Skip to main content

Host Innate Immune Factors Influencing Enterohemorrhagic Escherichia coli Pathogenicity

  • Chapter
  • First Online:
Foodborne Pathogens

Part of the book series: Food Microbiology and Food Safety ((PRACT))

  • 1638 Accesses

Abstract

Enterohemorrhagic Escherichia coli (EHEC) is a significant foodborne attaching and effacing (A/E) pathogen that causes diarrhea, hemorrhagic colitis and the hemolytic-uremic syndrome (HUS) in humans. EHEC is closely related to enteropathogenic E. coli (EPEC) and both induce characteristic A/E lesions on the gut mucosal surface. During EHEC and EPEC infection, host innate immune responses, such as inflammation and cell death are rapidly activated, upon the detection of bacterial components and virulence factor activity. To promote A/E lesion formation and dissemination of the pathogen in the body, EHEC and EPEC deliver a repertoire of effector proteins, including Tir, NleA/EspI and NleB to -H, to the host cell cytosol via a type III secretion system (T3SS). These interfere with a range of host cell processes, including host defense mechanisms. Several T3SS effector proteins specifically modify or cleave host proteins involved in inflammation and cell death, thereby inactivating these pathways. The identification of the host targets and the characterization of the biochemical function of T3SS effectors have greatly contributed to understanding the pathogenesis of EHEC and EPEC infections.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 149.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 199.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
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

Abbreviations

A/E pathogen:

Attaching/effacing pathogen

AP-1:

Activation protein-1

BI-1:

Bax inhibitor-1

CLR:

C-type lection receptor

CRL:

Cullin Ring E3 ligases

DC:

Dendritic cell

DD:

Death domains

DISC:

Death-inducing signaling complex

EHEC:

Enterohemorrhagic Escherichia coli

FA:

Focal adhesion

GlcNAc:

N-acetylglucosamine

HUS:

Hemolytic uremic syndrome

IE:

Integrative element

ILK:

Integrin-linked kinase

ITIM:

Immunoreceptor tyrosine-based inhibitory motifs

LEE:

Locus of enterocyte effacement

LPS:

Lipopolysaccharide

MAPK:

Mitogen-activated protein kinase

MTS:

Mitochondrial targeting sequence

NF-κB:

Nuclear-factor κB

NLR:

NOD-like receptor

NZF:

Npl4 Zinc figure

OI:

O-island

PAMPs:

Pathogen-associated molecular patterns

PKC:

Protein kinase C

PRRs:

Pattern recognition receptors

RLR:

RIG-I-like receptor

SAM:

S-adenosyl-L-methionine

Stx:

Shiga toxins

T3SS:

Type III secretion system

TAB2 and TAB3:

TAK1-binding proteins 2 and 3

TAD:

Transcription activation domain

TIM17b:

Translocase of inner mitochondrial membrane 17b

Tir:

Translocated intimin receptor

TLR:

Toll-like receptor

TNFR1:

Tumor necrosis factor receptor 1

TRAIL:

TNF-associated apoptosis-inducing ligand

References

  • Akira, S., Uematsu, S., & Takeuchi, O. (2006). Pathogen recognition and innate immunity. Cell, 124(4), 783–801.

    Article  CAS  PubMed  Google Scholar 

  • Barnett Foster, D., et al. (2000). Enterohemorrhagic Escherichia coli induces apoptosis which augments bacterial binding and phosphatidylethanolamine exposure on the plasma membrane outer leaflet. Infection and Immunity, 68(6), 3108–3115.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baruch, K., et al. (2011). Metalloprotease type III effectors that specifically cleave JNK and NF-kappaB. The EMBO Journal, 30(1), 221–231.

    Article  CAS  PubMed  Google Scholar 

  • Berger, C. N., et al. (2012). EspZ of enteropathogenic and enterohemorrhagic Escherichia coli regulates type III secretion system protein translocation. MBio, 3(5), e00317–e00312.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Berin, M. C., et al. (2002). Role of EHEC O157:H7 virulence factors in the activation of intestinal epithelial cell NF-kappaB and MAP kinase pathways and the upregulated expression of interleukin 8. Cellular Microbiology, 4(10), 635–648.

