Skip to main content
SpringerLink
Log in

The Type III Secretion System of Pathogenic Escherichia coli

  • Chapter
  • First Online:
Escherichia coli, a Versatile Pathogen

Part of the book series: Current Topics in Microbiology and Immunology ((CT MICROBIOLOGY,volume 416))

Abstract

Infection with enteropathogenic and enterohaemorrhagic Escherichia coli (EPEC and EHEC), enteroinvasive E. coli (EIEC) and Shigella relies on the elaboration of a type III secretion system (T3SS). Few strains also encode a second T3SS, named ETT2. Through the integration of coordinated intracellular and extracellular cues, the modular T3SS is assembled within the bacterial cell wall, as well as the plasma membrane of the host cell. As such, the T3SS serves as a conduit, allowing the chaperone-regulated translocation of effector proteins directly into the host cytosol to subvert eukaryotic cell processes. Recent technological advances revealed high structural resolution of the T3SS apparatus and how it could be exploited to treat enteric disease. This chapter summarises the current knowledge of the structure and function of the E. coli T3SSs.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Alsharif G, Ahmad S, Islam MS, Shah R, Busby SJ, Krachler AM (2015) Host attachment and fluid shear are integrated into a mechanical signal regulating virulence in Escherichia coli O157:H7. Proc Natl Acad Sci U S A 112:5503–5508

    CAS  PubMed  PubMed Central  Google Scholar 

  • Berdichevsky T, Friedberg D, Nadler C, Rokney A, Oppenheim A, Rosenshine I (2005) Ler is a negative autoregulator of the LEE1 operon in enteropathogenic Escherichia coli. J Bacteriol 187:349–357

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bern C, Martines J, de Zoysa I, Glass RI (1992) The magnitude of the global problem of diarrhoeal disease: a ten-year update. Bull World Health Organ 70:705–714

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bhat A, Shin M, Jeong J-H, Kim H-J, Lim H-J, Rhee JH, Paik S-Y, Takeyasu K, Tobe T, Yen H et al (2014) DNA looping-dependent autorepression of LEE1 P1 promoters by Ler in enteropathogenic Escherichia coli (EPEC). Proc Natl Acad Sci U S A 111:E2586–E2595

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bichsel C, Neeld DK, Hamazaki T, Wu D, Chang LJ, Yang L, Terada N, Jin S (2011) Bacterial delivery of nuclear proteins into pluripotent and differentiated cells. PLoS ONE 6

    Google Scholar 

  • Biemans-Oldehinkel E, Sal-Man N, Deng W, Foster LJ, Finlay BB (2011) Quantitative proteomic analysis reveals formation of an EscL-EscQ-EscN type III complex in enteropathogenic Escherichia coli. J Bacteriol 193:5514–5519

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bingle LEH, Constantinidou C, Shaw RK, Islam MS, Patel M, Snyder LAS, Lee DJ, Penn CW, Busby SJW, Pallen MJ (2014) Microarray analysis of the Ler regulon in enteropathogenic and enterohaemorrhagic Escherichia coli strains. PLoS ONE 9:1–12

    Google Scholar 

  • Burkinshaw BJ, Deng W, Lameignère E, Wasney GA, Zhu H, Worrall LJ, Finlay BB, Strynadka NCJ (2015) Structural analysis of a specialized type III secretion system peptidoglycan-cleaving enzyme. J Biol Chem 290:10406–10417

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bustamante VH, Santana FJ, Calva E, Puente JL (2001) Transcriptional regulation of type III secretion genes in enteropathogenic Escherichia coli: ler antagonizes H-NS-dependent repression. Mol Microbiol 39:664–678

    CAS  PubMed  Google Scholar 

  • Buttner D (2012) Protein export according to schedule: architecture, assembly, and regulation of type III secretion systems from plant- and animal-pathogenic bacteria. Microbiol Mol Biol Rev 76:262–310

    PubMed  PubMed Central  Google Scholar 

  • Bzymek KP, Hamaoka BY, Ghosh P (2012) Two translation products of Yersinia yscQ assemble to form a complex essential to type III secretion. Biochemistry 51:1669–1677

    CAS  PubMed  PubMed Central  Google Scholar 

  • Carlson-Banning KM, Sperandio V (2018) Enterohemorrhagic Escherichia coli outwits hosts through sensing small molecules. Curr Opin Microbiol 41:83–88

    CAS  PubMed  Google Scholar 

  • Charro N, Mota LJ (2015) Approaches targeting the type III secretion system to treat or prevent bacterial infections. Expert Opin Drug Discov 10:373–387

    CAS  PubMed  Google Scholar 

  • Chen HD, Frankel G (2005) Enteropathogenic Escherichia coli: unravelling pathogenesis. FEMS Microbiol Rev 29:83–98

