Pathogenic Mechanisms of Uropathogens

  • Ryan Chanyi
  • Jeremy P. Burton
  • Peter A. Cadieux


Urinary tract infections (UTIs) can affect both men and women at almost any stage in their lifetime. While the vast majority of these are not life-threatening, they cause significant morbidity to patients and place a heavy burden on healthcare systems worldwide. This is further complicated by the use of urinary drainage devices such as catheters and stents, which provide additional sites for bacterial/fungal attachment and biofilm development. Despite being exposed to a wide array of antagonistic environmental conditions and the host immune system, uropathogens are generally very successful at establishing infection. This is mainly due to the plethora of pathogenic mechanisms they utilize that provide an advantage over the host. In this brief review, we discuss a small subset of the mechanisms used by uropathogens including the appendages, proteins and sugars used to adhere to surfaces, the invasion into host tissues, immune evasion strategies and antibiotic resistance. This work illustrates the complexity of the interaction between the urinary tract and uropathogens, and supports the development and application of multi-faceted strategies for infection prevention and treatment.


Extracellular Polymeric Substance Urothelial Cell Yersinia Pestis Bladder Epithelium Persister Cell 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. 1.
    Klevens RM, Edwards JR, Richards CL, Horan TC, Gaynes RP, et al. Estimating health care-associated infections and deaths in U.S. hospitals, 2002. Public Health Rep. 2007;122(2):160–6.PubMedCentralPubMedGoogle Scholar
  2. 2.
    Raz R, Gennesin Y, Wasser J, Stoler Z, Rosenfeld S, et al. Recurrent urinary tract infections in postmenopausal women. Clin Infect Dis. 2000;30(1):152–6.CrossRefPubMedGoogle Scholar
  3. 3.
    Bower JM, Eto DS, Mulvey MA. Covert operations of uropathogenic Escherichia coli within the urinary tract. Traffic. 2005;6:18–31.PubMedCentralCrossRefPubMedGoogle Scholar
  4. 4.
    Croxen MA, Finlay BB. Molecular mechanisms of Escherichia coli pathogenicity. Nat Rev Microbiol. 2010;8:26–38.PubMedGoogle Scholar
  5. 5.
    Klemm P, Schembri MA. Bacterial adhesins: function and structure. Int J Med Microbiol. 2000;290:27–35.CrossRefPubMedGoogle Scholar
  6. 6.
    Abraham SN, Sun D, Dale JB, Beachey EH. Conservation of the D-mannose-adhesion protein among type 1 fimbriated members of the family Enterobacteriaceae. Nature. 1988;336(6200):682–4.CrossRefPubMedGoogle Scholar
  7. 7.
    Connell I, Agace W, Klemm P, Schembri M, Marild S, Svanborg C. Type 1 fimbrial expression enhances Escherichia coli virulence for the urinary tract. Proc Natl Acad Sci U S A. 1996;93(18):9827–32.PubMedCentralCrossRefPubMedGoogle Scholar
  8. 8.
    Hultgren SJ, Porter TN, Schaeffer AJ, Duncan JL. Role of type 1 pili and effects of phase variation on lower urinary tract infections produced by Escherichia coli. Infect Immun. 1985;50(2):370–7.PubMedCentralPubMedGoogle Scholar
  9. 9.
    Jones CH, Pinkner JS, Roth R, Heuser J, Nicholes AV, et al. FimH adhesion of type 1 pili is assembled into a fibrillary tip structure in the Enterobacteriaceae. Proc Natl Acad Sci U S A. 1995;92(6):2081–5.PubMedCentralCrossRefPubMedGoogle Scholar
  10. 10.
    Krogfelt KA, Bergmans H, Klemm P. Direct evidence that the FimH protein is the mannose-specific adhesion of Escherichia coli type 1 fimbriae. Infect Immun. 1990;58(6):1995–8.PubMedCentralPubMedGoogle Scholar
  11. 11.
