TccP2-mediated subversion of actin dynamics by EPEC 2 - A distinct evolutionary lineage of enteropathogenic Escherichia coli

Andrew D. Whale, Rodrigo T. Hernandes, Tadasuke Ooka, Lothar Beutin, Stephanie Schüller, Junkal Garmendia, Lynette Crowther, Mônica A.M. Vieira, Yoshitoshi Ogura, Gladys Krause, Alan D. Phillips, Tania A.T. Gomes, Tetsuya Hayashi, Gad Frankel

Research output: Contribution to journalArticle

24 Citations (Scopus)

Abstract

Enteropathogenic Escherichia coli (EPEC) is a major cause of infantile diarrhoea in developing countries. While colonizing the gut mucosa, EPEC triggers extensive actin-polymerization activity at the site of intimate bacterial attachment, which is mediated by avid interaction between the outer-membrane adhesin intimin and the type III secretion system (T3SS) effector Tir. The prevailing dogma is that actin polymerization by EPEC is achieved following tyrosine phosphorylation of Tir, recruitment of Nck and activation of neuronal Wiskott-Aldrich syndrome protein (N-WASP). In closely related enterohaemorrhagic E. coli (EHEC) O157: H7, actin polymerization is triggered following recruitment of the T3SS effector TccP/EspFu (instead of Nck) and local activation of N-WASP. In addition to tccP, typical EHEC O157 : H7 harbour a pseudogene (tccP2). However, it has recently been found that atypical, sorbitol-fermenting EHEC O157 carries functional tccP and tccP2 alleles. Interestingly, intact tccP2 has been identified in the incomplete genome sequence of the prototype EPEC strain B171 (serotype O111 : H-), but it is missing from another prototype EPEC strain E2348/69 (O127 : H7). E2348/69 and B171 belong to two distinct evolutionary lineages of EPEC, termed EPEC 1 and EPEC 2, respectively. Here, it is reported that while both EPEC 1 and EPEC 2 triggered actin polymerization via the Nck pathway, tccP2 was found in 26 of 27 (96.2%) strains belonging to EPEC 2, and in none of the 34 strains belonging to EPEC 1. It was shown that TccP2 was: (i) translocated by the locus of enterocyte effacement-encoded T3SS; (ii) localized at the tip of the EPEC 2-induced actin-rich pedestals in infected HeLa cells and human intestinal in vitro organ cultures ex vivo; and (iii) essential for actin polymerization in infected Nck-/- cells. Therefore, unlike strains belonging to EPEC 1, strains belonging to EPEC 2 can trigger actin polymerization using both Nck and TccP2 actin-polymerization signalling cascades.

Original languageEnglish
Pages (from-to)1743-1755
Number of pages13
JournalMicrobiology
Volume153
Issue number6
DOIs
Publication statusPublished - Jun 1 2007

Fingerprint

Enteropathogenic Escherichia coli
Actins
Polymerization
Enterohemorrhagic Escherichia coli
Neuronal Wiskott-Aldrich Syndrome Protein
Escherichia coli O157
Microbiological Attachment Sites
Infantile Diarrhea
Pseudogenes
Sorbitol
Enterocytes
Organ Culture Techniques
HeLa Cells

All Science Journal Classification (ASJC) codes

  • Microbiology

Cite this

Whale, A. D., Hernandes, R. T., Ooka, T., Beutin, L., Schüller, S., Garmendia, J., ... Frankel, G. (2007). TccP2-mediated subversion of actin dynamics by EPEC 2 - A distinct evolutionary lineage of enteropathogenic Escherichia coli. Microbiology, 153(6), 1743-1755. https://doi.org/10.1099/mic.0.2006/004325-0

TccP2-mediated subversion of actin dynamics by EPEC 2 - A distinct evolutionary lineage of enteropathogenic Escherichia coli. / Whale, Andrew D.; Hernandes, Rodrigo T.; Ooka, Tadasuke; Beutin, Lothar; Schüller, Stephanie; Garmendia, Junkal; Crowther, Lynette; Vieira, Mônica A.M.; Ogura, Yoshitoshi; Krause, Gladys; Phillips, Alan D.; Gomes, Tania A.T.; Hayashi, Tetsuya; Frankel, Gad.

In: Microbiology, Vol. 153, No. 6, 01.06.2007, p. 1743-1755.