    PubMed  Google Scholar 

  • Cheng D, Zhu S, Su Z, Zuo W, Lu H (2012) Prevalence and isoforms of the pathogenicity island ETT2 among Escherichia coli isolates from colibacillosis in pigs and mastitis in cows. Curr Microbiol 64:43–49

    CAS  PubMed  Google Scholar 

  • Cleary J, Lai L-C, Shaw RK, Straatman-Iwanowska A, Donnenberg MS, Frankel G, Knutton S (2004) Enteropathogenic Escherichia coli (EPEC) adhesion to intestinal epithelial cells: role of bundle-forming pili (BFP), EspA filaments and intimin. Microbiology 150:527–538

    CAS  PubMed  Google Scholar 

  • Clements A, Young JC, Constantinou N, Frankel G (2011) Infection strategies of enteric pathogenic Escherichia coli. Gut Microbes 3:71–87

    Google Scholar 

  • Collins JW, Keeney KM, Crepin VF, Rathinam VAK, Fitzgerald KA, Finlay BB, Frankel G (2014) Citrobacter rodentium: infection, inflammation and the microbiota. Nat Rev Microbiol 12:612–623

    CAS  PubMed  Google Scholar 

  • Connolly JPR, Brett Finlay B, Roe AJ (2015) From ingestion to colonization: the influence of the host environment on regulation of the LEE encoded type III secretion system in enterohaemorrhagic Escherichia coli. Front Microbiol 6:1–15

    Google Scholar 

  • Creasey EA, Delahay RM, Daniell SJ, Frankel G (2003a) Yeast two-hybrid system survey of interactions between LEE-encoded proteins of enteropathogenic Escherichia coli. Microbiology 149:2093–2106

    CAS  PubMed  Google Scholar 

  • Creasey EA, Friedberg D, Shaw RK, Umanski T, Knutton S, Rosenshine I, Frankel G (2003b) CesAB is an enteropathogenic Escherichia coli chaperone for the type-III translocator proteins EspA and EspB. Microbiology 149:3639–3647

    CAS  PubMed  Google Scholar 

  • Crepin V, Shaw R, Abe C, Knutton S, Frankel G (2005) Polarity of enteropathogenic Escherichia coli EspA filament assembly and protein secretion. J Bacteriol 187:2881–2889

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dahan S, Knutton S, Shaw RK, Crepin VF, Dougan G, Frankel G (2004) Transcriptome of enterohemorrhagic Escherichia coli O157 adhering to eukaryotic plasma membranes. Infect Immun 72:5452–5459

    CAS  PubMed  PubMed Central  Google Scholar 

  • Daniell SJ, Takahashi N, Wilson R, Friedberg D, Rosenshine I, Booy FP, Shaw RK, Knutton S, Frankel G, Aizawa S (2001a) The filamentous type III secretion translocon of enteropathogenic Escherichia coli. Cell Microbiol 3:865–871

    CAS  PubMed  Google Scholar 

  • Daniell SJ, Delahay RM, Shaw RK, Hartland EL, Pallen MJ, Booy F, Ebel F, Knutton S, Frankel G (2001b) Coiled-coil domain of enteropathogenic Escherichia coli type III secreted protein EspD is involved in EspA filament-mediated cell attachment and hemolysis. Infect Immun 69:4055–4064

    CAS  PubMed  PubMed Central  Google Scholar 

  • De Nisco NJ, Rivera-Cancel G, Orth K (2018) The biochemistry of sensing: enteric pathogens regulate type III secretion in response to environmental and host cues. MBio 9:e02122-17

    Google Scholar 

  • Delahay RM, Knutton S, Shaw RK, Hartland EL, Pallen MJ, Frankel G (1999) The coiled-coil domain of EspA is essential for the assembly of the type III secretion translocon on the surface of enteropathogenic Escherichia coli. J Biol Chem 274:35969–35974

    CAS  PubMed  Google Scholar 

  • Deng W, Puente JL, Gruenheid S, Li Y, Vallance BA, Vázquez A, Barba J, Ibarra JA, O’Donnell P, Metalnikov P et al (2004) Dissecting virulence: systematic and functional analyses of a pathogenicity island. Proc Natl Acad Sci 101:3597–3602

    CAS  PubMed  Google Scholar 

  • Deng W, Li Y, Hardwidge PR, Frey EA, Pfuetzner RA, Lee S, Gruenheid S, Strynakda NCJ, Puente JL, Finlay BB (2005) Regulation of type III secretion hierarchy of translocators and effectors in attaching and effacing bacterial pathogens. Infect Immun 73:2135–2146

    CAS  PubMed  PubMed Central  Google Scholar 

  • Deng W, Yu HB, Li Y, Finlay BB (2015) SepD/SepL-dependent secretion signals of the type III secretion system translocator proteins in enteropathogenic Escherichia coli. J Bacteriol 197:1263–1275