    Mulvey MA, Lopez-Boado YS, Wilson CL, Roth R, Parks WC, et al. Induction and evasion of host defenses by type 1-piliated uropathogenic Escherichia coli. Science. 1998;282(5393):1494–7.CrossRefPubMedGoogle Scholar
  12. 12.
    Xie B, Zhou G, Chan SY, Shapiro E, Kong XP, et al. Distinct glycan structures of uroplakins Ia and Ib: structural basis for the selective binding of FimH adhesion to uroplakin Ia. J Biol Chem. 2006;281(21):14644–53.CrossRefPubMedGoogle Scholar
  13. 13.
    Zhou G, Mo WJ, Sebbel P, Min G, Neubert TA, et al. Uroplakin Ia is the urothelial receptor for uropathogenic Escherichia coli: evidence from in vitro FimH binding. J Cell Sci. 2001;114(Pt 22):4095–103.PubMedGoogle Scholar
  14. 14.
    Fukushi Y, Orikasa S, Kagayama M. An electron microscopic study of the interaction between vesical epithelium and E. coli. Invest Urol. 1979;17(1):61–8.PubMedGoogle Scholar
  15. 15.
    Martinez JJ, Mulvey MA, Schilling JD, Pinkner JS, Hultgren SJ. Type 1 pilus-mediated bacterial invasion of bladder epithelial cells. EMBO J. 2000;19(12):2803–12.PubMedCentralCrossRefPubMedGoogle Scholar
  16. 16.
    McTaggart LA, Rigby RC, Elliott TS. The pathogenesis of urinary tract infections associated with Escherichia coli, Staphylococcus saprophyticus and S. epidermidis. J Med Microbiol. 1990;32(2):135–41.CrossRefPubMedGoogle Scholar
  17. 17.
    Thumbikat P, Berry RE, Schaeffer AJ, Klumpp DJ. Differentiation-induced uroplakin III expression promotes urothelial cell death in response to uropathogenic E. coli. Microbes Infect. 2009;11(1):57–65.PubMedCentralCrossRefPubMedGoogle Scholar
  18. 18.
    Wang H, Min G, Glockshuber R, Sun TT, Kong XP. Uropathogenic E. coli adhesion-induced host cell receptor conformational changes: implications in transmembrane signalling transduction. J Mol Biol. 2009;392(2):352–61.PubMedCentralCrossRefPubMedGoogle Scholar
  19. 19.
    Klumpp DJ, Weiser AC, Sengupta S, Forrestal SG, Batler RA, et al. Uropathogenic Escherichia coli potentiates type 1 pilus-induced apoptosis by suppressing NF-kappaB. Infect Immun. 2001;69(11):6689–95.PubMedCentralCrossRefPubMedGoogle Scholar
  20. 20.
    Schwartz DJ, Kalas V, Pinkner JS, Chen SL, Spaulding CN, et al. Positively selected FimH residues enhance virulence during urinary tract infections by altering FimH conformation. Proc Natl Acad Sci U S A. 2013;110(39):15530–7.PubMedCentralCrossRefPubMedGoogle Scholar
  21. 21.
    Bateman SL, Stapleton AE, Stamm WE, Hooton TM, Seed PC. The type I pili regulator gene fimX and pathogenicity island PAI-X as molecular markers of uropathogenic Escherichia coli. Microbiology. 2013;159:1606–17.PubMedCentralCrossRefPubMedGoogle Scholar
  22. 22.
    Struve C, Bojer M, Krogfelt KA. Characterization of klebsiella pneumonia type 1 fimbriae by detection of phase variation during colonization and infection and impact on virulence. Infect Immun. 2008;76:4055–65.Google Scholar
  23. 23.
    Leffler H, Lomberg H, Gotschlich E, Hagberg L, Jodal U, et al. Chemical and clinical studies on the interaction of Escherichia coli with host glycolipid receptors in urinary tract infection. Scand J Infect Dis Suppl. 1982;33:46–51.PubMedGoogle Scholar
  24. 24.
