Home LiteratureArticle Details
PMID: 18331467 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Subversion of actin dynamics by EspM effectors of attaching and effacing bacterial pathogens.

Cellular microbiology ·Vol. 10 ·No. 7 ·2008-07-00 ·Pages 1429-41

Arbeloa A, Bulgin RR, MacKenzie G, Shaw RK, Pallen MJ, Crepin VF, Berger CN, Frankel G

Abstract

Rho GTPases are common targets of bacterial toxins and type III secretion system effectors. IpgB1 and IpgB2 of Shigella and Map of enteropathogenic (EPEC) and enterohemorrhagic (EHEC) Escherichia coli were recently grouped together on the basis that they share a conserved WxxxE motif. In this study, we characterized six WxxxE effectors from attaching and effacing pathogens: TrcA and EspM1 of EPEC strain B171, EspM1 and EspM2 of EHEC strain Sakai and EspM2 and EspM3 of Citrobacter rodentium. We show that EspM2 triggers formation of global parallel stress fibres, TrcA and EspM1 induce formation of localized parallel stress fibres and EspM3 triggers formation of localized radial stress fibres. Using EspM2 and EspM3 as model effectors, we report that while substituting the conserved Trp with Ala abolished activity, conservative Trp to Tyr or Glu to Asp substitutions did not affect stress-fibre formation. We show, using dominant negative constructs and chemical inhibitors, that the activity of EspM2 and EspM3 is RhoA and ROCK-dependent. Using Rhotekin pull-downs, we have shown that EspM2 and EspM3 activate RhoA; translocation of EspM2 and EspM3 triggered phosphorylation of cofilin. These results suggest that the EspM effectors modulate actin dynamics by activating the RhoA signalling pathway.