Research output: Contribution to journalArticle

Whale, AD, Hernandes, RT, Ooka, T, Beutin, L, Schüller, S, Garmendia, J, Crowther, L, Vieira, MAM, Ogura, Y, Krause, G, Phillips, AD, Gomes, TAT, Hayashi, T & Frankel, G 2007, 'TccP2-mediated subversion of actin dynamics by EPEC 2 - A distinct evolutionary lineage of enteropathogenic Escherichia coli', Microbiology, vol. 153, no. 6, pp. 1743-1755. https://doi.org/10.1099/mic.0.2006/004325-0
Whale, Andrew D. ; Hernandes, Rodrigo T. ; Ooka, Tadasuke ; Beutin, Lothar ; Schüller, Stephanie ; Garmendia, Junkal ; Crowther, Lynette ; Vieira, Mônica A.M. ; Ogura, Yoshitoshi ; Krause, Gladys ; Phillips, Alan D. ; Gomes, Tania A.T. ; Hayashi, Tetsuya ; Frankel, Gad. / TccP2-mediated subversion of actin dynamics by EPEC 2 - A distinct evolutionary lineage of enteropathogenic Escherichia coli. In: Microbiology. 2007 ; Vol. 153, No. 6. pp. 1743-1755.
@article{44727d1456aa4d439c0dcf6259e864f2,
title = "TccP2-mediated subversion of actin dynamics by EPEC 2 - A distinct evolutionary lineage of enteropathogenic Escherichia coli",
abstract = "Enteropathogenic Escherichia coli (EPEC) is a major cause of infantile diarrhoea in developing countries. While colonizing the gut mucosa, EPEC triggers extensive actin-polymerization activity at the site of intimate bacterial attachment, which is mediated by avid interaction between the outer-membrane adhesin intimin and the type III secretion system (T3SS) effector Tir. The prevailing dogma is that actin polymerization by EPEC is achieved following tyrosine phosphorylation of Tir, recruitment of Nck and activation of neuronal Wiskott-Aldrich syndrome protein (N-WASP). In closely related enterohaemorrhagic E. coli (EHEC) O157: H7, actin polymerization is triggered following recruitment of the T3SS effector TccP/EspFu (instead of Nck) and local activation of N-WASP. In addition to tccP, typical EHEC O157 : H7 harbour a pseudogene (tccP2). However, it has recently been found that atypical, sorbitol-fermenting EHEC O157 carries functional tccP and tccP2 alleles. Interestingly, intact tccP2 has been identified in the incomplete genome sequence of the prototype EPEC strain B171 (serotype O111 : H-), but it is missing from another prototype EPEC strain E2348/69 (O127 : H7). E2348/69 and B171 belong to two distinct evolutionary lineages of EPEC, termed EPEC 1 and EPEC 2, respectively. Here, it is reported that while both EPEC 1 and EPEC 2 triggered actin polymerization via the Nck pathway, tccP2 was found in 26 of 27 (96.2{\%}) strains belonging to EPEC 2, and in none of the 34 strains belonging to EPEC 1. It was shown that TccP2 was: (i) translocated by the locus of enterocyte effacement-encoded T3SS; (ii) localized at the tip of the EPEC 2-induced actin-rich pedestals in infected HeLa cells and human intestinal in vitro organ cultures ex vivo; and (iii) essential for actin polymerization in infected Nck-/- cells. Therefore, unlike strains belonging to EPEC 1, strains belonging to EPEC 2 can trigger actin polymerization using both Nck and TccP2 actin-polymerization signalling cascades.",
author = "Whale, {Andrew D.} and Hernandes, {Rodrigo T.} and Tadasuke Ooka and Lothar Beutin and Stephanie Sch{\"u}ller and Junkal Garmendia and Lynette Crowther and Vieira, {M{\^o}nica A.M.} and Yoshitoshi Ogura and Gladys Krause and Phillips, {Alan D.} and Gomes, {Tania A.T.} and Tetsuya Hayashi and Gad Frankel",
year = "2007",
month = "6",
day = "1",
doi = "10.1099/mic.0.2006/004325-0",
language = "English",
volume = "153",
pages = "1743--1755",
journal = "Microbiology",
issn = "1350-0872",
publisher = "Society for General Microbiology",
number = "6",

}

TY - JOUR

T1 - TccP2-mediated subversion of actin dynamics by EPEC 2 - A distinct evolutionary lineage of enteropathogenic Escherichia coli

AU - Whale, Andrew D.

AU - Hernandes, Rodrigo T.

AU - Ooka, Tadasuke

AU - Beutin, Lothar

AU - Schüller, Stephanie

AU - Garmendia, Junkal

AU - Crowther, Lynette

AU - Vieira, Mônica A.M.

AU - Ogura, Yoshitoshi

AU - Krause, Gladys

AU - Phillips, Alan D.

AU - Gomes, Tania A.T.

