Enterococcus faecalis subverts and invades the host urothelium in patients with chronic urinary tract infection

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Horsley, Harry ^a   Malone Lee, James ^a   Holland, David ^a   Tuz, Madeleine ^a   Hibbert, Andrew ^b   Kelsey, Michael ^c   Kupelian, Anthony ^a   Rohn, Jennifer L ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b ROYAL VETERINARY COLLEGE   (United Kingdom)

^c WHITTINGTON HOSPITAL NHS TRUST   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ARTICLE; BACTERIUM CULTURE; BLADDER DISEASE; CANCER CELL CULTURE; CELL INVASION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENTEROCOCCUS FAECALIS; ESCHERICHIA COLI; FEMALE; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; INFLAMMATION; LOWER URINARY TRACT SYMPTOM; MAJOR CLINICAL STUDY; NONHUMAN; TRANSITIONAL CELL CARCINOMA; URINARY TRACT INFECTION; UROTHELIUM;

ADULT; CELLS, CULTURED; CHRONIC DISEASE; ENTEROCOCCUS FAECALIS; HUMANS; LONDON; MICROSCOPY, FLUORESCENCE; URINARY BLADDER; URINARY TRACT INFECTIONS; UROTHELIUM;

EID: 84892577709     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0083637     Document Type: Article

References (63)

1. Foxman B (2000) Urinary tract infection: self-reported incidence and associated costs. Ann Epidemiol 10: 509-515. doi:10.1016/S1047-2797(00)00072-7. PubMed: 11118930.
2. Foxman B (2002) Epidemiology of urinary tract infections: incidence, morbidity, and economic costs. Am J Med 113(Suppl 1A): 5S. doi: 10.1016/S0002-9343(02)01054-9. PubMed: 1211386612601337.
3. Hooton TM (2001) Recurrent urinary tract infection in women. Int J Antimicrob Agents 17: 259-268. doi:10.1016/S0924-8579(00)00350-2. PubMed: 11295405.
4. Pouwels KB, Visser ST, Hak E (2013) Effect of pravastatin and fosinopril on recurrent urinary tract infections. J Antimicrob Chemother 68: 708-714. doi:10.1093/jac/dks419. PubMed: 23111852.
5. Hunstad DA (2010) Intracellular lifestyles and immune evasion strategies of uropathogenic Escherichia coli. Annu Rev Microbiol 64: 203-221. doi:10.1146/annurev.micro.112408.134258. PubMed: 20825346.
6. Colgan R (2011) Diagnosis and treatment of acute uncomplicated cystitis. Am Fam Physician 84: 771-776. PubMed: 22010614.
7. Abrams P (2003) The standardisation of terminology in lower urinary tract function: report from the standardisation sub-committee of the International Continence Society. Urology 61: 37-49. doi:10.1016/S0090-4295(02)02243-4. PubMed: 12559262.
8. National Institute for Health and Clinical Excellence (2006) Urinary incontinence: the management of urinary incontinence in women. Available: http://www.nice.org.uk/nicemedia/live/10996/30281/30281.pdf. Accessed 10 June 2013
9. Gormley EA, Lightner DJ, Burgio KL, Chai TC, Clemens JQ, et al. (2012) Diagnosis and treatment of overactive bladder (non-neurogenic) in adults: AUA/SUFU guideline. J Urol 188: 2455-2463. Available online at: S0022-5347(12)04959-2 [pii] doi:10.1016/j.juro.2012.09.079.
10. Lutters M, Vogt-Ferrier NB (2008) Antibiotic duration for treating uncomplicated, symptomatic lower urinary tract infections in elderly women. Cochrane Database of Systematic Reviews. doi: 10.1002/14651858.CD001535.pub2. PubMed: 1864607412137628.
11. Coyne KS, Sexton CC, Thompson CL, Milsom I, Irwin D et al. (2009) The prevalence of lower urinary tract symptoms (LUTS) in the USA, the UK and Sweden: results from the Epidemiology of LUTS (EpiLUTS) study. BJU Int 104: 352-360. doi:10.1111/j.1464-410X.2009.08427.x. PubMed: 19281467.
12. Irwin DE, Milsom I, Hunskaar S, Reilly K, Kopp Z et al. (2006) Population-Based Survey of Urinary Incontinence, Overactive Bladder, and Other Lower Urinary Tract Symptoms in Five Countries : Results of the EPIC Study. European Urology: 1306-1315.