    Article  CAS  PubMed  Google Scholar 

  • Blasche, S., et al. (2013). The E. coli effector protein NleF is a caspase inhibitor. PloS One, 8(3), e58937.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boyce, T. G., Swerdlow, D. L., & Griffin, P. M. (1995). Escherichia coli O157:H7 and the hemolytic-uremic syndrome. The New England Journal of Medicine, 333(6), 364–368.

    Article  CAS  PubMed  Google Scholar 

  • Callaway, T. R., et al. (2009). Diet, Escherichia coli O157:H7, and cattle: A review after 10 years. Current Issues in Molecular Biology, 11(2), 67–79.

    CAS  PubMed  Google Scholar 

  • Crow, A., et al. (2012). The molecular basis of ubiquitin-like protein NEDD8 deamidation by the bacterial effector protein Cif. Proceedings of the National Academy of Sciences of the United States of America, 109(27), E1830–E1838.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cui, J., et al. (2010). Glutamine deamidation and dysfunction of ubiquitin/NEDD8 induced by a bacterial effector family. Science, 329(5996), 1215–1218.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dean, P., et al. (2010). The enteropathogenic E. coli effector EspF targets and disrupts the nucleolus by a process regulated by mitochondrial dysfunction. PLoS Pathogens, 6(6), e1000961.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Deng, W., et al. (2004). Dissecting virulence: Systematic and functional analyses of a pathogenicity island. Proceedings of the National Academy of Sciences of the United States of America, 101(10), 3597–3602.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Durso, L. M., et al. (2005). Shiga-toxigenic Escherichia coli O157:H7 infections among livestock exhibitors and visitors at a Texas County fair. Vector Borne and Zoonotic Diseases, 5(2), 193–201.

    Article  PubMed  Google Scholar 

  • Elliott, S. J., et al. (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. Infection and Immunity, 68(11), 6115–6126.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Endo, Y., et al. (1988). Site of action of a Vero toxin (VT2) from Escherichia coli O157:H7 and of Shiga toxin on eukaryotic ribosomes. RNA N-glycosidase activity of the toxins. European Journal of Biochemistry, 171(1–2), 45–50.

    Article  CAS  PubMed  Google Scholar 

  • Feng, P. C., & Reddy, S. (2013). Prevalences of Shiga toxin subtypes and selected other virulence factors among Shiga-toxigenic Escherichia coli strains isolated from fresh produce. Applied and Environmental Microbiology, 79(22), 6917–6923.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Feuerbacher, L. A., & Hardwidge, P. R. (2014). Influence of NleH effector expression, host genetics, and inflammation on Citrobacter rodentium colonization of mice. Microbes and Infection, 16(5), 429–433.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Frankel, G., et al. (1998). Enteropathogenic and enterohaemorrhagic Escherichia coli: More subversive elements. Molecular Microbiology, 30(5), 911–921.

    Article  CAS  PubMed  Google Scholar 

  • From the Centers for Disease Control and Prevention. (1995). Escherichia coli O157:H7 outbreak linked to commercially distributed dry-cured salami – Washington and California, 1994. JAMA, 273(13), 985–986.

    Article  Google Scholar 

  • Gao, X., et al. (2009). Bacterial effector binding to ribosomal protein s3 subverts NF-kappaB function. PLoS Pathogens, 5(12), e1000708.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gao, X., et al. (2013). NleB, a bacterial effector with glycosyltransferase activity, targets GAPDH function to inhibit NF-kappaB activation. Cell Host & Microbe, 13(1), 87–99.

    Article  CAS  Google Scholar 

  • Ghosh, S., May, M. J., & Kopp, E. B. (1998). NF-kappa B and Rel proteins: Evolutionarily conserved mediators of immune responses. Annual Review of Immunology, 16, 225–260.

    Article  CAS  PubMed  Google Scholar 

  • Giogha, C., et al. (2015). Substrate recognition by the zinc metalloprotease effector NleC from enteropathogenic Escherichia coli. Cellular Microbiology, 17, 1766–1778.

    Article  CAS  PubMed  Google Scholar 

  • Hayden, M. S., & Ghosh, S. (2008). Shared principles in NF-kappaB signaling. Cell, 132(3), 344–362.

