journal article Open Access Jan 04, 2016

Subversion of Host Innate Immunity by Uropathogenic Escherichia coli

Pathogens Vol. 5 No. 1 pp. 2 · MDPI AG
View at Publisher Save 10.3390/pathogens5010002
Abstract
Uropathogenic Escherichia coli (UPEC) cause the majority of community-onset urinary tract infections (UTI) and represent a major etiologic agent of healthcare-associated UTI. Introduction of UPEC into the mammalian urinary tract evokes a well-described inflammatory response, comprising pro-inflammatory cytokines and chemokines as well as cellular elements (neutrophils and macrophages). In human UTI, this inflammatory response contributes to symptomatology and provides means for diagnosis by standard clinical testing. Early in acute cystitis, as demonstrated in murine models, UPEC gains access to an intracellular niche that protects a population of replicating bacteria from arriving phagocytes. To ensure the establishment of this protected niche, UPEC employ multiple strategies to attenuate and delay the initiation of host inflammatory components, including epithelial secretion of chemoattractants. Recent work has also revealed novel mechanisms by which UPEC blunts neutrophil migration across infected uroepithelium. Taken together, these attributes distinguish UPEC from commensal and nonpathogenic E. coli strains. This review highlights the unique immune evasion and suppression strategies of this bacterial pathogen and offers directions for further study; molecular understanding of these mechanisms will inform the development of adjunctive, anti-virulence therapeutics for UTI.
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References
72
[1]
Alto, N.M., and Orth, K. (2012). Subversion of cell signaling by pathogens. Cold Spring Harb. Perspect. Biol., 4. 10.1101/cshperspect.a006114
[2]
Giogha "Inhibition of death receptor signaling by bacterial gut pathogens" Cytokine Growth Factor Rev. (2014) 10.1016/j.cytogfr.2013.12.012
[3]
Krachler "Manipulation of kinase signaling by bacterial pathogens" J. Cell Biol. (2011) 10.1083/jcb.201107132
[4]
Silke "Masters, marionettes and modulators: Intersection of pathogen virulence factors and mammalian death receptor signaling" Curr. Opin. Immunol. (2013) 10.1016/j.coi.2013.05.011
[5]
Schappert "Ambulatory medical care utilization estimates for 2007" Vital Health Stat. Series 13, Data from the National Health Survey (2011)
[6]
UROLOGIC DISEASES IN AMERICA PROJECT: ANALYTICAL METHODS AND PRINCIPAL FINDINGS

MARK S. LITWIN, Christopher S. Saigal, Elizabeth M. Yano et al.

Journal of Urology 2005 10.1097/01.ju.0000152365.43125.3b
[7]
Extensive mosaic structure revealed by the complete genome sequence of uropathogenic Escherichia coli

Rodney A. Welch, V. Burland, G. Plunkett et al.

