1887

Abstract

Urinary tract infections (UTIs) caused by uropathogenic (UPEC) are amongst the most common bacterial infectious diseases in the developed world. The urovirulence of UPEC is mainly associated with the surface-exposed fimbrial adhesins and adhesins of the autotransporter (AT) family. The best studied of these proteins is antigen Ag43 mediating cell aggregation, adhesion and biofilm development as the causes of chronic UTIs. The IH11128 Dr ( ) strain of the Dr/Afa family of adhesins possesses two major surface-exposed virulence factors: Dr fimbrial polyadhesin and DraD protein (fimbrial tip subunit or protein component of the adhesive sheath). Here, we identified for the first time, to our knowledge, the gene encoding Ag43 in the WT clinical isolate of UPEC Dr as a new virulence factor not yet tested. We also found that Dr fimbrial expression, which like Ag43 is under the control of a phase-variable mechanism, did not exclude Ag43 surface presentation. However, the presence of Dr fimbriae supported by other structures on the cell surface caused a physical neutralization of Ag43-mediated autoaggregation during growth. The fimbrial bundling further increased the distance between the adjacent Ag43 cells, thus preventing head-to-tail association between surface-exposed Ag43 subunits and their interactions with the host cells. The investigations showed that Ag43 did not act as a specific adhesin and invasin, conversely to the major virulence factors of Dr, but played significant roles in the viability and metabolic activity of bacterial cells forming biofilm, and in the survival of bacteria within invaded epithelial cells.

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2015-05-01
2019-10-19
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References

  1. Adam B. , Baillie G. S. , Douglas L. J. . ( 2002;). Mixed species biofilms of Candida albicans and Staphylococcus epidermidis . . J Med Microbiol 51:, 344–349 Medline.
    [Google Scholar]
  2. Anderson G. G. , Palermo J. J. , Schilling J. D. , Roth R. , Heuser J. , Hultgren S. J. . ( 2003;). Intracellular bacterial biofilm-like pods in urinary tract infections. . Science 301:, 105–107 doi:10.1126/science.1084550 Medline.[CrossRef]
    [Google Scholar]
  3. Anderson K. L. , Billington J. , Pettigrew D. , Cota E. , Simpson P. , Roversi P. , Chen H. A. , Urvil P. , du Merle L. , Barlow P. N. . ( 2004;). An atomic resolution model for assembly, architecture, and function of the Dr adhesins. . Mol Cell 15:, 647–657 doi:10.1016/j.molcel.2004.08.003 Medline.[CrossRef]
    [Google Scholar]
  4. Blattner F. R. , Plunkett G. III , Bloch C. A. , Perna N. T. , Burland V. , Riley M. , Collado-Vides J. , Glasner J. D. , Rode C. K. , other authors . ( 1997;). The complete genome sequence of Escherichia coli K-12. . Science 277:, 1453–1462 doi:10.1126/science.277.5331.1453 Medline.[CrossRef]
    [Google Scholar]
  5. Blomfield I. C. , McClain M. S. , Princ J. A. , Calie P. J. , Eisenstein B. I. . ( 1991;). Type 1 fimbriation and fimE mutants of Escherichia coli K-12. . J Bacteriol 173:, 5298–5307 Medline.
    [Google Scholar]
  6. Caffrey P. , Owen P. . ( 1989;). Purification and N-terminal sequence of the alpha subunit of antigen 43, a unique protein complex associated with the outer membrane of Escherichia coli . . J Bacteriol 171:, 3634–3640 Medline.
    [Google Scholar]
  7. Celik N. , Webb C. T. , Leyton D. L. , Holt K. E. , Heinz E. , Gorrell R. , Kwok T. , Naderer T. , Strugnell R. A. , other authors . ( 2012;). A bioinformatic strategy for the detection, classification and analysis of bacterial autotransporters. . PLoS One 7:, e43245 doi:10.1371/journal.pone.0043245 Medline.[CrossRef]
    [Google Scholar]
  8. Chen S. L. , Hung C. S. , Xu J. , Reigstad C. S. , Magrini V. , Sabo A. , Blasiar D. , Bieri T. , Meyer R. R. , other authors . ( 2006;). Identification of genes subject to positive selection in uropathogenic strains of Escherichia coli: a comparative genomics approach. . Proc Natl Acad Sci U S A 103:, 5977–5982 doi:10.1073/pnas.0600938103 Medline.[CrossRef]
    [Google Scholar]
  9. Cota E. , Jones C. , Simpson P. , Altroff H. , Anderson K. L. , du Merle L. , Guignot J. , Servin A. , Le Bouguénec C. , other authors . ( 2006;). The solution structure of the invasive tip complex from Afa/Dr fibrils. . Mol Microbiol 62:, 356–366 doi:10.1111/j.1365-2958.2006.05375.x Medline.[CrossRef]
    [Google Scholar]
  10. Danese P. N. , Pratt L. A. , Dove S. L. , Kolter R. . ( 2000;). The outer membrane protein, antigen 43, mediates cell-to-cell interactions within Escherichia coli biofilms. . Mol Microbiol 37:, 424–432 doi:10.1046/j.1365-2958.2000.02008.x Medline.[CrossRef]
    [Google Scholar]
  11. Diderichsen B. . ( 1980;). flu, a metastable gene controlling surface properties of Escherichia coli . . J Bacteriol 141:, 858–867 Medline.