13. Perry S, Shaw C, Assassa P, Dallosso H, Williams K et al. (2000) An epidemiological study to establish the prevalence of urinary symptoms and felt need in the community: the Leicestershire MRC incontinence study. Journal of Public Health 22: 427-434. doi:10.1093/pubmed/22.3.427.
14. Stamm WE (1982) Diagnosis of coliform infection in acutely dysuric women. N Engl J Med 307: 463-468. doi:10.1056/NEJM198208193070802. PubMed: 7099208.
15. Khasriya R, Khan S, Lunawat R, Bishara S, Bignall J et al. (2010) The Inadequacy of Urinary Dipstick and Microscopy as Surrogate Markers of Urinary Tract Infection in Urological Outpatients With Lower Urinary Tract Symptoms Without Acute Frequency and Dysuria. J Urol 183: 1843-1847. doi:10.1016/j.juro. 2010.01.008. PubMed: 20303096.
16. Kupelian AS, Horsley H, Khasriya R, Amussah RT, Badiani R et al. (2013) Discrediting microscopic pyuria and leucocyte esterase as diagnostic surrogates for infection in patients with lower urinary tract symptoms: results from a clinical and laboratory evaluation. BJU Int 112: 231-238. doi:10.1111/j.1464- 410X.2012.11694.x. PubMed: 23305196.
17. Chapple CR, Wein AJ, Abrams P, Dmochowski RR, Giuliano F et al. (2008) Lower Urinary Tract Symptoms Revisited: A Broader Clinical Perspective. European Urology 54: 563-569. doi:10.1016/j.eururo. 2008.03.109.
18. Nakipoglu GF, Kaya AZ, Orhan G, Tezen O, Tunc H et al. (2009) Urinary dysfunction in multiple sclerosis. J Clin Neurosci 16: 1321-1324. doi:10.1016/j.jocn.2008.12.012. PubMed: 19560927.
19. Khasriya R, Sathiananthamoorthy S, Ismail S, Kelsey M, Wilson M, et al. (2013) The spectrum of bacterial colonisation associated with urothelial cells from patients with chronic lower urinary tract symptoms. J Clin Microbiol. doi:10.1128/JCM.03314-12.
20. Foxman B (2003) Epidemiology of urinary tract infections: Incidence, morbidity, and economic costs. Disease-a-Month 49: 53-70. doi: 10.1067/mda.2003.7. PubMed: 12601337.
21. Anderson GG, Martin SM, Hultgren SJ (2004) Host subversion by formation of intracellular bacterial communities in the urinary tract. Microbes Infect 6: 1094-1101. PubMed: 15380779.
22. Anderson GG (2004) Intracellular bacterial communities of uropathogenic Escherichia coli in urinary tract pathogenesis. Trends Microbiol 12: 424-430. doi:10.1016/j.tim.2004.07.005. PubMed: 15337164.
23. Anderson GG, Palermo JJ, Schilling JD, Roth R, Heuser J et al. (2003) Intracellular Bacterial Biofilm-Like Pods in Urinary Tract Infections. Science 301: 105-107. doi:10.1126/science.1084550. PubMed: 12843396.
24. Rosen DA, Hooton TM, Stamm WE, Humphrey PA, Hultgren SJ (2007) Detection of Intracellular Bacterial Communities in Human Urinary Tract. Infection - PLOS Med 4: e329. doi:10.1371/journal.pmed. 0040329.
25. Justice SS (2004) Differentiation and developmental pathways of uropathogenic Escherichia coli in urinary tract pathogenesis. Proc Natl Acad Sci U S A 101: 1333-1338. doi:10.1073/pnas.0308125100. PubMed: 14739341.
26. Blango MG, Mulvey MA (2010) Persistence of Uropathogenic Escherichia coli in the Face of Multiple Antibiotics. Antimicrobial Agents and Chemotherapy 54: 1855-1863. doi:10.1128/AAC.00014-10.
27. Garofalo CK, Hooton TM, Martin SM, Stamm WE, Palermo JJ et al. (2007) Escherichia coli from Urine of Female Patients with Urinary Tract Infections Is Competent for Intracellular Bacterial Community Formation. Infect Immun 75: 52-60. doi:10.1128/IAI.01123-06. PubMed: 17074856.
28. Dalal E (1994) Moderate stress protects female mice against bacterial-infection of the bladder by eliciting uroepithelial shedding. Infect Immun 62: 5505-5510. PubMed: 7960132.