Proceedings of the National Academy of Sciences 2002 10.1073/pnas.252529799
[8]
Hedges "Interleukin-6 response to deliberate colonization of the human urinary tract with Gram-negative bacteria" Infect. Immun. (1991) 10.1128/iai.59.1.421-427.1991
[9]
Samuelsson "Toll-like receptor 4 expression and cytokine responses in the human urinary tract mucosa" Infect. Immun. (2004) 10.1128/iai.72.6.3179-3186.2004
[10]
Song, J., Duncan, M.J., Li, G., Chan, C., Grady, R., Stapleton, A., and Abraham, S.N. (2007). A novel TLR4-mediated signaling pathway leading to IL-6 responses in human bladder epithelial cells. PLoS Pathog., 3. 10.1371/journal.ppat.0030060
[11]
Hawn "Cutting edge: Tlr5−/− mice are more susceptible to Escherichia coli urinary tract infection" J. Immunol. (2007) 10.4049/jimmunol.178.8.4717
[12]
Smith "Toll-like receptor responses of normal human urothelial cells to bacterial flagellin and lipopolysaccharide" J. Urol. (2011) 10.1016/j.juro.2011.04.112
[13]
Peck "Precarious balance: Th17 cells in host defense" Infect. Immun. (2010) 10.1128/iai.00929-09
[14]
Sivick "The innate immune response to uropathogenic Escherichia coli involves IL-17A in a murine model of urinary tract infection" J. Immunol. (2010) 10.4049/jimmunol.0902386
[15]
Chromek "The antimicrobial peptide cathelicidin protects the urinary tract against invasive bacterial infection" Nat. Med. (2006) 10.1038/nm1407
[16]
Danka "Cathelicidin augments epithelial receptivity and pathogenesis in experimental Escherichia coli cystitis" J. Infect. Dis. (2015) 10.1093/infdis/jiu577
[17]
Becknell, B., Spencer, J.D., Carpenter, A.R., Chen, X., Singh, A., Ploeger, S., Kline, J., Ellsworth, P., Li, B., and Proksch, E. (2013). Expression and antimicrobial function of beta-defensin 1 in the lower urinary tract. PLoS One, 8. 10.1371/journal.pone.0077714
[18]
Nielsen "Role of urinary cathelicidin LL-37 and human beta-defensin 1 in uncomplicated Escherichia coli urinary tract infections" Infect. Immun. (2014) 10.1128/iai.01393-13
[19]
Shahin "Neutrophil recruitment and bacterial clearance correlated with LPS responsiveness in local Gram-negative infection" J. Immunol. (1987) 10.4049/jimmunol.138.10.3475
[20]
Haraoka "Neutrophil recruitment and resistance to urinary tract infection" J. Infect. Dis. (1999) 10.1086/315006
[21]
Artifoni "Interleukin-8 and CXCR1 receptor functional polymorphisms and susceptibility to acute pyelonephritis" J. Urol. (2007) 10.1016/j.juro.2006.10.037
[22]
Ingersoll "G-CSF induction early in uropathogenic Escherichia coli infection of the urinary tract modulates host immunity" Cell. Microbiol. (2008) 10.1111/j.1462-5822.2008.01230.x
[23]
Svensson "Effects of epithelial and neutrophil CXCR2 on innate immunity and resistance to kidney infection" Kidney Int. (2008) 10.1038/ki.2008.105
[24]
Svensson "Acute pyelonephritis and renal scarring are caused by dysfunctional innate immunity in mCXCR2 heterozygous mice" Kidney Int. (2011) 10.1038/ki.2011.257
[25]
Song "TLR4-initiated and cAMP-mediated abrogation of bacterial invasion of the bladder" Cell Host Microbe (2007) 10.1016/j.chom.2007.05.007
[26]
Wright "Development of intracellular bacterial communities of uropathogenic Escherichia coli depends on type 1 pili" Cell. Microbiol. (2007) 10.1111/j.1462-5822.2007.00952.x
[27]
Eto "Clathrin, AP-2, and the NPXY-binding subset of alternate endocytic adaptors facilitate FimH-mediated bacterial invasion of host cells" Cell. Microbiol. (2008) 10.1111/j.1462-5822.2008.01229.x
[28]
Schilling "Bacterial invasion augments epithelial cytokine responses to Escherichia coli through a lipopolysaccharide-dependent mechanism" J. Immunol. (2001) 10.4049/jimmunol.166.2.1148
[29]
Berry "Urothelial cultures support intracellular bacterial community formation by uropathogenic Escherichia coli" Infect. Immun. (2009) 10.1128/iai.00323-09
[30]
Intracellular Bacterial Biofilm-Like Pods in Urinary Tract Infections

Gregory G. Anderson, Joseph J. Palermo, Joel D. Schilling et al.