    CAS  PubMed  PubMed Central  Google Scholar 

  • Desai MS, Seekatz AM, Koropatkin NM, Kamada N, Hickey CA, Wolter M, Pudlo NA, Kitamoto S, Terrapon N, Muller A et al (2016) A dietary fiber-deprived gut microbiota degrades the colonic mucus barrier and enhances pathogen susceptibility. Cell 167(1339–1353):e21

    Google Scholar 

  • Diepold A, Amstutz M, Abel S, Sorg I, Jenal U, Cornelis GR (2010) Deciphering the assembly of the Yersinia type III secretion injectisome. EMBO J 29:1928–1940

    CAS  PubMed  PubMed Central  Google Scholar 

  • Diepold A, Wiesand U, Cornelis GR (2011) The assembly of the export apparatus (YscR, S, T, U, V) of the Yersinia type III secretion apparatus occurs independently of other structural components and involves the formation of an YscV oligomer. Mol Microbiol 82:502–514

    PubMed  Google Scholar 

  • Donnenberg MS, Tacket CO, James SP, Losonsky G, Nataro JP, Wasserman SS, Kaper JB, Levine MM (1993) Role of the eaeA gene in experimental enteropathogenic Escherichia coli infection. J Clin Invest 92:1412–1417

    CAS  PubMed  PubMed Central  Google Scholar 

  • Elliott SJ, Sperandio V, Girón JA, Shin S, Mellies JL, Wainwright L, Hutcheson SW, McDaniel TK, Kaper JB (2000) The locus of enterocyte effacement (LEE)-encoded regulator controls expression of both LEE- and non-LEE-encoded virulence factors in enteropathogenic and enterohemorrhagic Escherichia coli. Infect Immun 68:6115–6126

    CAS  PubMed  PubMed Central  Google Scholar 

  • Feria JM, García-Gómez E, Espinosa N, Minamino T, Namba K, González-Pedrajo B (2012) Role of escp (Orf16) in injectisome biogenesis and regulation of type III protein secretion in enteropathogenic Escherichia coli. J Bacteriol 194:6029–6045

    CAS  Google Scholar 

  • Freedman SB, Xie J, Neufeld MS, Hamilton WL, Hartling L, Tarr PI (2016) Shiga toxin-producing Escherichia coli infection, antibiotics, and risk of developing hemolytic uremic syndrome: a meta-analysis. Clin Infect Dis 62:1251–1258

    PubMed  PubMed Central  Google Scholar 

  • Furniss RCD, Clements A (2017) Regulation of the locus of enterocyte effacement in attaching and effacing pathogens. J Bacteriol JB.00336-17

    Google Scholar 

  • García-Gómez E, Espinosa N, de la Mora J, Dreyfus G, González-Pedrajo B (2011) The muramidase EtgA from enteropathogenic Escherichia coli is required for efficient type III secretion. Microbiology 157:1145–1160

    PubMed  Google Scholar 

  • Gauthier A, Finlay BB (2003) Translocated intimin receptor and its chaperone interact with ATPase of the type III secretion apparatus of enteropathogenic Escherichia coli. J Bacteriol 185:6747–6755

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gaytán MO, Martínez-Santos VI, Soto E, González-Pedrajo B (2016) Type three secretion system in attaching and effacing pathogens. Front Cell Infect Microbiol 6:129

    PubMed  PubMed Central  Google Scholar 

  • Gaytán MO, Monjarás Feria J, Soto E, Espinosa N, Benítez JM, Georgellis D, González-Pedrajo B (2017) Novel insights into the mechanism of SepL-mediated control of effector secretion in enteropathogenic Escherichia coli. Microbiologyopen e00571

    Google Scholar 

  • Gomez-Duarte OG, Kaper JB (1995) A plasmid-encoded regulatory region activates chromosomal eaeA expression in enteropathogenic Escherichia coli. Infect Immun 63:1767–1776

    CAS  PubMed  PubMed Central  Google Scholar 

  • González-Prieto C, Lesser CF (2018) Rationale redesign of type III secretion systems: toward the development of non-pathogenic E. coli for in vivo delivery of therapeutic payloads. Curr Opin Microbiol 41:1–7

    PubMed  Google Scholar 

  • Hodges K, Gill R (2010) Infectious diarrhea: cellular and molecular mechanisms. Gut Microbes 1:4–21

    PubMed  PubMed Central  Google Scholar 

  • Hughes DT, Sperandio V (2008) Inter-kingdom signalling: communication between bacteria and their hosts. Nat Rev Microbiol 6:111–120

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hyma KE, Lacher DW, Nelson AM, Bumbaugh AC, Janda JM, Strockbine NA, Young VB, Whittam TS (2005) Evolutionary genetics of a new pathogenic Escherichia species: Escherichia albertii and related Shigella boydii strains. J Bacteriol 187:619–628

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ibuki T, Imada K, Minamino T, Kato T, Miyata T, Namba K (2011) Common architecture of the flagellar type III protein export apparatus and F- and V-type ATPases. Nat Struct Mol Biol 18:277–282