    Article  CAS  PubMed  Google Scholar 

  • Hemrajani, C., et al. (2008). Role of NleH, a type III secreted effector from attaching and effacing pathogens, in colonization of the bovine, ovine, and murine gut. Infection and Immunity, 76(11), 4804–4813.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hemrajani, C., et al. (2010). NleH effectors interact with Bax inhibitor-1 to block apoptosis during enteropathogenic Escherichia coli infection. Proceedings of the National Academy of Sciences of the United States of America, 107(7), 3129–3134.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hurley, B. P., Thorpe, C. M., & Acheson, D. W. (2001). Shiga toxin translocation across intestinal epithelial cells is enhanced by neutrophil transmigration. Infection and Immunity, 69(10), 6148–6155.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Iguchi, A., et al. (2009). Complete genome sequence and comparative genome analysis of enteropathogenic Escherichia coli O127:H6 strain E2348/69. Journal of Bacteriology, 191(1), 347–354.

    Article  CAS  PubMed  Google Scholar 

  • Imtiyaz, H. Z., Zhang, Y., & Zhang, J. (2005). Structural requirements for signal-induced target binding of FADD determined by functional reconstitution of FADD deficiency. The Journal of Biological Chemistry, 280(36), 31360–31367.

    Article  CAS  PubMed  Google Scholar 

  • Johnson, G. L., & Lapadat, R. (2002). Mitogen-activated protein kinase pathways mediated by ERK, JNK, and p38 protein kinases. Science, 298(5600), 1911–1912.

    Article  CAS  PubMed  Google Scholar 

  • Kanack, K. J., et al. (2005). SepZ/EspZ is secreted and translocated into HeLa cells by the enteropathogenic Escherichia coli type III secretion system. Infection and Immunity, 73(7), 4327–4337.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaper, J. B., Nataro, J. P., & Mobley, H. L. (2004). Pathogenic Escherichia coli. Nature Reviews. Microbiology, 2(2), 123–140.

    Article  CAS  PubMed  Google Scholar 

  • Karmali, M. A., et al. (1983). Sporadic cases of haemolytic-uraemic syndrome associated with faecal cytotoxin and cytotoxin-producing Escherichia coli in stools. Lancet, 1(8325), 619–620.

    Article  CAS  PubMed  Google Scholar 

  • Karmali, M. A., Gannon, V., & Sargeant, J. M. (2010). Verocytotoxin-producing Escherichia coli (VTEC). Veterinary Microbiology, 140(3–4), 360–370.

    Article  CAS  PubMed  Google Scholar 

  • Kashiwamura, M., et al. (2009). Shiga toxin kills epithelial cells isolated from distal but not proximal part of mouse colon. Biological & Pharmaceutical Bulletin, 32(9), 1614–1617.

    Article  CAS  Google Scholar 

  • Kelly, M., et al. (2006). Essential role of the type III secretion system effector NleB in colonization of mice by Citrobacter rodentium. Infection and Immunity, 74(4), 2328–2337.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kenny, B., & Jepson, M. (2000). Targeting of an enteropathogenic Escherichia coli (EPEC) effector protein to host mitochondria. Cellular Microbiology, 2(6), 579–590.

    Article  CAS  PubMed  Google Scholar 

  • Khan, M. A., et al. (2006). Toll-like receptor 4 contributes to colitis development but not to host defense during Citrobacter rodentium infection in mice. Infection and Immunity, 74(5), 2522–2536.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim, D. W., et al. (2005). The Shigella flexneri effector OspG interferes with innate immune responses by targeting ubiquitin-conjugating enzymes. Proceedings of the National Academy of Sciences of the United States of America, 102(39), 14046–14051.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim, M., et al. (2009). Bacteria hijack integrin-linked kinase to stabilize focal adhesions and block cell detachment. Nature, 459(7246), 578–582.

    Article  CAS  PubMed  Google Scholar 

  • Li, S., et al. (2013). Pathogen blocks host death receptor signalling by arginine GlcNAcylation of death domains. Nature, 501(7466), 242–246.

    Article  CAS  PubMed  Google Scholar 

  • Liu, S., & Chen, Z. J. (2011). Expanding role of ubiquitination in NF-kappaB signaling. Cell Research, 21(1), 6–21.

    Article  PubMed  CAS  Google Scholar 

  • Lupfer, C. R., et al. (2014). Reactive oxygen species regulate caspase-11 expression and activation of the non-canonical NLRP3 inflammasome during enteric pathogen infection. PLoS Pathogens, 10(9), e1004410.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ma, C., et al. (2006). Citrobacter rodentium infection causes both mitochondrial dysfunction and intestinal epithelial barrier disruption in vivo: Role of mitochondrial associated protein (Map). Cellular Microbiology, 8(10), 1669–1686.