    Plos K, Connell H, Jodal U, Marklund BI, Mårild S, et al. Intestinal carriage of P fimbriated Escherichia coli and the susceptibility to urinary tract infection in young children. J Infect Dis. 1995;171(3):625–31.CrossRefPubMedGoogle Scholar
  25. 25.
    Väisänen V, Elo J, Tallgren LG, Siitonen A, Mäkelä PH, et al. Mannose-resistant haemagglutination and P antigen recognition are characteristic of Escherichia coli causing primary pyelonephritis. Lancet. 1981;2(8260–61):1366–9.CrossRefPubMedGoogle Scholar
  26. 26.
    Melican K, Sandoval RM, Kader A, Josefsson L, Tanner GA, et al. Uropathogenic Escherichia coli P and type 1 fimbriae act in synergy in a living host to facilitate renal colonization leading to nephron obstruction. PLoS Pathog. 2011;7(2):e1001298.PubMedCentralCrossRefPubMedGoogle Scholar
  27. 27.
    Zunino P, Geymonat L, Allen AG, Preston A, Sosa V, et al. New aspects of the role of MR/P fimbriae in Proteus mirabilis urinary tract infection. FEMS Immunol Med Microbiol. 2001;31(2):113–20.CrossRefPubMedGoogle Scholar
  28. 28.
    Lindberg S, Xia Y, Sonden B, Goransson M, Hacker J, et al. Regulatory interactions among adhesion gene systems of uropathogenic Escherichia coli. Infect Immun. 2008;76(2):771–80.PubMedCentralCrossRefPubMedGoogle Scholar
  29. 29.
    Marre R, Kreft B, Hacker J. Genetically engineered S and F1C fimbriae differ in their contribution to adherence of Escherichia coli to cultured renal tubular cells. Infect Immun. 1990;58(10):3434–7.PubMedCentralPubMedGoogle Scholar
  30. 30.
    Mulvey MA. Adhesion and entry of uropathogenic Escherichia coli. Cell Microbiol. 2002;4(5):257–71.CrossRefPubMedGoogle Scholar
  31. 31.
    Korhonen TK, Valtonen MV, Parkkinen J, Väisänen-Rhen V, Finne J, et al. Serotypes, hemolysin production, and receptor recognition of Escherichia coli strains associated with neonatal sepsis and meningitis. Infect Immun. 1985;48(2):486–91.PubMedCentralPubMedGoogle Scholar
  32. 32.
    Totsika M, Kostakioti M, Hannan TJ, Upton M, Beatson SA, Janetka JW, Hultgren SJ, Schembri MA. A FimH inhibitor prevents acute bladder infection and treats chronic cystitis cause by multidrug-resistant uropathogenic Escherichia coli ST131. J Infect Dis. 2013;208(6):921–8.PubMedCentralCrossRefPubMedGoogle Scholar
  33. 33.
    Volkan E, Kalas V, Pinkner JS, Dodson KW, Henderson NS, et al. Molecular basis of usher pore gating in Escherichia coli pilus biogenesis. Proc Natl Acad Sci U S A. 2013;110(51):20741–6.PubMedCentralCrossRefPubMedGoogle Scholar
  34. 34.
    Tenke P, Köves B, Nagy K, Hultgren SJ, Mendling W, Wullt B, Grabe M, Wagenlehner FM, Cek M, Pickard R, Botto H, Naber KG, Bjerklund Johansen TE. Update on biofilm infections in the urinary tract. World J Urol. 2012;30(1):51–7.CrossRefPubMedGoogle Scholar
  35. 35.
    Donlan RM. Biofilm elimination on intravascular catheters: important considerations for the infectious disease practitioner. Clin Infect Dis. 2011;52(8):1038–45.CrossRefPubMedGoogle Scholar
  36. 36.
    Fujiwara S, Miyake Y, Usi T, Suginaka H. Effect of adherence on antimicrobial suspectibility of Pseudomonas aeruginosa, Serratia marscescens and Proteus mirabilis. Hiroshima J Med Sci. 1998;47:1–5.Google Scholar
  37. 37.