    CAS  PubMed  Google Scholar 

  • Ide T, Laarmann S, Greune L, Schillers H, Oberleithner H, Schmidt MA (2001) Characterization of translocation pores inserted into plasma membranes by type III-secreted Esp proteins of enteropathogenic Escherichia coli. Cell Microbiol 3:669–679

    CAS  PubMed  Google Scholar 

  • Ide T, Michgehl S, Knappstein S, Heusipp G, Schmidt MA (2003) Differential modulation by Ca2+ of type III secretion of diffusely adhering enteropathogenic Escherichia coli. Infect Immun 71:1725–1732

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ideses D, Gophna U, Paitan Y, Chaudhuri RR, Pallen MJ, Ron EZ (2005) A degenerate type III secretion system from septicemic Escherichia coli contributes to pathogenesis. J Bacteriol 187:8164–8171

    CAS  PubMed  PubMed Central  Google Scholar 

  • Imada K, Minamino T, Tahara A, Namba K (2007) Structural similarity between the flagellar type III ATPase FliI and F1-ATPase subunits. Proc Natl Acad Sci U S A 104:485–490

    CAS  PubMed  PubMed Central  Google Scholar 

  • Iyoda S, Watanabe H (2005) ClpXP protease controls expression of the type III protein secretion system through regulation of RpoS and GrlR levels in enterohemorrhagic Escherichia coli. J Bacteriol 187:4086–4094

    CAS  PubMed  PubMed Central  Google Scholar 

  • Izoré T, Job V, Dessen A (2011) Biogenesis, regulation, and targeting of the type III secretion system. Structure 19:603–612

    PubMed  Google Scholar 

  • Jimenez R, Cruz-Migoni SB, Huerta-Saquero A, Bustamante VH, Puente JL (2010) Molecular characterization of GrlA, a specific positive regulator of ler expression in enteropathogenic Escherichia coli. J Bacteriol 192:4627–4642

    CAS  PubMed  PubMed Central  Google Scholar 

  • Journet L, Agrain C, Broz P, Cornelis GR (2003) The needle length of bacterial injectisomes is determined by a molecular ruler. Science (80-) 302:1757–1760

    CAS  PubMed  Google Scholar 

  • Kenny B, Abe A, Stein M, Finlay BB (1997) Enteropathogenic Escherichia coli protein secretion is induced in response to conditions similar to those in the gastrointestinal tract. Infect Immun 65:2606–2612

    CAS  PubMed  PubMed Central  Google Scholar 

  • Knutton S, Rosenshine I, Pallen MJ, Nisan I, Neves BC, Bain C, Wolff C, Dougan G (1998) A novel EspA-associated surface organelle of enteropathogenic Escherichia coli involved in protein translocation into epithelial cells. EMBO J 17:2166–2176

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kosek M, Bern C, Guerrant RL (2003) The global burden of diarrhoeal disease, as estimated from studies published between 1992 and 2000. Bull World Health Organ 81:197–204

    PubMed  PubMed Central  Google Scholar 

  • Kubori T, Matsushima Y, Nakamura D, Uralil J, Lara-Tejero M, Sukhan A, Galán JE, Aizawa SI (1998) Supramolecular structure of the Salmonella typhimurium type III protein secretion system. Science 280:602–605

    CAS  PubMed  Google Scholar 

  • Lara-Tejero M, Kato J, Wagner S, Liu X, Galán JE (2011) A sorting platform determines the order of protein secretion in bacterial type III systems. Science 331:1188–1191

    CAS  PubMed  Google Scholar 

  • Larzábal M, Mercado EC, Vilte DA, Salazar-González H, Cataldi A, Navarro-Garcia F (2010) Designed coiled-coil peptides inhibit the type three secretion system of enteropathogenic Escherichia coli. PLoS ONE 5

    Google Scholar 

  • Law RJ, Gur-Arie L, Rosenshine I, Brett Finlay B (2013) In vitro and in vivo model systems for studying enteropathogenic Escherichia coli infections. Cold Spring Harb Perspect Med 3:a009977

    PubMed  PubMed Central  Google Scholar 

  • Le Gouëllec A, Chauchet X, Laurin D, Aspord C, Verove J, Wang Y, Genestet C, Trocme C, Ahmadi M, Martin S et al (2013) A safe bacterial microsyringe for in vivo antigen delivery and immunotherapy. Mol Ther 21:1076–1086

    PubMed  PubMed Central  Google Scholar 

  • Litvak Y, Sharon S, Hyams M, Zhang L, Kobi S, Katsowich N, Dishon S, Nussbaum G, Dong N, Shao F et al (2017) Epithelial cells detect functional type III secretion system of enteropathogenic Escherichia coli through a novel NF-κB signaling pathway. PLoS Pathog 13:e1006472