    Article  CAS  PubMed  Google Scholar 

  • Manning, S. D., et al. (2008). Variation in virulence among clades of Escherichia coli O157:H7 associated with disease outbreaks. Proceedings of the National Academy of Sciences of the United States of America, 105(12), 4868–4873.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marches, O., et al. (2003). Enteropathogenic and enterohaemorrhagic Escherichia coli deliver a novel effector called Cif, which blocks cell cycle G2/M transition. Molecular Microbiology, 50(5), 1553–1567.

    Article  CAS  PubMed  Google Scholar 

  • Marches, O., et al. (2005). Characterization of two non-locus of enterocyte effacement-encoded type III-translocated effectors, NleC and NleD, in attaching and effacing pathogens. Infection and Immunity, 73(12), 8411–8417.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McCormack, R. M., et al. (2015). Enteric pathogens deploy cell cycle inhibiting factors to block the bactericidal activity of Perforin-2. eLife, 4, e06505.

    PubMed  PubMed Central  Google Scholar 

  • McDaniel, T. K., et al. (1995). A genetic locus of enterocyte effacement conserved among diverse enterobacterial pathogens. Proceedings of the National Academy of Sciences of the United States of America, 92(5), 1664–1668.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mead, P. S., & Griffin, P. M. (1998). Escherichia coli O157:H7. Lancet, 352(9135), 1207–1212.

    Article  CAS  PubMed  Google Scholar 

  • Miyamoto, Y., et al. (2006). Role of Shiga toxin versus H7 flagellin in enterohaemorrhagic Escherichia coli signalling of human colon epithelium in vivo. Cellular Microbiology, 8(5), 869–879.

    Article  CAS  PubMed  Google Scholar 

  • Morita-Ishihara, T., et al. (2013). EspO1-2 regulates EspM2-mediated RhoA activity to s(43): p. 30101-13. Tabilize formation of focal adhesions in enterohemorrhagic Escherichia coli-infected host cells. PloS One, 8(2), e55960.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Muhlen, S., Ruchaud-Sparagano, M. H., & Kenny, B. (2011). Proteasome-independent degradation of canonical NFkappaB complex components by the NleC protein of pathogenic Escherichia coli. The Journal of Biological Chemistry, 286(7), 5100–5107.

    Article  PubMed  CAS  Google Scholar 

  • Mukaida, N., Mahe, Y., & Matsushima, K. (1990). Cooperative interaction of nuclear factor-kappa B- and cis-regulatory enhancer binding protein-like factor binding elements in activating the interleukin-8 gene by pro-inflammatory cytokines. The Journal of Biological Chemistry, 265(34), 21128–21133.

    CAS  PubMed  Google Scholar 

  • Mukaida, N., et al. (1994). Molecular mechanism of interleukin-8 gene expression. Journal of Leukocyte Biology, 56(5), 554–558.

    CAS  PubMed  Google Scholar 

  • Muthing, J., et al. (2009). Shiga toxins, glycosphingolipid diversity, and endothelial cell injury. Thrombosis and Haemostasis, 101(2), 252–264.

    PubMed  Google Scholar 

  • Nadler, C., et al. (2010). The type III secretion effector NleE inhibits NF-kappaB activation. PLoS Pathogens, 6(1), e1000743.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Neel, B. G., Gu, H., & Pao, L. (2003). The 'Shp'ing news: SH2 domain-containing tyrosine phosphatases in cell signaling. Trends in Biochemical Sciences, 28(6), 284–293.

    Article  CAS  PubMed  Google Scholar 

  • Newton, H. J., et al. (2010). The type III effectors NleE and NleB from enteropathogenic E. coli and OspZ from Shigella block nuclear translocation of NF-kappaB p65. PLoS Pathogens, 6(5), e1000898.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nordlander, S., Pott, J., & Maloy, K. J. (2014). NLRC4 expression in intestinal epithelial cells mediates protection against an enteric pathogen. Mucosal Immunology, 7(4), 775–785.

    CAS  PubMed  Google Scholar 

  • Nougayrede, J. P., Foster, G. H., & Donnenberg, M. S. (2007). Enteropathogenic Escherichia coli effector EspF interacts with host protein Abcf2. Cellular Microbiology, 9(3), 680–693.