AU - Hayashi, Tetsuya

AU - Frankel, Gad

PY - 2007/6/1

Y1 - 2007/6/1

N2 - Enteropathogenic Escherichia coli (EPEC) is a major cause of infantile diarrhoea in developing countries. While colonizing the gut mucosa, EPEC triggers extensive actin-polymerization activity at the site of intimate bacterial attachment, which is mediated by avid interaction between the outer-membrane adhesin intimin and the type III secretion system (T3SS) effector Tir. The prevailing dogma is that actin polymerization by EPEC is achieved following tyrosine phosphorylation of Tir, recruitment of Nck and activation of neuronal Wiskott-Aldrich syndrome protein (N-WASP). In closely related enterohaemorrhagic E. coli (EHEC) O157: H7, actin polymerization is triggered following recruitment of the T3SS effector TccP/EspFu (instead of Nck) and local activation of N-WASP. In addition to tccP, typical EHEC O157 : H7 harbour a pseudogene (tccP2). However, it has recently been found that atypical, sorbitol-fermenting EHEC O157 carries functional tccP and tccP2 alleles. Interestingly, intact tccP2 has been identified in the incomplete genome sequence of the prototype EPEC strain B171 (serotype O111 : H-), but it is missing from another prototype EPEC strain E2348/69 (O127 : H7). E2348/69 and B171 belong to two distinct evolutionary lineages of EPEC, termed EPEC 1 and EPEC 2, respectively. Here, it is reported that while both EPEC 1 and EPEC 2 triggered actin polymerization via the Nck pathway, tccP2 was found in 26 of 27 (96.2%) strains belonging to EPEC 2, and in none of the 34 strains belonging to EPEC 1. It was shown that TccP2 was: (i) translocated by the locus of enterocyte effacement-encoded T3SS; (ii) localized at the tip of the EPEC 2-induced actin-rich pedestals in infected HeLa cells and human intestinal in vitro organ cultures ex vivo; and (iii) essential for actin polymerization in infected Nck-/- cells. Therefore, unlike strains belonging to EPEC 1, strains belonging to EPEC 2 can trigger actin polymerization using both Nck and TccP2 actin-polymerization signalling cascades.

AB - Enteropathogenic Escherichia coli (EPEC) is a major cause of infantile diarrhoea in developing countries. While colonizing the gut mucosa, EPEC triggers extensive actin-polymerization activity at the site of intimate bacterial attachment, which is mediated by avid interaction between the outer-membrane adhesin intimin and the type III secretion system (T3SS) effector Tir. The prevailing dogma is that actin polymerization by EPEC is achieved following tyrosine phosphorylation of Tir, recruitment of Nck and activation of neuronal Wiskott-Aldrich syndrome protein (N-WASP). In closely related enterohaemorrhagic E. coli (EHEC) O157: H7, actin polymerization is triggered following recruitment of the T3SS effector TccP/EspFu (instead of Nck) and local activation of N-WASP. In addition to tccP, typical EHEC O157 : H7 harbour a pseudogene (tccP2). However, it has recently been found that atypical, sorbitol-fermenting EHEC O157 carries functional tccP and tccP2 alleles. Interestingly, intact tccP2 has been identified in the incomplete genome sequence of the prototype EPEC strain B171 (serotype O111 : H-), but it is missing from another prototype EPEC strain E2348/69 (O127 : H7). E2348/69 and B171 belong to two distinct evolutionary lineages of EPEC, termed EPEC 1 and EPEC 2, respectively. Here, it is reported that while both EPEC 1 and EPEC 2 triggered actin polymerization via the Nck pathway, tccP2 was found in 26 of 27 (96.2%) strains belonging to EPEC 2, and in none of the 34 strains belonging to EPEC 1. It was shown that TccP2 was: (i) translocated by the locus of enterocyte effacement-encoded T3SS; (ii) localized at the tip of the EPEC 2-induced actin-rich pedestals in infected HeLa cells and human intestinal in vitro organ cultures ex vivo; and (iii) essential for actin polymerization in infected Nck-/- cells. Therefore, unlike strains belonging to EPEC 1, strains belonging to EPEC 2 can trigger actin polymerization using both Nck and TccP2 actin-polymerization signalling cascades.

UR - http://www.scopus.com/inward/record.url?scp=34247847571&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=34247847571&partnerID=8YFLogxK

U2 - 10.1099/mic.0.2006/004325-0

DO - 10.1099/mic.0.2006/004325-0

M3 - Article

VL - 153

SP - 1743

EP - 1755

JO - Microbiology

JF - Microbiology

SN - 1350-0872

IS - 6

ER -