    PubMed  PubMed Central  Google Scholar 

  • Liu L, Oza S, Hogan D, Perin J, Rudan I, Lawn JE, Cousens S, Mathers C, Black RE (2015) Global, regional, and national causes of child mortality in 2000–13, with projections to inform post-2015 priorities: an updated systematic analysis. Lancet 385:430–440

    PubMed  Google Scholar 

  • Lorenz C, Hausner J, Büttner D (2012) HrcQ provides a docking site for early and late type III secretion substrates from Xanthomonas. PLoS ONE 7

    Google Scholar 

  • Loureiro I, Frankel G, Adu-Bobie J, Dougan G, Trabulsi LR, Carneiro-Sampaio MM (1998) Human colostrum contains IgA antibodies reactive to enteropathogenic Escherichia coli virulence-associated proteins: intimin, BfpA, EspA, and EspB. J Pediatr Gastroenterol Nutr 27:166–171

    CAS  PubMed  Google Scholar 

  • Luzader DH, Willsey GG, Wargo MJ, Kendall MM (2016) The ETT2-encoded regulator EtrB modulates enterohemorrhagic Escherichia coli virulence gene expression. Infect Immun 84:2555–2565

    CAS  PubMed  PubMed Central  Google Scholar 

  • Martínez-Santos VI, Medrano-López A, Saldaña Z, Girón JA, Puente JL (2012) Transcriptional regulation of the ecp operon by EcpR, IHF, and H-NS in attaching and effacing Escherichia coli. J Bacteriol 194:5020–5033

    PubMed  PubMed Central  Google Scholar 

  • McNeilly TN, Mitchell MC, Corbishley A, Nath M, Simmonds H, McAteer SP, Mahajan A, Low JC, Smith DGE, Huntley JF et al (2015) Optimizing the protection of cattle against Escherichia coli O157:H7 colonization through immunization with different combinations of H7 flagellin, Tir, intimin-531 or EspA. PLoS ONE 10:1–19

    Google Scholar 

  • Mcshan AC, Guzman RN De (2015) The bacterial type III secretion system as a target for developing new antibiotics. Chem Biol Drug Des 85:30–42

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mellies JL, Elliott SJ, Sperandio V, Donnenberg MS, Kaper JB (1999) The Per regulon of enteropathogenic Escherichia coli: identification of a regulatory cascade and a novel transcriptional activator, the locus of enterocyte effacement (LEE)-encoded regulator (Ler). Mol Microbiol 33:296–306

    CAS  PubMed  Google Scholar 

  • Mellies JL, Navarro-Garcia F, Okeke I, Frederickson J, Nataro JP, Kaper JB (2001) espC pathogenicity island of enteropathogenic Escherichia coli encodes an enterotoxin. Infect Immun 69:315–324

    CAS  PubMed  PubMed Central  Google Scholar 

  • Miletic S, Hünerberg M, Kaldis A, MacDonald J, Leuthreau A, McAllister T, Menassa R (2017) A plant-produced candidate subunit vaccine reduces shedding of enterohemorrhagic Escherichia coli in ruminants. Biotechnol J 12:1–9

    Google Scholar 

  • Milon A, Oswald E, De Rycke J (1999) Rabbit EPEC: a model for the study of enteropathogenic Escherichia coli. Vet Res 30:203–219

    CAS  PubMed  Google Scholar 

  • Minamino T, Saijo-Hamano Y, Furukawa Y, González-Pedrajo B, Macnab RM, Namba K (2004) Domain organization and function of Salmonella FliK, a flagellar hook-length control protein. J Mol Biol 341:491–502

    CAS  PubMed  Google Scholar 

  • Moreira CG, Russell R, Mishra AA, Narayanan S, Ritchie JM, Waldor MK, Curtis MM, Winter SE, Weinshenker D, Sperandio V (2016) Bacterial adrenergic sensors regulate virulence of enteric pathogens in the gut. MBio 7:e00826-16

    Google Scholar 

  • Navarro-Garcia F, Serapio-Palacios A, Vidal JE, Isabel Salazar M, Tapia-Pastrana G (2014) EspC promotes epithelial cell detachment by enteropathogenic Escherichia coli via sequential cleavages of a cytoskeletal protein and then focal adhesion proteins. Infect Immun 82:2255–2265

    PubMed  PubMed Central  Google Scholar 

  • Neves BC, Shaw RK, Frankel G, Knutton S (2003a) Polymorphisms within Espa filaments of enteropathogenic and enterohemorrhagic Escherichia coli. Infect Immun 71:2262–2265

    CAS  PubMed  PubMed Central  Google Scholar 

  • Neves BC, Mundy R, Petrovska L, Dougan G, Knutton S, Frankel G (2003b) CesD2 of enteropathogenic Escherichia coli is a second chaperone for the type III secretion translocator protein EspD. Infect Immun 71:2130–2141