MeSH Terms
3T3 Cells Actin Depolymerizing Factors/metabolism Actins/metabolism Amino Acid Sequence Animals Apoptosis Regulatory Proteins Bacteria/metabolism,pathogenicity Bacterial Adhesion/physiology Bacterial Proteins/genetics,metabolism Enzyme Activation GTP-Binding Proteins Humans Intracellular Signaling Peptides and Proteins/genetics,metabolism Mice Molecular Sequence Data Mutagenesis, Site-Directed Phylogeny Sequence Alignment Signal Transduction/physiology Stress Fibers/metabolism rho GTP-Binding Proteins/genetics,metabolism rho-Associated Kinases/metabolism
Chemicals
Actin Depolymerizing Factors Actins Apoptosis Regulatory Proteins Bacterial Proteins Intracellular Signaling Peptides and Proteins Rtkn protein, mouse rho-Associated Kinases GTP-Binding Proteins rho GTP-Binding Proteins
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Arbeloa Ana
Division of Cell and Molecular Biology, Imperial College London, London SW7 2AZ, UK.
Bulgin Richard R
MacKenzie Georgina
Shaw Robert K
Pallen Mark J
Crepin Valerie F
Berger Cedric N
Frankel Gad
References (42)
42 references, click to expand
  1. Multiple sequence alignment with hierarchical clustering.
    Nucleic Acids Res. 1988 Nov 25;16(22):10881-90 PMID: 2849754
  2. Shigella IpgB1 promotes bacterial entry through the ELMO-Dock180 machinery.
    Nat Cell Biol. 2007 Jan;9(1):121-8 PMID: 17173036
  3. Targeting of an enteropathogenic Escherichia coli (EPEC) effector protein to host mitochondria.
    Cell Microbiol. 2000 Dec;2(6):579-90 PMID: 11207610
  4. The enteropathogenic Escherichia coli type III secretion system effector Map binds EBP50/NHERF1: implication for cell signalling and diarrhoea.
    Mol Microbiol. 2006 Apr;60(2):349-63 PMID: 16573685
  5. Yersinia pseudotuberculosis spatially controls activation and misregulation of host cell Rac1.
    PLoS Pathog. 2005 Oct;1(2):e16 PMID: 16228016
  6. Bacterial virulence strategies that utilize Rho GTPases.
    Curr Top Microbiol Immunol. 2005;291:1-10 PMID: 15981456
  7. Protein delivery into eukaryotic cells by type III secretion machines.
    Nature. 2006 Nov 30;444(7119):567-73 PMID: 17136086
  8. Signaling from Rho to the actin cytoskeleton through protein kinases ROCK and LIM-kinase.
    Science. 1999 Aug 6;285(5429):895-8 PMID: 10436159
  9. Plasmid-encoded expression of lipopolysaccharide O-antigenic polysaccharide in enteropathogenic Escherichia coli.
    Infect Immun. 1987 Sep;55(9):2052-6 PMID: 3305360
  10. EspFU is a translocated EHEC effector that interacts with Tir and N-WASP and promotes Nck-independent actin assembly.
    Dev Cell. 2004 Aug;7(2):217-28 PMID: 15296718
  11. Bacterial invasion: the paradigms of enteroinvasive pathogens.
    Science. 2004 Apr 9;304(5668):242-8 PMID: 15073367
  12. Enteropathogenic E. coli (EPEC) transfers its receptor for intimate adherence into mammalian cells.
    Cell. 1997 Nov 14;91(4):511-20 PMID: 9390560
  13. Escherichia coli strains that cause diarrhoea but do not produce heat-labile or heat-stable enterotoxins and are non-invasive.
    Lancet. 1978 May 27;1(8074):1119-22 PMID: 77415
  14. Co-ordinate regulation of distinct host cell signalling pathways by multifunctional enteropathogenic Escherichia coli effector molecules.
    Mol Microbiol. 2002 May;44(4):1095-1107 PMID: 12046591
  15. Salmonella maintains the integrity of its intracellular vacuole through the action of SifA.
    EMBO J. 2000 Jul 3;19(13):3235-49 PMID: 10880437
  16. Organ specificity, colonization and clearance dynamics in vivo following oral challenges with the murine pathogen Citrobacter rodentium.
    Cell Microbiol. 2004 Oct;6(10):963-72 PMID: 15339271
  17. Enteropathogenic Escherichia coli type III effectors EspG and EspG2 disrupt the microtubule network of intestinal epithelial cells.
    Infect Immun. 2005 Jul;73(7):4385-90 PMID: 15972534
  18. Pathogenic Escherichia coli.
    Nat Rev Microbiol. 2004 Feb;2(2):123-40 PMID: 15040260
  19. Rho and Rab small G proteins coordinately reorganize stress fibers and focal adhesions in MDCK cells.
    Mol Biol Cell. 1998 Sep;9(9):2561-75 PMID: 9725912
  20. Complete genome sequence of enterohemorrhagic Escherichia coli O157:H7 and genomic comparison with a laboratory strain K-12.
    DNA Res. 2001 Feb 28;8(1):11-22 PMID: 11258796