    Article  CAS  PubMed  Google Scholar 

  • Orchard, R. C., et al. (2012). Identification of F-actin as the dynamic hub in a microbial-induced GTPase polarity circuit. Cell, 148(4), 803–815.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pallett, M. A., et al. (2014). The type III secretion effector NleF of enteropathogenic Escherichia coli activates NF-kappaB early during infection. Infection and Immunity, 82(11), 4878–4888.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Park, H. H., et al. (2007). The death domain superfamily in intracellular signaling of apoptosis and inflammation. Annual Review of Immunology, 25, 561–586.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pearson, J. S., & Hartland, E. L. (2014). The inflammatory response during Enterohemorrhagic Escherichia coli infection. Microbiology Spectrum, 2(4), 321–339.

    Google Scholar 

  • Pearson, J. S., et al. (2011). A type III effector protease NleC from enteropathogenic Escherichia coli targets NF-kappaB for degradation. Molecular Microbiology, 80(1), 219–230.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pearson, J. S., et al. (2013). A type III effector antagonizes death receptor signalling during bacterial gut infection. Nature, 501(7466), 247–251.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Perna, N. T., et al. (2001). Genome sequence of enterohaemorrhagic Escherichia coli O157:H7. Nature, 409(6819), 529–533.

    Article  CAS  PubMed  Google Scholar 

  • Pham, T. H., et al. (2012). Functional differences and interactions between the Escherichia coli type III secretion system effectors NleH1 and NleH2. Infection and Immunity, 80(6), 2133–2140.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raymond, B., et al. (2011). The WxxxE effector EspT triggers expression of immune mediators in an Erk/JNK and NF-kappaB-dependent manner. Cellular Microbiology, 13(12), 1881–1893.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Riley, L. W., et al. (1983). Hemorrhagic colitis associated with a rare Escherichia coli serotype. The New England Journal of Medicine, 308(12), 681–685.

    Article  CAS  PubMed  Google Scholar 

  • Robinson, K. S., et al. (2010). The enteropathogenic Escherichia coli effector NleH inhibits apoptosis induced by Clostridium difficile toxin B. Microbiology, 156(Pt 6), 1815–1823.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ruchaud-Sparagano, M. H., et al. (2011). The enteropathogenic E. coli (EPEC) Tir effector inhibits NF-kappaB activity by targeting TNFalpha receptor-associated factors. PLoS Pathogens, 7(12), e1002414.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Samba-Louaka, A., et al. (2008). Bacterial cyclomodulin Cif blocks the host cell cycle by stabilizing the cyclin-dependent kinase inhibitors p21 and p27. Cellular Microbiology, 10(12), 2496–2508.

    Article  CAS  PubMed  Google Scholar 

  • Samba-Louaka, A., et al. (2009). The enteropathogenic Escherichia coli effector Cif induces delayed apoptosis in epithelial cells. Infection and Immunity, 77(12), 5471–5477.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sato, Y., et al. (2009). Structural basis for specific recognition of Lys 63-linked polyubiquitin chains by NZF domains of TAB2 and TAB3. The EMBO Journal, 28(24), 3903–3909.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schuller, S., Frankel, G., & Phillips, A. D. (2004). Interaction of Shiga toxin from Escherichia coli with human intestinal epithelial cell lines and explants: Stx2 induces epithelial damage in organ culture. Cellular Microbiology, 6(3), 289–301.

    Article  PubMed  Google Scholar 

  • Sellin, M. E., et al. (2015). Inflammasomes of the intestinal epithelium. Trends in Immunology, 36(8), 442–450.

    Article  CAS  PubMed  Google Scholar 

  • Sham, H. P., et al. (2011). Attaching and effacing bacterial effector NleC suppresses epithelial inflammatory responses by inhibiting NF-kappaB and p38 mitogen-activated protein kinase activation. Infection and Immunity, 79(9), 3552–3562.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shames, S. R., et al. (2010). The pathogenic E. coli type III effector EspZ interacts with host CD98 and facilitates host cell prosurvival signalling. Cellular Microbiology, 12(9), 1322–1339.

    Article  CAS  PubMed  Google Scholar 

  • Shames, S. R., et al. (2011a). The pathogenic Escherichia coli type III secreted protease NleC degrades the host acetyltransferase p300. Cellular Microbiology, 13(10), 1542–1557.