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nguyen Y, Sperandio V (2012) Enterohemorrhagic E. coli (EHEC) pathogenesis. Front Cell Infect Microbiol 2:1–7

    Google Scholar 

  • Notti RQ, Bhattacharya S, Lilic M, Stebbins CE (2015) A common assembly module in injectisome and flagellar type III secretion sorting platforms. Nat Commun 6:7125

    PubMed  PubMed Central  Google Scholar 

  • O’Connell CB, Creasey EA, Knutton S, Elliott S, Crowther LJ, Luo W, John Albert M, Kaper JB, Frankel G, Donnenberg MS (2004) SepL, a protein required for enteropathogenic Escherichia coli type III translocation, interacts with secretion component SepD. Mol Microbiol 52:1613–1625

    PubMed  Google Scholar 

  • Ogino T, Ohno R, Sekiya K, Kuwae A, Matsuzawa T, Nonaka T, Fukuda H, Imajoh-ohmi S, Abe A (2006) Assembly of the type III secretion apparatus of enteropathogenic Escherichia coli. J Bacteriol 188:2801–2811

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ooka T, Ogura Y, Katsura K, Seto K, Kobayashi H, Kawano K, Tokuoka E, Furukawa M, Harada S, Yoshino S et al (2015) Defining the genome features of Escherichia albertii, an emerging enteropathogen closely related to Escherichia coli. Genome Biol Evol 7:3170–3179

    PubMed  PubMed Central  Google Scholar 

  • O’Ryan M, Vidal R, del Canto F, Salazar JC, Montero D (2015) Vaccines for viral and bacterial pathogens causing acute gastroenteritis: Part I: Overview, vaccines for enteric viruses and Vibrio cholerae. Hum Vaccin Immunother 11:584–600

    PubMed  PubMed Central  Google Scholar 

  • Osawa K, Shibata M, Nishiyama Y, Kurokawa M, Yamamoto G, Kinoshita S, Kataoka N (2006) Identification of the ETT2 locus in human diarrheagenic Escherichia coli by multiplex PCR. J Infect Chemother 12:157–159

    CAS  PubMed  Google Scholar 

  • Pacheco AR, Curtis MM, Ritchie JM, Munera D, Waldor MK, Moreira CG, Sperandio V (2012) Fucose sensing regulates bacterial intestinal colonization. Nature 492:113–117

    CAS  PubMed  PubMed Central  Google Scholar 

  • Padavannil A, Jobichen C, Mills E, Velazquez-Campoy A, Li M, Leung KY, Mok YK, Rosenshine I, Sivaraman J (2013) Structure of GrlR–GrlA complex that prevents GrlA activation of virulence genes. Nat Commun 4:2–11

    Google Scholar 

  • Pallen MJ, Beatson SA, Bailey CM (2005) Bioinformatics analysis of the locus for enterocyte effacement provides novel insights into type-III secretion. BMC Microbiol 5:9

    PubMed  PubMed Central  Google Scholar 

  • Petty NK, Feltwell T, Pickard D, Clare S, Toribio AL, Fookes M, Roberts K, Monson R, Nair S, Kingsley RA et al (2011) Citrobacter rodentium is an unstable pathogen showing evidence of significant genomic flux. PLoS Pathog 7

    Google Scholar 

  • Potter AA, Klashinsky S, Li Y, Frey E, Townsend H, Rogan D, Erickson G, Hinkley S, Klopfenstein T, Moxley RA et al (2004) Decreased shedding of Escherichia coli O157:H7 by cattle following vaccination with type III secreted proteins. Vaccine 22:362–369

    CAS  PubMed  Google Scholar 

  • Ren CP, Chaudhuri RR, Fivian A, Bailey CM, Antonio M, Barnes WM, Pallen MJ (2004) The ETT2 gene cluster, encoding a second type III secretion system from Escherichia coli, is present in the majority of strains but has undergone widespread mutational attrition. J Bacteriol 186:3547–3560

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ritchie JM (2014) Animal models of enterohemorrhagic Escherichia coli infection. Microbiol, Spectr, p 2

    Google Scholar 

  • Romo-Castillo M, Andrade A, Espinosa N, Feria JM, Soto E, Díaz-Guerrero M, González-Pedrajo B (2014) EscO, a functional and structural analog of the flagellar fliJ protein, is a positive regulator of EscN ATPase activity of the enteropathogenic Escherichia coli injectisome. J Bacteriol 196:2227–2241

    PubMed  PubMed Central  Google Scholar 

  • Ruano-Gallego D, Álvarez B, Fernández LÁ (2015) Engineering the controlled assembly of filamentous injectisomes in E. coli K-12 for protein translocation into mammalian cells. ACS Synth Biol 4:1030–1041

    CAS  PubMed  PubMed Central  Google Scholar 

  • Russell RM, Sharp FC, Rasko DA, Sperandio V (2007) QseA and GrlR/GrlA regulation of the locus of enterocyte effacement genes in enterohemorrhagic Escherichia coli. J Bacteriol 189:5387–5392