    [Google Scholar]
  12. Eto D. S. , Sundsbak J. L. , Mulvey M. A. . ( 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 Medline.[CrossRef]
    [Google Scholar]
  13. Fang L. , Nowicki B. , Yallampalli C. . ( 2001;). Differential expression of uterine NO in pregnant and nonpregnant rats with intrauterine bacterial infection. . Am J Physiol Regul Integr Comp Physiol 280:, R1356–R1363 Medline.
    [Google Scholar]
  14. Foxman B. . ( 1990;). Recurring urinary tract infection: incidence and risk factors. . Am J Public Health 80:, 331–333 doi:10.2105/AJPH.80.3.331 Medline.[CrossRef]
    [Google Scholar]
  15. Foxman B. . ( 2002;). Epidemiology of urinary tract infections: incidence, morbidity, and economic costs. . Am J Med 113: (Suppl 1A), 5–13 doi:10.1016/S0002-9343(02)01054-9 Medline.[CrossRef]
    [Google Scholar]
  16. Foxman B. , Brown P. . ( 2003;). Epidemiology of urinary tract infections: transmission and risk factors, incidence, and costs. . Infect Dis Clin North Am 17:, 227–241 doi:10.1016/S0891-5520(03)00005-9 Medline.[CrossRef]
    [Google Scholar]
  17. Foxman B. , Zhang L. , Tallman P. , Palin K. , Rode C. , Bloch C. , Gillespie B. , Marrs C. F. . ( 1995;). Virulence characteristics of Escherichia coli causing first urinary tract infection predict risk of second infection. . J Infect Dis 172:, 1536–1541 doi:10.1093/infdis/172.6.1536 Medline.[CrossRef]
    [Google Scholar]
  18. Frazier C. L. , San Filippo J. , Lambowitz A. M. , Mills D. A. . ( 2003;). Genetic manipulation of Lactococcus lactis by using targeted group II introns: generation of stable insertions without selection. . Appl Environ Microbiol 69:, 1121–1128 doi:10.1128/AEM.69.2.1121-1128.2003 Medline.[CrossRef]
    [Google Scholar]
  19. Gabrielson J. , Hart M. , Jarelöv A. , Kühn I. , McKenzie D. , Möllby R. . ( 2002;). Evaluation of redox indicators and the use of digital scanners and spectrophotometer for quantification of microbial growth in microplates. . J Microbiol Methods 50:, 63–73 doi:10.1016/S0167-7012(02)00011-8 Medline.[CrossRef]
    [Google Scholar]
  20. Garcia M. I. , Jouve M. , Nataro J. P. , Gounon P. , Le Bouguénec C. . ( 2000;). Characterization of the AfaD-like family of invasins encoded by pathogenic Escherichia coli associated with intestinal and extra-intestinal infections. . FEBS Lett 479:, 111–117 doi:10.1016/S0014-5793(00)01898-6 Medline.[CrossRef]
    [Google Scholar]
  21. Goluszko P. , Popov V. , Selvarangan R. , Nowicki S. , Pham T. , Nowicki B. J. . ( 1997a;). Dr fimbriae operon of uropathogenic Escherichia coli mediate microtubule-dependent invasion to the HeLa epithelial cell line. . J Infect Dis 176:, 158–167 doi:10.1086/514018 Medline.[CrossRef]
    [Google Scholar]
  22. Goluszko P. , Moseley S. L. , Truong L. D. , Kaul A. , Williford J. R. , Selvarangan R. , Nowicki S. , Nowicki B. J. . ( 1997b;). Development of experimental model of chronic pyelonephritis with Escherichia coli O75 : K5:H-bearing Dr fimbriae: mutation in the dra region prevented tubulointerstitial nephritis. . J Clin Invest 99:, 1662–1672 doi:10.1172/JCI119329 Medline.[CrossRef]
    [Google Scholar]
  23. Goluszko P. , Niesel D. , Nowicki B. , Selvarangan R. , Nowicki S. , Hart A. , Pawelczyk E. , Das M. , Urvil P. , Hasan R. . ( 2001;). Dr operon-associated invasiveness of Escherichia coli from pregnant patients with pyelonephritis. . Infect Immun 69:, 4678–4680 doi:10.1128/IAI.69.7.4678-4680.2001 Medline.[CrossRef]
    [Google Scholar]
  24. Hasman H. , Chakraborty T. , Klemm P. . ( 1999;). Antigen-43-mediated autoaggregation of Escherichia coli is blocked by fimbriation. . J Bacteriol 181:, 4834–4841 Medline.