    Article  CAS  PubMed  Google Scholar 

  • Shames, S. R., et al. (2011b). The type III system-secreted effector EspZ localizes to host mitochondria and interacts with the translocase of inner mitochondrial membrane 17b. Infection and Immunity, 79(12), 4784–4790.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shaulian, E., & Karin, M. (2001). AP-1 in cell proliferation and survival. Oncogene, 20(19), 2390–2400.

    Article  CAS  PubMed  Google Scholar 

  • Smith, W. E., et al. (2003). Shiga toxin 1 triggers a ribotoxic stress response leading to p38 and JNK activation and induction of apoptosis in intestinal epithelial cells. Infection and Immunity, 71(3), 1497–1504.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Spika, J. S., et al. (1986). Hemolytic uremic syndrome and diarrhea associated with Escherichia coli O157:H7 in a day care center. The Journal of Pediatrics, 109(2), 287–291.

    Article  CAS  PubMed  Google Scholar 

  • Stahl, A. L., et al. (2006). Lipopolysaccharide from enterohemorrhagic Escherichia coli binds to platelets through TLR4 and CD62 and is detected on circulating platelets in patients with hemolytic uremic syndrome. Blood, 108(1), 167–176.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Taieb, F., et al. (2006). Escherichia coli Cyclomodulin Cif induces G2 arrest of the host cell cycle without activation of the DNA-damage checkpoint-signalling pathway. Cellular Microbiology, 8(12), 1910–1921.

    Article  CAS  PubMed  Google Scholar 

  • Takaesu, G., et al. (2000). TAB2, a novel adaptor protein, mediates activation of TAK1 MAPKKK by linking TAK1 to TRAF6 in the IL-1 signal transduction pathway. Molecular Cell, 5(4), 649–658.

    Article  CAS  PubMed  Google Scholar 

  • Takeuchi, O., & Akira, S. (2010). Pattern recognition receptors and inflammation. Cell, 140(6), 805–820.

    Article  CAS  PubMed  Google Scholar 

  • Thorpe, C. M., et al. (1999). Shiga toxins stimulate secretion of interleukin-8 from intestinal epithelial cells. Infection and Immunity, 67(11), 5985–5993.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Thorpe, C. M., et al. (2001). Shiga toxins induce, superinduce, and stabilize a variety of C-X-C chemokine mRNAs in intestinal epithelial cells, resulting in increased chemokine expression. Infection and Immunity, 69(10), 6140–6147.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Toro, T. B., Toth, J. I., & Petroski, M. D. (2013). The cyclomodulin cycle inhibiting factor (CIF) alters cullin neddylation dynamics. The Journal of Biological Chemistry, 288(21), 14716–14726.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tzipori, S., et al. (1985). Enteropathogenic Escherichia coli enteritis: Evaluation of the gnotobiotic piglet as a model of human infection. Gut, 26(6), 570–578.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tzipori, S., Gibson, R., & Montanaro, J. (1989). Nature and distribution of mucosal lesions associated with enteropathogenic and enterohemorrhagic Escherichia coli in piglets and the role of plasmid-mediated factors. Infection and Immunity, 57(4), 1142–1150.

    CAS  PubMed  PubMed Central  Google Scholar 

  • van Setten, P. A., et al. (1996). Effects of verocytotoxin-1 on nonadherent human monocytes: Binding characteristics, protein synthesis, and induction of cytokine release. Blood, 88(1), 174–183.

    PubMed  Google Scholar 

  • Vallabhapurapu, S., & Karin, M. (2009). Regulation and function of NF-kappaB transcription factors in the immune system. Annual Review of Immunology, 27, 693–733.

    Article  CAS  PubMed  Google Scholar 

  • Varma, J. K., et al. (2003). An outbreak of Escherichia coli O157 infection following exposure to a contaminated building. JAMA, 290(20), 2709–2712.

    Article  CAS  PubMed  Google Scholar 

  • Vossenkamper, A., et al. (2010). Inhibition of NF-kappaB signaling in human dendritic cells by the enteropathogenic Escherichia coli effector protein NleE. Journal of Immunology, 185(7), 4118–4127.

    Article  CAS  Google Scholar 

  • Walters, M. D., et al. (1989). The polymorphonuclear leucocyte count in childhood haemolytic uraemic syndrome. Pediatric Nephrology, 3(2), 130–134.