29. Smith YC (2008) 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 76: 2978-2990. doi:10.1128/IAI.00075-08. PubMed: 18443089.
30. Thumbikat P (2009) Bacteria-Induced Uroplakin Signaling Mediates Bladder Response to Infection. PLoS Pathog 5: e1000415. PubMed: 19412341.
31. Hannan TJ, Mysorekar IU, Hung CS, Isaacson-Schmid ML, Hultgren SJ (2010) Early severe inflammatory responses to uropathogenic E. coli predispose to chronic and recurrent urinary tract infection. PLoS Pathog 6: e1001042. doi:10.1371/journal.ppat.1001042. PubMed: 20811584.
32. Mysorekar IU, Hultgren SJ (2006) Mechanisms of uropathogenic Escherichia coli persistence and eradication from the urinary tract. Proc Natl Acad Sci U S A 103: 14170-14175. doi:10.1073/pnas.0602136103. PubMed: 16968784.
33. Russo TA (1995) Chromosomal restriction fragment length polymorphism analysis of Escherichia coli strains causing recurrent urinary tract infections in young women. J Infect Dis 172: 440-445. doi: 10.1093/infdis/172.2.440. PubMed: 7622887.
34. Cass AS (1985) Antibacterial perineal washing for prevention of recurrent urinary tract infections. Urology 25: 492-494. doi: 10.1016/0090-4295(85)90458- 3. PubMed: 3992773.
35. Brauner A (1992) Urinary Escherichia coli causing recurrent infections - a prospective follow-up of biochemical phenotypes. Clin Nephrol 38: 318-323. PubMed: 1468162.
36. Szabados F (2008) Staphylococcus saprophyticus ATCC 15305 is internalized into human urinary bladder carcinoma cell line 5637. FEMS Microbiol Lett 285: 163-169. doi:10.1111/j.1574-6968.2008.01218.x. PubMed: 18573154.
37. Rosen DA (2008) Utilization of an intracellular bacterial community pathway in Klebsiella pneumoniae urinary tract infection and the effects of fimK on type 1 pilus expression. Infect Immun 76: 3337-3345. doi: 10.1128/IAI.00090-08. PubMed: 18411285.
38. Mandell GL (1973) Interaction of intraleukocytic bacteria and antibiotics. J Clin Invest 52: 1673-1679. doi:10.1172/JCI107348. PubMed: 4718959.
39. Edwards AM, Massey RC (2011) Invasion of Human Cells by a Bacterial Pathogen. J Vis Exp: e2693. PubMed: 21445052.
40. Mohamed JA, Huang DB (2007) Biofilm formation by Enterococci. J Med Microbiol 56: 1581-1588. doi:10.1099/jmm.0.47331-0. PubMed: 18033823.
41. Chai WL, Hamimah H, Cheng SC, Sallam AA, Abdullah M (2007) Susceptibility of Enterococcus faecalis biofilm to antibiotics and calcium hydroxide. J Oral Sci 49: 161-166.
42. Guiton PS, Hannan TJ, Ford B, Caparon MG, Hultgren SJ (2013) Enterococcus faecalis overcomes foreign body-mediated inflammation to establish urinary tract infections. Infect Immun 81: 329-339. doi: 10.1128/IAI.00856-12. PubMed: 23132492.
43. Poulsen L, Bisgaard M, Son N, Trung N, An H et al. (2012) Enterococcus and Streptococcus spp. associated with chronic and self-medicated urinary tract infections in Vietnam. BMC Infectious Diseases 12: 320. doi:10.1186/1471-2334- 12-320.
44. Felmingham D, Wilson AP, Quintana AI, Grüneberg RN (1992) Enterococcus species in urinary tract infection. Clin Infect Dis 15: 295-301. doi:10.1093/clinids/15.2.295. PubMed: 1387807.
45. Hanin A, Sava I, Bao Y, Huebner J, Hartke A et al. (2010) Screening of In Vivo activated genes in Enterococcus faecalis during insect and mouse infections and growth in urine. PLOS ONE 5: e11879. doi: 10.1371/journal.pone. 0011879. PubMed: 20686694.
46. Nichol KA, Sill M, Laing NM, Johnson JL, Hoban DJ et al. (2006) Molecular epidemiology of urinary tract isolates of vancomycin-resistant Enterococcus faecium from North America. Int J Antimicrob Agents 27: 392-396. doi:10.1016/j.ijantimicag.2005.12.006. PubMed: 16621463.
