Sakai (O157Cu) developed microcolonies on Caco-2 cells;however, the number of microcolonies was lower than that of O157Sakai,as were the production and secretion levels of EspA, EspB, andTir. Introduction of a mini-pO157 plasmid (pIC37) composed ofthe toxB and ori regions restored full adherence capacity to O157Cu,including production and secretion of the proteins. In contrast,introduction of a pO157 mutant possessing toxB::Km into O157Cucould not restore the full adherence phenotype. Expression oftruncated versions of His-tagged ToxB also promoted EspB productionand/or secretion by O157Cu. These results suggest that ToxB contributesto the adherence of EHEC to epithelial cells through promotionof the production and/or secretion of type III secretedproteins.

^* Corresponding author. Mailing address: Department of Microbiology and Immunology, Institute of Medical Science, Universityof Tokyo, 4-6-1 Shirokanedai, Minato-ku, Tokyo 108-8639, Japan.Phone: 81-3-5449-5252. Fax: 81-3-5449-5405. E-mail: sasakawa{at}ims.u-tokyo.ac.jp.

This article has been cited by other articles:

Ho, T. D., Davis, B. M., Ritchie, J. M., Waldor, M. K. (2008). Type 2 Secretion Promotes Enterohemorrhagic Escherichia coli Adherence and Intestinal Colonization. Infect. Immun. 76: 1858-1865 [Abstract] [Full Text]
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]
Musken, A., Bielaszewska, M., Greune, L., Schweppe, C. H., Muthing, J., Schmidt, H., Schmidt, M. A., Karch, H., Zhang, W. (2008). Anaerobic Conditions Promote Expression of Sfp Fimbriae and Adherence of Sorbitol-Fermenting Enterohemorrhagic Escherichia coli O157:NM to Human Intestinal Epithelial Cells. Appl. Environ. Microbiol. 74: 1087-1093 [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]
Wu, G., Carter, B., Mafura, M., Liebana, E., Woodward, M. J., Anjum, M. F. (2008). Genetic Diversity among Escherichia coli O157:H7 Isolates and Identification of Genes Linked to Human Infections. Infect. Immun. 76: 845-856 [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]
Mellies, J. L., Barron, A. M. S., Carmona, A. M. (2007). Enteropathogenic and Enterohemorrhagic Escherichia coli Virulence Gene Regulation. Infect. Immun. 75: 4199-4210 [Full Text]
Lim, J. Y., Sheng, H., Seo, K. S., Park, Y. H., Hovde, C. J. (2007). Characterization of an Escherichia coli O157:H7 Plasmid O157 Deletion Mutant and Its Survival and Persistence in Cattle. Appl. Environ. Microbiol. 73: 2037-2047 [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]
Brinkley, C., Burland, V., Keller, R., Rose, D. J., Boutin, A. T., Klink, S. A., Blattner, F. R., Kaper, J. B. (2006). Nucleotide Sequence Analysis of the Enteropathogenic Escherichia coli Adherence Factor Plasmid pMAR7. Infect. Immun. 74: 5408-5413 [Abstract] [Full Text]
Sheng, H., Lim, J. Y., Knecht, H. J., Li, J., Hovde, C. J. (2006). Role of Escherichia coli O157:H7 Virulence Factors in Colonization at the Bovine Terminal Rectal Mucosa.. Infect. Immun. 74: 4685-4693 [Abstract] [Full Text]
Zhang, W., Qi, W., Albert, T. J., Motiwala, A. S., Alland, D., Hyytia-Trees, E. K., Ribot, E. M., Fields, P. I., Whittam, T. S., Swaminathan, B. (2006). Probing genomic diversity and evolution of Escherichia coli O157 by single nucleotide polymorphisms. Genome Res. 16: 757-767 [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]
Low, A. S., Dziva, F., Torres, A. G., Martinez, J. L., Rosser, T., Naylor, S., Spears, K., Holden, N., Mahajan, A., Findlay, J., Sales, J., Smith, D. G. E., Low, J. C., Stevens, M. P., Gally, D. L. (2006). Cloning, Expression, and Characterization of Fimbrial Operon F9 from Enterohemorrhagic Escherichia coli O157:H7. Infect. Immun. 74: 2233-2244 [Abstract] [Full Text]
Kim, S.-H., Jia, W., Parreira, V. R., Bishop, R. E., Gyles, C. L. (2006). Phosphoethanolamine substitution in the lipid A of Escherichia coli O157 : H7 and its association with PmrC.. Microbiology 152: 657-666 [Abstract] [Full Text]