    Danese PN, Pratt LA, Dove SL, Kolter R. The outer membrane protein, antigen 43, mediates cell-to-cell interactions within Escherichia coli biofilms. Mol Microbiol. 2000;37(2):424–32.CrossRefPubMedGoogle Scholar
  38. 38.
    Kjaergaard K, Schembri MA, Ramos C, Molin S, Klemm P. Antigen 43 facilitates formation of multispecies biofilms. Environ Microbiol. 2000;2(6):695–702.CrossRefPubMedGoogle Scholar
  39. 39.
    Reidl S, Lehmann A, Schiller R, Salam Khan A, Dobrindt U. Impact of O-glycosylation on the molecular and cellular adhesion properties of the Escherichia coli autotransporter protein Ag43. Int J Med Microbiol. 2009;299(6):389–401.CrossRefPubMedGoogle Scholar
  40. 40.
    Clarke SR, Wiltshire MD, Foster SJ. IsdA of Staphylococcus aureus is a broad spectrum, iron-regulated adhesion. Mol Microbiol. 2004;51(5):1509–19.CrossRefPubMedGoogle Scholar
  41. 41.
    Ní Eidhin D, Perkins S, Francois P, Vaudaux P, Höök M, et al. Clumping factor B (ClfB), a new surface-located fibrinogen-binding adhesion of Staphylococcus aureus. Mol Microbiol. 1998;30(2):245–57.CrossRefPubMedGoogle Scholar
  42. 42.
    Sillanpää J, Nallapareddy SR, Houston J, Ganesh VK, Bourgogne A, et al. A family of fibrinogen-binding MSCRAMMs from Enterococcus faecalis. Microbiology. 2009;155(Pt 7):2390–400.PubMedCentralCrossRefPubMedGoogle Scholar
  43. 43.
    Flores-Mireles A, Pinkner JS, Caparon MG, Hultgren SJ. EbpA vaccine antibodies block binding of Enterococcus faecalis to fibrinogen to prevent catheter-associated bladder infection in mice. Sci Transl Med. 2014;6(254):254ra127.PubMedCentralCrossRefPubMedGoogle Scholar
  44. 44.
    Clarke SR, Foster SJ. Surface adhesins of Staphylococcus aureus. Adv Microb Physiol. 2006;51:187–224.CrossRefPubMedGoogle Scholar
  45. 45.
    Anderson GG, Martin SM, Hultgren SJ. Host subversion by formation of intracellular bacterial communities in the urinary tract. Microbes Infect. 2004;6(12):1094–101.CrossRefPubMedGoogle Scholar
  46. 46.
    Eto DS, Jones TA, Sundsbak JL, Mulvey MA. Integrin-mediated host cell invasion by type 1-piliated uropathogenic Escherichia coli. PLoS Pathog. 2007;3(7):e100.PubMedCentralCrossRefPubMedGoogle Scholar
  47. 47.
    Song J, Bishop BL, Li G, Duncan MJ, Abraham SN. TLR4-initiated and cAMP-mediated abrogation of bacterial invasion of the bladder. Cell Host Microbe. 2007;1(4):287–98.PubMedCentralCrossRefPubMedGoogle Scholar
  48. 48.
    Hannan TJ, Totsika M, Mansfield KJ, Moore KH, Schembri MA, et al. Host-pathogen checkpoints and population bottlenecks in persistent and intracellular uropathogenic E. coli bladder infection. FEMS Microbiol Rev. 2012;36(3):616–48.PubMedCentralCrossRefPubMedGoogle Scholar
  49. 49.
    Hunstad DA, Justice SS. Intracellular lifestyles and immune evasion stratagies of uropathogenic Escherichia coli. Nat Rev Microbiol. 2010;64:203–21.Google Scholar
  50. 50.
    Reigstad CS, Hultgren SJ, Gordon JI. Functional genomic studies of uropathogenic Escherichia coli and host urothelial cells when intracellular bacterial communities are assembled. J Biol Chem. 2007;282(29):21259–67.CrossRefPubMedGoogle Scholar
  51. 51.