    CAS  PubMed  PubMed Central  Google Scholar 

  • Salinger N, Kokona B, Fairman R, Okeke IN (2009) The plasmid-encoded regulator activates factors conferring lysozyme resistance on enteropathogenic Escherichia coli strains. Appl Environ Microbiol 75:275–280

    CAS  PubMed  Google Scholar 

  • Sal-Man N, Deng W, Finlay BB (2012) EscI: a crucial component of the type III secretion system forms the inner rod structure in enteropathogenic Escherichia coli. Biochem J 442:119–125

    CAS  PubMed  Google Scholar 

  • Sal-Man N, Setiaputra D, Scholz R, Deng W, Yu ACY, Strynadka NCJ, Finlay BB (2013) EscE and EscG are cochaperones for the type III needle protein EscF of enteropathogenic Escherichia coli. J Bacteriol 195:2481–2489

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schauer DB, Zabel BA, Pedraza IF, O’Hara CM, Steigerwalt AG, Brenner DJ (1995) Genetic and biochemical characterization of Citrobacter rodentium sp. nov. J Clin Microbiol 33:2064–2068

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sekiya K, Ohishi M, Ogino T, Tamano K, Sasakawa C, Abe A (2001) Supermolecular structure of the enteropathogenic Escherichia coli type III secretion system and its direct interaction with the EspA-sheath-like structure. Proc Natl Acad Sci U S A 98:11638–11643

    CAS  Google Scholar 

  • Shaulov L, Gershberg J, Deng W, Finlay BB, Sal-Man N (2017) The ruler protein EscP of the enteropathogenic Escherichia coli type III secretion system is involved in calcium sensing and secretion hierarchy regulation by interacting with the gatekeeper protein SepL. MBio 8:1–15

    Google Scholar 

  • Shaw RK, Cleary J, Murphy MS, Frankel G, Knutton S (2005) Interaction of enteropathogenic Escherichia coli with human intestinal mucosa: role of effector proteins in brush border remodeling and formation of attaching and effacing lesions. Infect Immun 73(2):1243–1251. https://doi.org/10.1128/IAI.73.2.1243-1251.2005

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shi L, Yu B, Cai C-H, Huang J-D (2016) Angiogenic inhibitors delivered by the type III secretion system of tumor-targeting Salmonella typhimurium safely shrink tumors in mice. AMB Express 6:56

    PubMed  PubMed Central  Google Scholar 

  • Snyder JD, Merson MH (1982) The magnitude of the global problem of acute diarrhoeal disease: a review of active surveillance data. Bull World Health Organ 60:605–613

    CAS  PubMed  PubMed Central  Google Scholar 

  • Soto E, Espinosa N, Díaz-Guerrero M, Gaytán MO, Puente JL, González-Pedrajo B (2017) Functional characterization of EscK (Orf4), a sorting platform component of the enteropathogenic Escherichia coli injectisome. J Bacteriol 199

    Google Scholar 

  • Sperandio V, Mellies JL, Nguyen W, Shin S, Kaper JB (1999) Quorum sensing controls expression of the type III secretion gene transcription and protein secretion in enterohemorrhagic and enteropathogenic Escherichia coli. Proc Natl Acad Sci U S A 96:15196–15201

    CAS  PubMed  PubMed Central  Google Scholar 

  • Su MSW, Kao HC, Lin CN, Syu WJ (2008) Gene l0017 encodes a second chaperone for EspA of enterohaemorrhagic Escherichia coli O157: H7. Microbiology 154:1094–1103

    CAS  PubMed  Google Scholar 

  • Tacket CO, Sztein MB, Losonsky G, Abe A, Finlay BB, McNamara BP, Fantry GT, James SP, Nataro JP, Levine MM, Donnenberg MS (2000) Role of EspB in experimental human enteropathogenic Escherichia coli infection. Infect Immun 68(6):3689–3695

    CAS  PubMed  PubMed Central  Google Scholar 

  • Thomas J, Stafford GP, Hughes C (2004) Docking of cytosolic chaperone-substrate complexes at the membrane ATPase during flagellar type III protein export. Proc Natl Acad Sci U S A 101:3945–3950

    CAS  PubMed  PubMed Central  Google Scholar 

  • Thomas NA, Deng W, Baker N, Puente J, Finlay BB (2007) Hierarchical delivery of an essential host colonization factor in enteropathogenic Escherichia coli. J Biol Chem 282:29634–29645

    CAS  PubMed  Google Scholar 

  • Umanski T, Rosenshine I, Friedberg D (2002) Thermoregulated expression of virulence genes in enteropathogenic Escherichia coli. Microbiology 148:2735–2744