Science 2003 10.1126/science.1084550
[31]
Type 1 pilus-mediated bacterial invasion of bladder epithelial cells

J. J. Martinez

The EMBO Journal 2000 10.1093/emboj/19.12.2803
[32]
Establishment of a Persistent Escherichia coli Reservoir during the Acute Phase of a Bladder Infection

Matthew A. Mulvey, Joel D. Schilling, Scott J. Hultgren

Infection and Immunity 2001 10.1128/iai.69.7.4572-4579.2001
[33]
Eto, D.S., Jones, T.A., Sundsbak, J.L., and Mulvey, M.A. (2007). Integrin-mediated host cell invasion by type 1-piliated uropathogenic Escherichia coli. PLoS Pathog., 3. 10.1371/journal.ppat.0030100
[34]
Duncan "Bacterial penetration of bladder epithelium through lipid rafts" J. Biol. Chem. (2004) 10.1074/jbc.m400769200
[35]
Cyclic AMP–regulated exocytosis of Escherichia coli from infected bladder epithelial cells

Brian L Bishop, Mathew J Duncan, Jeongmin Song et al.

Nature Medicine 2007 10.1038/nm1572
[36]
Eto "Actin-gated intracellular growth and resurgence of uropathogenic Escherichia coli" Cell. Microbiol. (2006) 10.1111/j.1462-5822.2006.00691.x
[37]
Differentiation and developmental pathways of uropathogenic Escherichia coli in urinary tract pathogenesis

Sheryl S. Justice, Chia Hung, Julie A. Theriot et al.

Proceedings of the National Academy of Sciences 2004 10.1073/pnas.0308125100
[38]
Intracellular Bacteria in the Pathogenesis of Escherichia coli Urinary Tract Infection in Children

Luciana Robino, Paola Scavone, Lucia Araujo et al.

Clinical Infectious Diseases 2014 10.1093/cid/ciu634
[39]
Robino "Detection of intracellular bacterial communities in a child with Escherichia coli recurrent urinary tract infections" Pathog. Dis. (2013) 10.1111/2049-632x.12047
[40]
Detection of Intracellular Bacterial Communities in Human Urinary Tract Infection

David A Rosen, Thomas M Hooton, Walter E Stamm et al.

PLoS Medicine 10.1371/journal.pmed.0040329
[41]
OmpA of Uropathogenic Escherichia coli Promotes Postinvasion Pathogenesis of Cystitis

Tracy F. Nicholson, Kristin M. Watts, David A. Hunstad

Infection and Immunity 2009 10.1128/iai.00670-09
[42]
Justice "Filamentation by Escherichia coli subverts innate defenses during urinary tract infection" Proc. Natl. Acad. Sci. USA (2006) 10.1073/pnas.0606329104
[43]
Horvath "Morphological plasticity promotes resistance to phagocyte killing of uropathogenic Escherichia coli" Microbes Infect. (2011) 10.1016/j.micinf.2010.12.004
[44]
Justice "Morphological plasticity as a bacterial survival strategy" Nat. Rev. Microbiol. (2008) 10.1038/nrmicro1820
[45]
Champion "Role of target geometry in phagocytosis" Proc. Natl. Acad. Sci. USA (2006) 10.1073/pnas.0600997103
[46]
Klumpp "Uropathogenic Escherichia coli potentiates type 1 pilus-induced apoptosis by suppressing NF-κB" Infect. Immun. (2001) 10.1128/iai.69.11.6689-6695.2001
[47]
Billips "Modulation of host innate immune response in the bladder by uropathogenic Escherichia coli" Infect. Immun. (2007) 10.1128/iai.00922-07
[48]
Hunstad "Suppression of bladder epithelial cytokine responses by uropathogenic Escherichia coli" Infect. Immun. (2005) 10.1128/iai.73.7.3999-4006.2005
[49]
Billips "Molecular basis of uropathogenic Escherichia coli evasion of the innate immune response in the bladder" Infect. Immun. (2008) 10.1128/iai.00069-08
[50]
Characterization of the role of the Escherichia coli periplasmic chaperone SurA using differential proteomics

Didier Vertommen, Natividad Ruiz, Pauline Leverrier et al.

PROTEOMICS 2009 10.1002/pmic.200800794

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Published
Jan 04, 2016
Vol/Issue
5(1)
Pages
2
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Cite This Article
Patrick Olson, David Hunstad (2016). Subversion of Host Innate Immunity by Uropathogenic Escherichia coli. Pathogens, 5(1), 2. https://doi.org/10.3390/pathogens5010002
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