    Wright KJ, Seed PC, Hultgren SJ. Development of intracellular bacterial communities of uropathogenic Escherichia coli depends on type 1 pili. Cell Microbiol. 2007;9(9):2230–41.CrossRefPubMedGoogle Scholar
  52. 52.
    Anderson GG, Goller CC, Justice S, Hultgren SJ, Seed PC. Polysaccharide capsule and sialic acid-mediated regulation promote biofilm-like intracellular bacterial communities during cystitis. Infect Immun. 2010;78(3):963–75.PubMedCentralCrossRefPubMedGoogle Scholar
  53. 53.
    Goller CC, Seed PC. Revisiting the Escherichia coli polysaccharide capsule as a virulence factor urinary tract infection. Virulence. 2010;1(4):333–7.CrossRefPubMedGoogle Scholar
  54. 54.
    Hadjifrangiskou M, Gu AP, Pinkner JS, Kostakioti M, Zhang EW, Greene SE, Hultgren SJ. Transposon mutagenesis identifies uropathogenic Escherichia coli biofilm factors. J Bacteriol. 2012;194(22):6195–205.PubMedCentralCrossRefPubMedGoogle Scholar
  55. 55.
    Blango MG, Mulvey MA. Persistence of uropathogenic Escherichia coli in the face of multiple antibiotics. Antimicrob Agents Chemother. 2010;54(5):1855–63.PubMedCentralCrossRefPubMedGoogle Scholar
  56. 56.
    Mulvey MA, Schilling JD, Hultgren SJ. Establishment of a persistent Escherichia coli reservoir during the acute phase of a bladder infection. Infect Immun. 2001;69(7):4572–9.PubMedCentralCrossRefPubMedGoogle Scholar
  57. 57.
    Mysorekar IU, Hultgren SJ. Mechanisms of uropathogenic Escherichia coli persistence and eradication from the urinary tract. Proc Natl Acad Sci U S A. 2006;103(38):14170–5.PubMedCentralCrossRefPubMedGoogle Scholar
  58. 58.
    Gur C, Coppenhagen-Glazer S, Rosenberg S, Yamin R, Enk J, et al. Natural killer cell-mediated host defense against uropathogenic E. coli is counteracted by bacterial hemolysinA-dependent killing of NK cells. Cell Host Microbe. 2013;14:664–74.CrossRefPubMedGoogle Scholar
  59. 59.
    Dhakal BK, Mulvey MA. The UPEC pore-forming toxin α-hemolysin triggers proteolysis of host proteins to disrupt cell adhesion, inflammatory and survival pathways. Cell Host Microbe. 2012;11:58–69.PubMedCentralCrossRefPubMedGoogle Scholar
  60. 60.
    Wiles TJ, Kulesus RR, Mulvey MA. Origins and virulence mechanisms of uropathogenic Escherichia coli. Exp Mol Pathol. 2008;85(1):11–9.PubMedCentralCrossRefPubMedGoogle Scholar
  61. 61.
    Davis JM, Carvalho HM, Rasmussen SB, O’Brien AD. Cytotoxic necrotizing factor 1 delivered by outer membrane vesicles of uropathogenic Escherichia coli attenuates polymorphonuclear leukocyte antimicrobial activity and chemotaxis. Infect Immun. 2006;74(8):4401–8.PubMedCentralCrossRefPubMedGoogle Scholar
  62. 62.
    Kouokam JC, Wai SN, Fällman M, Dobrindt U, Hacker J, et al. Active cytotoxic necrotizing factor 1 associated with outer membrane vesicles from uropathogenic Escherichia coli. Infect Immun. 2006;74(4):2022–30.PubMedCentralCrossRefPubMedGoogle Scholar
  63. 63.
    Garcia TA, Ventura CL, Smith MA, Merrell DS, O’Brien AD. Cytotoxic necrotizing factor 1 and hemolysin from uropathogenic Escherichia coli elicit different host responses in the murine bladder. Infect Immun. 2012;81(1):99–109.CrossRefPubMedGoogle Scholar
  64. 64.