    CAS  PubMed  Google Scholar 

  • Vilte DA, Larzábal M, Cataldi ÁA, Mercado EC (2008) Bovine colostrum contains immunoglobulin G antibodies against intimin, EspA, and EspB and inhibits hemolytic activity mediated by the type three secretion system of attaching and effacing Escherichia coli. Clin Vaccine Immunol 15:1208–1213

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wagner S, Königsmaier L, Lara-Tejero M, Lefebre M, Marlovits TC, Galán JE (2010) Organization and coordinated assembly of the type III secretion export apparatus. Proc Natl Acad Sci U S A 107:17745–17750

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wainwright LA, Kaper JB (1998) EspB and EspD require a specific chaperone for proper secretion from enteropathogenic Escherichia coli. Mol Microbiol 27:1247–1260

    CAS  PubMed  Google Scholar 

  • Wang D, Roe AJ, McAteer S, Shipston MJ, Gally DL (2008) Hierarchal type III secretion of translocators and effectors from Escherichia coli O157:H7 requires the carboxy terminus of SepL that binds to Tir. Mol Microbiol 69:1499–1512

    CAS  PubMed  Google Scholar 

  • Wang S, Liu X, Xu X, Yang D, Wang D, Han X, Shi Y, Tian M, Ding C, Peng D et al (2016) Escherichia coli type III secretion system 2 ATPase EivC Is involved in the motility and virulence of avian pathogenic Escherichia coli. Front Microbiol 7:1–14

    Google Scholar 

  • Wang S, Xu X, Liu X, Wang D, Liang H, Wu X, Tian M, Ding C, Wang G, Yu S (2017) Escherichia coli type III secretion system 2 regulator EtrA promotes virulence of avian pathogenic Escherichia coli. Microbiology (United Kingdom) 163:1515–1524

    CAS  Google Scholar 

  • Winardhi RS, Gulvady R, Mellies JL, Yan J (2014) Locus of enterocyte effacement-encoded regulator (Ler) of pathogenic Escherichia coli competes off histone-like nucleoid-structuring protein (H-NS) through noncooperative DNA binding. J Biol Chem 289:13739–13750

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wong AR, Pearson JS, Bright MD, Munera D, Robinson KS, Lee SF, Frankel G, Hartland EL (2011) Enteropathogenic and enterohaemorrhagic Escherichia coli: even more subversive elements. Mol Microbiol 80(6):1420–1438. https://doi.org/10.1111/j.1365-2958.2011.07661.x. Epub 2011 May 5

    CAS  PubMed  Google Scholar 

  • Wood SE, Jin J, Lloyd SA (2008) YscP and YscU switch the substrate specificity of the Yersinia type III secretion system by regulating export of the inner rod protein YscI. J Bacteriol 190:4252–4262

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yip CK, Finlay BB, Strynadka NCJ (2005) Structural characterization of a type III secretion system filament protein in complex with its chaperone. Nat Struct Mol Biol 12:75–81

    CAS  PubMed  Google Scholar 

  • Zarivach R, Vuckovic M, Deng W, Finlay BB, Strynadka NCJ (2007) Structural analysis of a prototypical ATPase from the type III secretion system. Nat Struct Mol Biol 14:131–137

    CAS  PubMed  Google Scholar 

  • Zhang L, Chaudhuri RR, Hobman JL, Patel MD, Antony C, Sarti D, Roe AJ, Vlisidou I, Shaw RK, Falciani F et al (2004) Regulators encoded in the Escherichia coli type III secretion system 2 gene cluster influence exression of genes withing the locus of enterocyte effacement in Enterohemorrhagic E. coli O157:H7. Infect Immun 72:7282–7293

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou M, Guo Z, Duan Q, Hardwidge PR, Zhu G (2014) Escherichia coli type III secretion system 2: a new kind of T3SS? Vet Res 45:32

    PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Life Sciences, MRC Centre for Molecular Bacteriology and Infection, Imperial College London, London, UK

    Sabrina L. Slater, Agnes M. Sågfors, Dominic J. Pollard, David Ruano-Gallego & Gad Frankel

Authors
  1. Sabrina L. Slater
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Agnes M. Sågfors
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Dominic J. Pollard
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. David Ruano-Gallego
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Gad Frankel
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Gad Frankel .

Editor information

Editors and Affiliations

  1. Department of Life Sciences, Imperial College London, London, UK

    Gad Frankel

  2. Faculty of Life Sciences, Tel Aviv University, Tel Aviv, Israel

    Eliora Z Ron

Rights and permissions

Reprints and permissions

Copyright information

© 2018 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Slater, S.L., Sågfors, A.M., Pollard, D.J., Ruano-Gallego, D., Frankel, G. (2018). The Type III Secretion System of Pathogenic Escherichia coli. In: Frankel, G., Ron, E. (eds) Escherichia coli, a Versatile Pathogen. Current Topics in Microbiology and Immunology, vol 416. Springer, Cham. https://doi.org/10.1007/82_2018_116

Download citation

Publish with us

Policies and ethics

Search

Navigation