    Article  CAS  PubMed  Google Scholar 

  • Wan, F., et al. (2011). IKKbeta phosphorylation regulates RPS3 nuclear translocation and NF-kappaB function during infection with Escherichia coli strain O157:H7. Nature Immunology, 12(4), 335–343.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang, L., et al. (2010). The Fas-FADD death domain complex structure reveals the basis of DISC assembly and disease mutations. Nature Structural & Molecular Biology, 17(11), 1324–1329.

    Article  CAS  Google Scholar 

  • Wilbur, J. S., et al. (2015). The secreted effector protein EspZ is essential for virulence of rabbit enteropathogenic Escherichia coli. Infection and Immunity, 83(3), 1139–1149.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wong Fok Lung, T., et al. (2014). The cell death response to enteropathogenic Escherichia coli infection. Cellular Microbiology, 16(12), 1736–1745.

    Article  PubMed  CAS  Google Scholar 

  • Wong, A. R., et al. (2011). Enteropathogenic and enterohaemorrhagic Escherichia coli: Even more subversive elements. Molecular Microbiology, 80(6), 1420–1438.

    Article  CAS  PubMed  Google Scholar 

  • Yan, D., et al. (2012). Inhibition of TLR signaling by a bacterial protein containing immunoreceptor tyrosine-based inhibitory motifs. Nature Immunology, 13(11), 1063–1071.

    Article  CAS  PubMed  Google Scholar 

  • Yan, D., et al. (2013). Enteropathogenic Escherichia coli Tir recruits cellular SHP-2 through ITIM motifs to suppress host immune response. Cellular Signalling, 25(9), 1887–1894.

    Article  CAS  PubMed  Google Scholar 

  • Yao, Q., et al. (2014). Structure and specificity of the bacterial cysteine methyltransferase effector NleE suggests a novel substrate in human DNA repair pathway. PLoS Pathogens, 10(11), e1004522.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yen, H., et al. (2010). NleC, a type III secretion protease, compromises NF-kappaB activation by targeting p65/RelA. PLoS Pathogens, 6(12), e1001231.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yen, H., Sugimoto, N., & Tobe, T. (2015). Enteropathogenic Escherichia coli uses NleA to inhibit NLRP3 inflammasome activation. PLoS Pathogens, 11(9), e1005121.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yi, C. R., et al. (2014). Systematic analysis of bacterial effector-postsynaptic density 95/disc large/zonula occludens-1 (PDZ) domain interactions demonstrates Shigella OspE protein promotes protein kinase C activation via PDLIM proteins. The Journal of Biological Chemistry, 289, 30101–30113.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang, Q., et al. (2000). Lack of phosphotyrosine phosphatase SHP-1 expression in malignant T-cell lymphoma cells results from methylation of the SHP-1 promoter. The American Journal of Pathology, 157(4), 1137–1146.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang, L., et al. (2012). Cysteine methylation disrupts ubiquitin-chain sensing in NF-kappaB activation. Nature, 481(7380), 204–208.

    Article  CAS  Google Scholar 

  • Zhou, X., et al. (2003). Flagellin of enteropathogenic Escherichia coli stimulates interleukin-8 production in T84 cells. Infection and Immunity, 71(4), 2120–2129.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zurawski, D. V., et al. (2008). The NleE/OspZ family of effector proteins is required for polymorphonuclear transepithelial migration, a characteristic shared by enteropathogenic Escherichia coli and Shigella flexneri infections. Infection and Immunity, 76(1), 369–379.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by grants to ELH from the Australian National Health and Medical Research Council (APP1044061). JSP is the recipient of an NHMRC Early Career Fellowship. YZ is the recipient of a University of Melbourne International Research Scholarship (MIRS).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Elizabeth L. Hartland .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer International Publishing AG

About this chapter

Cite this chapter

Zhang, Y., Pearson, J.S., Hartland, E.L. (2017). Host Innate Immune Factors Influencing Enterohemorrhagic Escherichia coli Pathogenicity. In: Gurtler, J., Doyle, M., Kornacki, J. (eds) Foodborne Pathogens. Food Microbiology and Food Safety(). Springer, Cham. https://doi.org/10.1007/978-3-319-56836-2_12

Download citation

Publish with us

Policies and ethics