    Smith YC, Rasmussen SB, Grande KK, Conran RM, O’Brien AD. Hemolysin of uropathogenic Escherichia coli evokes extensive shedding of the uroepithelium and hemorrhage in bladder tissue within the first 24 hours after intraurethral inoculation of mice. Infect Immun. 2008;76(7):2978–90.PubMedCentralCrossRefPubMedGoogle Scholar
  65. 65.
    Fiorentini C, Fabbri A, Matarrese P, Falzano L, Boquet P, et al. Hinderance of apoptosis and phagocytic behaviour induced by Escherichia coli cytotoxic necrotizing factor 1: two related activities in epithelial cells. Biochem Biophys Res Commun. 1997;241(2):314–46.CrossRefGoogle Scholar
  66. 66.
    Lerm M, Schmidt G, Goehring UM, Schirmer J, Aktories K. Identification of the region of rho involved in substrate recognition by Escherichia coli cytotoxic necrotizing factor 1 (CNF1). J Biol Chem. 1999;274(41):28999–9004.CrossRefPubMedGoogle Scholar
  67. 67.
    Mills M, Meysick KC, O’Brien AD. Cytotoxic necrotizing factor type 1 of uropathogenic Escherichia coli kills cultured human uroepithelial 5637 cells by an apoptotic mechanism. Infect Immun. 2000;68(10):5869–80.PubMedCentralCrossRefPubMedGoogle Scholar
  68. 68.
    Gao Q, Wang X, Xu H, Xu Y, Ling J, Zhang D, Gao S, Liu X. Roles of iron acquisition systems in virulence of extraintestinal pathogenic Escherichia coli: salmochelin and aerobactin contribute more to virulence than heme in a chicken infection model. BMC Microbiol. 2012;12:143.PubMedCentralCrossRefPubMedGoogle Scholar
  69. 69.
    Torres AG, Redford P, Welch RA, Payne SM. TonB-dependent systems of uropathogenic Escherichia coli: aerobactin and heme transport and TonB are required for virulence in the mouse. Infect Immun. 2001;69(10):6179–85.PubMedCentralCrossRefPubMedGoogle Scholar
  70. 70.
    Feldmann F, Sorsa LJ, Hildinger K, Schubert S. The salmochelin siderophore receptor IroN contributes to invasion of urothelial cells by extraintestinal pathogenic Escherichia coli in vitro. Infect Immun. 2007;75(6):3183–7.PubMedCentralCrossRefPubMedGoogle Scholar
  71. 71.
    Fetherston JD, Kirillina O, Bobrov AG, Paulley JT, Perry RD. The yersiniabactin transport system is critical for the pathogensis of bubonic and pneumonic plague. Infect Immun. 2010;78(5):2045–52.PubMedCentralCrossRefPubMedGoogle Scholar
  72. 72.
    Garcia EC, Brumbaugh AR, Mobley HL. Redundancy and specificity of Escherichia coli iron acquisition systems during urinary tract infection. Infect Immun. 2011;79(3):1225–35.PubMedCentralCrossRefPubMedGoogle Scholar
  73. 73.
    Chaturvedi KS, Hung CS, Crowley JR, Stapleton AE, Henderson JP. The siderophore yersiniabactin binds copper to protect pathogens during infection. Nat Chem Biol. 2012;8(8):731–6.PubMedCentralCrossRefPubMedGoogle Scholar
  74. 74.
    Brumbaugh AR, Smith SN, Mobley HL. Immunization with the yersiniabactin receptor, FyuA, protects against pyelonephritis in a murine model of urinary tract infection. Infect Immun. 2013;81(9):3309–16.PubMedCentralCrossRefPubMedGoogle Scholar
  75. 75.
    Torzewska A, Budzyńska A, Białczak-Kokot M, Różalski A. In vitro studies of epithelium-associated crystallization caused by uropathogens during urinary calculi development. Microb Pathog. 2014;71–72:25–31.CrossRefPubMedGoogle Scholar
  76. 76.
