TccP2 of O157:H7 and non-O157 enterohemorrhagic Escherichia coli (EHEC)

Challenging the dogma of EHEC-induced actin polymerization

Yoshitoshi Ogura, Tadasuke Ooka, Andrew Whale, Junkal Garmendia, Lothar Beutin, Sharon Tennant, Gladys Krause, Stefano Morabito, Isabel Chinen, Toru Tobe, Hiroyuki Abe, Rosangela Tozzoli, Alfredo Caprioli, Marta Rivas, Roy Robins-Browne, Tetsuya Hayashi, Gad Frankel

Research output: Contribution to journalArticle

42 Citations (Scopus)

Abstract

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, β-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 ΔtccP 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.

Original languageEnglish
Pages (from-to)604-612
Number of pages9
JournalInfection and Immunity
Volume75
Issue number2
DOIs
Publication statusPublished - Feb 1 2007
Externally publishedYes

Fingerprint

Enterohemorrhagic Escherichia coli
Polymerization
Actins
Escherichia coli O157
Cytoskeleton
Prophages
Tyrosine
Enteropathogenic Escherichia coli
Proteins
Genes
Bacterial Adhesion
Sorbitol
Glucuronidase
Complement System Proteins
Alleles
Binding Sites
Phosphorylation
Polymerase Chain Reaction

All Science Journal Classification (ASJC) codes

  • Parasitology
  • Microbiology
  • Immunology
  • Infectious Diseases

Cite this

TccP2 of O157:H7 and non-O157 enterohemorrhagic Escherichia coli (EHEC) : Challenging the dogma of EHEC-induced actin polymerization. / Ogura, Yoshitoshi; Ooka, Tadasuke; Whale, Andrew; Garmendia, Junkal; Beutin, Lothar; Tennant, Sharon; Krause, Gladys; Morabito, Stefano; Chinen, Isabel; Tobe, Toru; Abe, Hiroyuki; Tozzoli, Rosangela; Caprioli, Alfredo; Rivas, Marta; Robins-Browne, Roy; Hayashi, Tetsuya; Frankel, Gad.

In: Infection and Immunity, Vol. 75, No. 2, 01.02.2007, p. 604-612.

Research output: Contribution to journalArticle

Ogura, Y, Ooka, T, Whale, A, Garmendia, J, Beutin, L, Tennant, S, Krause, G, Morabito, S, Chinen, I, Tobe, T, Abe, H, Tozzoli, R, Caprioli, A, Rivas, M, Robins-Browne, R, Hayashi, T & Frankel, G 2007, 'TccP2 of O157:H7 and non-O157 enterohemorrhagic Escherichia coli (EHEC): Challenging the dogma of EHEC-induced actin polymerization', Infection and Immunity, vol. 75, no. 2, pp. 604-612. https://doi.org/10.1128/IAI.01491-06
Ogura, Yoshitoshi ; Ooka, Tadasuke ; Whale, Andrew ; Garmendia, Junkal ; Beutin, Lothar ; Tennant, Sharon ; Krause, Gladys ; Morabito, Stefano ; Chinen, Isabel ; Tobe, Toru ; Abe, Hiroyuki ; Tozzoli, Rosangela ; Caprioli, Alfredo ; Rivas, Marta ; Robins-Browne, Roy ; Hayashi, Tetsuya ; Frankel, Gad. / TccP2 of O157:H7 and non-O157 enterohemorrhagic Escherichia coli (EHEC) : Challenging the dogma of EHEC-induced actin polymerization. In: Infection and Immunity. 2007 ; Vol. 75, No. 2. pp. 604-612.
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abstract = "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, β-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 ΔtccP 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.",
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AU - Ooka, Tadasuke

AU - Whale, Andrew

AU - Garmendia, Junkal

AU - Beutin, Lothar

AU - Tennant, Sharon

AU - Krause, Gladys

AU - Morabito, Stefano

AU - Chinen, Isabel

AU - Tobe, Toru

AU - Abe, Hiroyuki

AU - Tozzoli, Rosangela

AU - Caprioli, Alfredo

AU - Rivas, Marta

AU - Robins-Browne, Roy

AU - Hayashi, Tetsuya

AU - Frankel, Gad

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