Tozzoli, R., Caprioli, A., Morabito, S. (2005). Detection of toxB, a Plasmid Virulence Gene of Escherichia coli O157, in Enterohemorrhagic and Enteropathogenic E. coli. J. Clin. Microbiol. 43: 4052-4056 [Abstract] [Full Text]
Yoon, J. W., Lim, J. Y., Park, Y. H., Hovde, C. J. (2005). Involvement of the Escherichia coli O157:H7(pO157) ecf Operon and Lipid A Myristoyl Transferase Activity in Bacterial Survival in the Bovine Gastrointestinal Tract and Bacterial Persistence in Farm Water Troughs. Infect. Immun. 73: 2367-2378 [Abstract] [Full Text]
Klapproth, J.-M. A., Sasaki, M., Sherman, M., Babbin, B., Donnenberg, M. S., Fernandes, P. J., Scaletsky, I. C. A., Kalman, D., Nusrat, A., Williams, I. R. (2005). Citrobacter rodentium lifA/efa1 Is Essential for Colonic Colonization and Crypt Cell Hyperplasia In Vivo. Infect. Immun. 73: 1441-1451 [Abstract] [Full Text]
Nagai, T., Abe, A., Sasakawa, C. (2005). Targeting of Enteropathogenic Escherichia coli EspF to Host Mitochondria Is Essential for Bacterial Pathogenesis: CRITICAL ROLE OF THE 16TH LEUCINE RESIDUE IN EspF. J. Biol. Chem. 280: 2998-3011 [Abstract] [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]
Zhang, L., Chaudhuri, R. R., Constantinidou, C., Hobman, J. L., Patel, M. D., Jones, A. C., Sarti, D., Roe, A. J., Vlisidou, I., Shaw, R. K., Falciani, F., Stevens, M. P., Gally, D. L., Knutton, S., Frankel, G., Penn, C. W., Pallen, M. J. (2004). Regulators Encoded in the Escherichia coli Type III Secretion System 2 Gene Cluster Influence Expression of Genes within the Locus for Enterocyte Effacement in Enterohemorrhagic E. coli O157:H7. Infect. Immun. 72: 7282-7293 [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]
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]
Stevens, M. P., Roe, A. J., Vlisidou, I., van Diemen, P. M., La Ragione, R. M., Best, A., Woodward, M. J., Gally, D. L., Wallis, T. S. (2004). Mutation of toxB and a Truncated Version of the efa-1 Gene in Escherichia coli O157:H7 Influences the Expression and Secretion of Locus of Enterocyte Effacement-Encoded Proteins but not Intestinal Colonization in Calves or Sheep. Infect. Immun. 72: 5402-5411 [Abstract] [Full Text]
Kim, S.-H., Jia, W., Bishop, R. E., Gyles, C. (2004). An msbB Homologue Carried in Plasmid pO157 Encodes an Acyltransferase Involved in Lipid A Biosynthesis in Escherichia coli O157:H7. Infect. Immun. 72: 1174-1180 [Abstract] [Full Text]
Schmidt, H., Hensel, M. (2004). Pathogenicity Islands in Bacterial Pathogenesis. Clin. Microbiol. Rev. 17: 14-56 [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]
Batisson, I., Guimond, M.-P., Girard, F., An, H., Zhu, C., Oswald, E., Fairbrother, J. M., Jacques, M., Harel, J. (2003). Characterization of the Novel Factor Paa Involved in the Early Steps of the Adhesion Mechanism of Attaching and Effacing Escherichia coli. Infect. Immun. 71: 4516-4525 [Abstract] [Full Text]
Tatsuno, I., Nagano, K., Taguchi, K., Rong, L., Mori, H., Sasakawa, C. (2003). Increased Adherence to Caco-2 Cells Caused by Disruption of the yhiE and yhiF Genes in Enterohemorrhagic Escherichia coli O157:H7. Infect. Immun. 71: 2598-2606 [Abstract] [Full Text]
Tarr, C. L., Large, T. M., Moeller, C. L., Lacher, D. W., Tarr, P. I., Acheson, D. W., Whittam, T. S. (2002). Molecular Characterization of a Serotype O121:H19 Clone, a Distinct Shiga Toxin-Producing Clone of Pathogenic Escherichia coli. Infect. Immun. 70: 6853-6859 [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]
Stevens, M. P., van Diemen, P. M., Frankel, G., Phillips, A. D., Wallis, T. S. (2002). Efa1 Influences Colonization of the Bovine Intestine by Shiga Toxin-Producing Escherichia coli Serotypes O5 and O111. Infect. Immun. 70: 5158-5166 [Abstract] [Full Text]

J. Bacteriol.	J. Virol.	Eukaryot. Cell

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