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Journal of Bacteriology, July 2008, p. 5063-5074, Vol. 190, No. 14
0021-9193/08/$08.00+0 doi:10.1128/JB.00440-08
Copyright © 2008, American Society for Microbiology. All Rights Reserved.
Transient Shielding of Intimin and the Type III Secretion System of Enterohemorrhagic and Enteropathogenic Escherichia coli by a Group 4 Capsule
,
Yulia Shifrin,1
Adi Peleg,1
Ophir Ilan,1
Chen Nadler,1
Simi Kobi,1
Kobi Baruch,1
Gal Yerushalmi,1
Tatiana Berdichevsky,1
Shoshy Altuvia,1
Maya Elgrably-Weiss,1
Cecilia Abe,2,
Stuart Knutton,2
Chihiro Sasakawa,3
Jennifer M. Ritchie,4
Matthew K. Waldor,4 and
Ilan Rosenshine1*
Department of Molecular Genetics and Biotechnology, The Hebrew University Faculty of Medicine, POB 12272, Jerusalem 91120, Israel,1 Institute of Child Health, University of Birmingham, Whittall Street, Birmingham B4 6NH, United Kingdom,2 Departments of Microbiology and Immunology and Infectious Disease Control, International Research Center for Infectious Disease, Institute of Medical Science, University of Tokyo, 4-6-1 Shirokanedai, Minato-ku, Tokyo 108-8639, Japan,3 The Channing Laboratory, Harvard Medical School, 181 Longwood Ave., Boston Massachusetts 021154
Received 31 March 2008/ Accepted 12 May 2008
Enterohemorrhagic and enteropathogenic Escherichia coli (EHEC and EPEC, respectively) strains represent a major global health problem. Their virulence is mediated by the concerted activity of an array of virulence factors including toxins, a type III protein secretion system (TTSS), pili, and others. We previously showed that EPEC O127 forms a group 4 capsule (G4C), and in this report we show that EHEC O157 also produces a G4C, whose assembly is dependent on the etp, etk, and wzy genes. We further show that at early time points postinfection, these G4Cs appear to mask surface structures including intimin and the TTSS. This masking inhibited the attachment of EPEC and EHEC to tissue-cultured epithelial cells, diminished their capacity to induce the formation of actin pedestals, and attenuated TTSS-mediated protein translocation into host cells. Importantly, we found that Ler, a positive regulator of intimin and TTSS genes, represses the expression of the capsule-related genes, including etp and etk. Thus, the expression of TTSS and G4C is conversely regulated and capsule production is diminished upon TTSS expression. Indeed, at later time points postinfection, the diminishing capsule no longer interferes with the activities of intimin and the TTSS. Notably, by using the rabbit infant model, we found that the EHEC G4C is required for efficient colonization of the rabbit large intestine. Taken together, our results suggest that temporal expression of the capsule, which is coordinated with that of the TTSS, is required for optimal EHEC colonization of the host intestine.
* Corresponding author. Mailing address: Department of Molecular Genetics and Biotechnology, Faculty of Medicine, The Hebrew University, POB 12272, Jerusalem 91120, Israel. Phone: 972-2-6758754. Fax: 972-2-6757308. E-mail: ilanr{at}ekmd.huji.ac.il
Published ahead of print on 23 May 2008.
Supplemental material for this article may be found at http://jb.asm.org/.
Present address: Laboratório de Bacteriologia, Instituto Butantan, Avenida Vital Brazil, 1500, cep 05503-900, São Paulo, Brazil.
Journal of Bacteriology, July 2008, p. 5063-5074, Vol. 190, No. 14
0021-9193/08/$08.00+0 doi:10.1128/JB.00440-08
Copyright © 2008, American Society for Microbiology. All Rights Reserved.
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