  21. Characterization of Escherichia coli DNA lesions generated within J774 macrophages.
    J Bacteriol. 2000 Sep;182(18):5225-30 PMID: 10960109
  22. Enteropathogenic Escherichia coli O125:H6 triggers attaching and effacing lesions on human intestinal biopsy specimens independently of Nck and TccP/TccP2.
    Infect Immun. 2008 Jan;76(1):361-8 PMID: 17984209
  23. A novel chromosomal locus of enteropathogenic Escherichia coli (EPEC), which encodes a bfpT-regulated chaperone-like protein, TrcA, involved in microcolony formation by EPEC.
    Mol Microbiol. 1999 Aug;33(4):741-52 PMID: 10447884
  24. Cyclic AMP induces morphological changes of vascular smooth muscle cells by inhibiting a Rac-dependent signaling pathway.
    J Cell Physiol. 2005 Aug;204(2):412-22 PMID: 15706595
  25. Endoproteolytic processing of RhoA by Rce1 is required for the cleavage of RhoA by Yersinia enterocolitica outer protein T.
    Infect Immun. 2006 Mar;74(3):1712-7 PMID: 16495543
  26. Rho GTPases: biochemistry and biology.
    Annu Rev Cell Dev Biol. 2005;21:247-69 PMID: 16212495
  27. TccP is an enterohaemorrhagic Escherichia coli O157:H7 type III effector protein that couples Tir to the actin-cytoskeleton.
    Cell Microbiol. 2004 Dec;6(12):1167-83 PMID: 15527496
  28. Purification, characterization, cloning, and expression of a glutamic acid-specific protease from Bacillus licheniformis ATCC 14580.
    J Biol Chem. 1992 Nov 25;267(33):23782-8 PMID: 1429718
  29. Structural basis for induced-fit binding of Rho-kinase to the inhibitor Y-27632.
    J Biochem. 2006 Sep;140(3):305-11 PMID: 16891330
  30. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs.
    Nucleic Acids Res. 1997 Sep 1;25(17):3389-402 PMID: 9254694
  31. The effects of methyl (5-(2-thienylcarbonyl)-1H-benzimidazol-2-yl) carbamate, (R 17934; NSC 238159), a new synthetic antitumoral drug interfering with microtubules, on mammalian cells cultured in vitro.
    Cancer Res. 1976 Mar;36(3):905-16 PMID: 766963
  32. Rac downregulates Rho activity: reciprocal balance between both GTPases determines cellular morphology and migratory behavior.
    J Cell Biol. 1999 Nov 29;147(5):1009-22 PMID: 10579721
  33. Rapid modulation of electrolyte transport in Caco-2 cell monolayers by enteropathogenic Escherichia coli (EPEC) infection.
    Gut. 1998 Feb;42(2):200-7 PMID: 9536944
  34. Adhesion of enteropathogenic Escherichia coli to human intestinal enterocytes and cultured human intestinal mucosa.
    Infect Immun. 1987 Jan;55(1):69-77 PMID: 3539808
  35. Identification of the secretion and translocation domain of the enteropathogenic and enterohemorrhagic Escherichia coli effector Cif, using TEM-1 beta-lactamase as a new fluorescence-based reporter.
    J Bacteriol. 2004 Aug;186(16):5486-95 PMID: 15292151
  36. The etiology of transmissible murine colonic hyperplasia.
    Lab Anim Sci. 1976 Dec;26(6 Pt 1):889-94 PMID: 1018473
  37. Identification of a bacterial type III effector family with G protein mimicry functions.
    Cell. 2006 Jan 13;124(1):133-45 PMID: 16413487
  38. EspJ of enteropathogenic and enterohaemorrhagic Escherichia coli inhibits opsono-phagocytosis.
    Cell Microbiol. 2008 May;10(5):1104-15 PMID: 18201246
  39. The structure and regulation of vinculin.
    Trends Cell Biol. 2006 Sep;16(9):453-60 PMID: 16893648
  40. An extensive repertoire of type III secretion effectors in Escherichia coli O157 and the role of lambdoid phages in their dissemination.
    Proc Natl Acad Sci U S A. 2006 Oct 3;103(40):14941-6 PMID: 16990433
  41. IpgB1 is a novel Shigella effector protein involved in bacterial invasion of host cells. Its activity to promote membrane ruffling via Rac1 and Cdc42 activation.
    J Biol Chem. 2005 Jun 24;280(25):24022-34 PMID: 15849186
  42. Enteropathogenic Escherichia coli activates the RhoA signaling pathway via the stimulation of GEF-H1.
    EMBO J. 2004 Sep 1;23(17):3570-82 PMID: 15318166
Article Info
Journal
Cellular microbiology
Abbr.
Cell Microbiol
ISSN
1462-5822
Published
2008-07-00
Epub
2008-00-05
Pages
1429-41
Language
English
Region
England
NLM ID
100883691
PMCID
PMC2610399
Subset
IM
Grants
Wellcome Trust · United Kingdom
Medical Research Council · G0401551 · United Kingdom
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com