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Infection and Immunity, February 2007, p. 604-612, Vol. 75, No. 2
0019-9567/07/$08.00+0     doi:10.1128/IAI.01491-06
Copyright © 2007, American Society for Microbiology. All Rights Reserved.

TccP2 of O157:H7 and Non-O157 Enterohemorrhagic Escherichia coli (EHEC): Challenging the Dogma of EHEC-Induced Actin Polymerization{triangledown}

Yoshitoshi Ogura,1,{dagger} Tadasuke Ooka,1,{dagger} Andrew Whale,2,{dagger} Junkal Garmendia,2 Lothar Beutin,3 Sharon Tennant,4 Gladys Krause,3 Stefano Morabito,5 Isabel Chinen,6 Toru Tobe,7 Hiroyuki Abe,7 Rosangela Tozzoli,5 Alfredo Caprioli,5 Marta Rivas,6 Roy Robins-Browne,4 Tetsuya Hayashi,1 and Gad Frankel2*

Division of Bioenvironmental Science, Frontier Science Research Center, University of Miyazaki, 5200 Kiyotake, Miyazaki 889-1692, Japan,1 Division of Cell and Molecular Biology, Imperial College London, London SW7 2AZ, United Kingdom,2 Nationales Referenzlabor für Escherichia coli, Bundesinstitut für Risikobewertung, Diedersdorfer Weg 1, D-12277 Berlin, Germany,3 Department of Microbiology and Immunology, University of Melbourne, Melbourne, Victoria, Australia,4 Dipartimento di Sanità Alimentare e Animale Istituto Superiore di Sanità, 00161 Rome, Italy,5 Instituto Nacional de Enfermedades Infecciosas, 1281 Buenos Aires, Argentina,6 Graduate School of Medicine, Osaka University, 2-2 Yamadaoka, Suita, Osaka 565-0871, Japan7

Received 18 September 2006/ Returned for modification 13 October 2006/ Accepted 20 October 2006

Enterohemorrhagic Escherichia coli (EHEC) O157:H7 and enteropathogenic E. coli (EPEC) trigger actin polymerization at the site of bacterial adhesion by inducing different signaling pathways. Actin assembly by EPEC requires tyrosine phosphorylation of Tir, which subsequently binds the host adaptor protein Nck. In contrast, TirEHEC O157 is not tyrosine phosphorylated and instead of Nck utilizes the bacterially encoded Tir-cytoskeleton coupling protein (TccP)/EspFU, which mimics the function of Nck. tccP is carried on prophage CP-933U/Sp14 (TccP). Typical isolates of EHEC O157:H7 harbor a pseudo-tccP gene that is carried on prophage CP-933 M/Sp4 (tccP2). Here we report that atypical, ß-glucuronidase-positive and sorbitol-fermenting, strains of EHEC O157 harbor intact tccP and tccP2 genes, both of which are secreted by the LEE-encoded type III secretion system. Non-O157 EHEC strains, including O26, O103, O111, and O145, are typically tccP negative and translocate a Tir protein that encompasses an Nck binding site. Unexpectedly, we found that most clinical non-O157 EHEC isolates carry a functional tccP2 gene that encodes a secreted protein that can complement an EHEC O157:H7 {Delta}tccP mutant. Using discriminatory, allele-specific PCR, we have demonstrated that over 90% of tccP2-positive non-O157 EHEC strains contain a Tir protein that can be tyrosine phosphorylated. These results suggest that the TccP pathway can be used by both O157 and non-O157 EHEC and that non-O157 EHEC can also trigger actin polymerization via the Nck pathway.

* Corresponding author. Mailing address: Division of Cell and Molecular Biology, Flowers Building, Imperial College London, London SW7 2AZ, United Kingdom. Phone: 44 020 2594 525. Fax: 44 020 5794 3069. E-mail: g.frankel{at}imperial.ac.uk.

{triangledown} Published ahead of print on 13 November 2006.

Editor: A. D. O'Brien

{dagger} Yoshitoshi Ogura, Tadasuke Ooka, and Andrew Whale contributed equally to this work.

Infection and Immunity, February 2007, p. 604-612, Vol. 75, No. 2
0019-9567/07/$08.00+0     doi:10.1128/IAI.01491-06
Copyright © 2007, American Society for Microbiology. All Rights Reserved.



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