47. Swaminathan S, Alangaden GJ (2010) Treatment of resistant Enterococcal urinary tract infections. Curr Infect Dis Rep 12: 455-464. doi:10.1007/s11908- 010-0138-8. PubMed: 21308555.
48. Dukes C (1928) Some Observations on Pyuria. Proc R Soc Med 21: 1179-1183. PubMed: 19986501.
49. Gill K, Kupelian AS, Swarmy S, Malone-Lee J (2011) The Problem of Pyuria 1-9 wbc ul-1; Are We Missing Significant Disease. Int Urogynecol J 22: 1769-2008. doi:10.1007/s00192-011-1521-1.
50. Wu XR, Lin JH, Walz T, Häner M, Yu J et al. (1994) Mammalian uroplakins. A group of highly conserved urothelial differentiation-related membrane proteins. J Biol Chem 269: 13716-13724. PubMed: 8175808.
51. Wu XR, Manabe M, Yu J, Sun TT (1990) Large scale purification and immunolocalization of bovine uroplakins I, II, and III. Molecular markers of urothelial differentiation. J Biol Chem 265: 19170-19179.
52. Sizemore RK, Caldwell JJ, Kendrick AS (1990) Alternate gram staining technique using a fluorescent lectin. Appl Environ Microbiol 56: 2245-2247. PubMed: 1697149.
53. Romero R, Schaudinn C, Kusanovic JP, Gorur A, Gotsch F et al. (2008) Detection of a microbial biofilm in intraamniotic infection. Am J Obstet Gynecol 198: 135. PubMed: 18166328.
54. Stender H (2003) PNA FISH: an intelligent stain for rapid diagnosis of infectious diseases. Expert Rev Mol Diagn 3: 649-655. doi: 10.1586/14737159.3.5. 649. PubMed: 14510184.
55. Rosen DA, Pinkner JS, Walker JN, Elam JS, Jones JM et al. (2008) Molecular variations in Klebsiella pneumoniae and Escherichia coli FimH affect function and pathogenesis in the urinary tract. Infect Immun 76: 3346-3356. doi:10.1128/IAI.00340-08. PubMed: 18474655.
56. Snyder JA, Lloyd AL, Lockatell CV, Johnson DE, Mobley HLT (2006) Role of phase variation of type 1 fimbriae in a uropathogenic Escherichia coli cystitis isolate during urinary tract infection. Infect Immun 74: 1387-1393. doi:10.1128/IAI.74.2.1387-1393.2006. PubMed: 16428790.
57. Wright KJ (2006) Sticky fibers and uropathogenesis: bacterial adhesins in the urinary tract. Future Microbiol 1: 75-87. doi: 10.2217/17460913.1.1.75. PubMed: 17661687.
58. Wright KJ (2007) Development of intracellular bacterial communities of uropathogenic Escherichia coli depends on type 1 pili. Cell Microbiol 9: 2230-2241. doi:10.1111/j.1462-5822.2007.00952.x. PubMed: 17490405.
59. Schembri MA, Klemm P (2001) Biofilm formation in a hydrodynamic environment by novel FimH variants and ramifications for virulence. Infect Immun 69: 1322-1328. doi:10.1128/IAI.69.3.1322-1328.2001. PubMed: 11179294.
60. Sava IG, Heikens E, Huebner J (2010) Pathogenesis and immunity in enterococcal infections. Clin Microbiol Infect 16: 533-540. doi:10.1111/j.1469- 0691.2010.03213.x. PubMed: 20569264.
61. Sartingen S, Rozdzinski E, Muscholl-Silberhorn A, Marre R (2000) Aggregation substance increases adherence and internalization, but not translocation, of Enterococcus faecalis through different intestinal epithelial cells in vitro. Infect Immun 68: 6044-6047. doi:10.1128/IAI.68.10.6044-6047. 2000. PubMed: 10992519.
62. Bubeník J, Baresová M, Viklický V, Jakoubková J, Sainerová H et al. (1973) Established cell line of urinary bladder carcinoma (T24) containing tumour-specific antigen. Int J Cancer 11: 765-773. doi: 10.1002/ijc.2910110327. PubMed: 4133950.
63. Eto DS (2006) Actin-gated intracellular growth and resurgence of uropathogenic Escherichia coli. Cell Microbiol 8: 704-717. doi: 10.1111/j.1462-5822.2006.00691.x. PubMed: 16548895.