    Yasufuku T, Shigemura K, Shirakawa T, Matsumoto M, Nakano Y, Tanaka K, Arakawa S, Kinoshita S, Kawabata M, Fujisawa M. Correlation of overexpression of efflux pump genes with antibiotic resistance in Escherichia coli. Strains clinically isolated from urinary tract infection patients. J Clin Microbiol. 2011;49(1):189–94.PubMedCentralCrossRefPubMedGoogle Scholar
  77. 77.
    Micenková L, Sišková P, Bosák L, Jamborová I, Cernohorská L, et al. Characterization of human uropathogenic ESBL-producing Escherichia coli in the Czech Republic: spread of CTX-M-27-producing strains in a university hospital. Microb Drug Resist. 2014;20(6):610–7.CrossRefPubMedGoogle Scholar
  78. 78.
    Chandrakanth RK, Raju S, Patil SA. Aminoglycoside-resistance mechanisms in multidrug-resistant Staphylococcus aureus clinical isolates. Curr Microbiol. 2008;56(6):558–62.CrossRefPubMedGoogle Scholar
  79. 79.
    Soleimani N, Aganj M, Ali L, Shokoohizadeh L, Sakinc T. Frequency distribution of genes encoding aminoglycoside modifying enzymes in uropathogenic E. coli isolated from Iranian hospital. BMC Res Notes. 2014;7:842.PubMedCentralCrossRefPubMedGoogle Scholar
  80. 80.
    Ali I, Kumar N, Ahmed S, Dasti JI. Antibiotic resistance in uropathogenic E. coli strains isolated from non-hospitalized patients in Pakistan. J Clin Diagn Res. 2014;8(9):DC01–4.PubMedCentralPubMedGoogle Scholar
  81. 81.
    Sköld O. Sulfonamide resistance: mechanisms and trends. Drug Resist Updat. 2000;3(3):155–60.CrossRefPubMedGoogle Scholar
  82. 82.
    Goneau LW, Yeoh NS, MacDonald KW, Cadieux PA, Burton JP, Razvi H, Reid G. Selective target inactivation rather than global metabolic dormancy causes antibiotic tolerance in uropathogens. Antimicrob Agents Chemother. 2014;58(4):2089–97.PubMedCentralCrossRefPubMedGoogle Scholar
  83. 83.
    Lang T, Hudemann C, Tchatalbachev S, Stammler A, Michel V, et al. Uropathogenic Escherichia coli modulates innate immunity to suppress Th1-mediated inflammatory response during infectious epididymitis. Infect Immun. 2014;82(3):1104–11.PubMedCentralCrossRefPubMedGoogle Scholar
  84. 84.
    Billips BK, Schaeffer AJ, Klumpp DJ. Molecular basis of uropathogenic Escherichia coli evasion of the innate immune response in the bladder. Infect Immun. 2008;76(9):3891–900.PubMedCentralCrossRefPubMedGoogle Scholar
  85. 85.
    Lau ME, Loughman JA, Hunstad DA. YbcL of uropathogenic Escherichia coli suppresses transepithelial neutrophil migration. Infect Immun. 2012;80(12):4123–32.PubMedCentralCrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Ryan Chanyi
    • 1
    • 2
  • Jeremy P. Burton
    • 3
    • 4
  • Peter A. Cadieux
    • 5
    • 6
  1. 1.Department of Microbiology and ImmunologyCanadian Centre for Human Microbiome and Probiotics, Lawson Health Research InstituteLondonCanada
  2. 2.Divison of UrologySt Joseph’s Hospital Care LondonLondonCanada
  3. 3.Canadian Centre for Human Microbiome and ProbioticsLawson Health Research InstituteLondonCanada
  4. 4.Division of Urology, Department of Surgery/Department of Microbiology and ImmunologyWestern UniversityLondonCanada
  5. 5.Pre-Health Science, School of Health SciencesFanshawe CollegeLondonCanada
  6. 6.Department of Microbiology and ImmunologyWestern UniversityLondonCanada

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