    [Google Scholar]
  25. Henderson I. R. , Nataro J. P. . ( 2001;). Virulence functions of autotransporter proteins. . Infect Immun 69:, 1231–1243 doi:10.1128/IAI.69.3.1231-1243.2001 Medline.[CrossRef]
    [Google Scholar]
  26. Henderson I. R. , Meehan M. , Owen P. . ( 1997;). Antigen 43, a phase-variable bipartite outer membrane protein, determines colony morphology and autoaggregation in Escherichia coli K-12. . FEMS Microbiol Lett 149:, 115–120 doi:10.1111/j.1574-6968.1997.tb10317.x Medline.[CrossRef]
    [Google Scholar]
  27. Henderson I. R. , Cappello R. , Nataro J. P. . ( 2000;). Autotransporter proteins, evolution and redefining protein secretion. . Trends Microbiol 8:, 529–532 doi:10.1016/S0966-842X(00)01853-9 Medline.[CrossRef]
    [Google Scholar]
  28. Henderson I. R. , Navarro-Garcia F. , Desvaux M. , Fernandez R. C. , Ala'Aldeen D. . ( 2004;). Type V protein secretion pathway: the autotransporter story. . Microbiol Mol Biol Rev 68:, 692–744 doi:10.1128/MMBR.68.4.692-744.2004 Medline.[CrossRef]
    [Google Scholar]
  29. Johnson J. R. . ( 1991;). Virulence factors in Escherichia coli urinary tract infection. . Clin Microbiol Rev 4:, 80–128 Medline.
    [Google Scholar]
  30. Jouve M. , Garcia M. I. , Courcoux P. , Labigne A. , Gounon P. , Le Bouguénec C. . ( 1997;). Adhesion to and invasion of HeLa cells by pathogenic Escherichia coli carrying the afa-3 gene cluster are mediated by the AfaE and AfaD proteins, respectively. . Infect Immun 65:, 4082–4089 Medline.
    [Google Scholar]
  31. Justice S. S. , Hung C. , Theriot J. A. , Fletcher D. A. , Anderson G. G. , Footer M. J. , Hultgren S. J. . ( 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 Medline.[CrossRef]
    [Google Scholar]
  32. Kajava A. V. , Steven A. C. . ( 2006;). The turn of the screw: variations of the abundant beta-solenoid motif in passenger domains of Type V secretory proteins. . J Struct Biol 155:, 306–315 doi:10.1016/j.jsb.2006.01.015 Medline.[CrossRef]
    [Google Scholar]
  33. Kajava A. V. , Cheng N. , Cleaver R. , Kessel M. , Simon M. N. , Willery E. , Jacob-Dubuisson F. , Locht C. , Steven A. C. . ( 2001;). Beta-helix model for the filamentous haemagglutinin adhesin of Bordetella pertussis and related bacterial secretory proteins. . Mol Microbiol 42:, 279–292 doi:10.1046/j.1365-2958.2001.02598.x Medline.[CrossRef]
    [Google Scholar]
  34. Klemm P. , Schembri M. A. . ( 2000;). Bacterial adhesins: function and structure. . Int J Med Microbiol 290:, 27–35 doi:10.1016/S1438-4221(00)80102-2 Medline.[CrossRef]
    [Google Scholar]
  35. Klemm P. , Hjerrild L. , Gjermansen M. , Schembri M. A. . ( 2004;). Structure-function analysis of the self-recognizing Antigen 43 autotransporter protein from Escherichia coli . . Mol Microbiol 51:, 283–296 doi:10.1046/j.1365-2958.2003.03833.x Medline.[CrossRef]
    [Google Scholar]
  36. Le Bouguénec C. , Servin A. L. . ( 2006;). Diffusely adherent Escherichia coli strains expressing Afa/Dr adhesins (Afa/Dr DAEC): hitherto unrecognized pathogens. . FEMS Microbiol Lett 256:, 185–194 doi:10.1111/j.1574-6968.2006.00144.x Medline.[CrossRef]
    [Google Scholar]
  37. McCluskey C. , Quinn J. P. , McGrath J. W. . ( 2005;). An evaluation of three new-generation tetrazolium salts for the measurement of respiratory activity in activated sludge microorganisms. . Microb Ecol 49:, 379–387 doi:10.1007/s00248-004-0012-z Medline.[CrossRef]
    [Google Scholar]
  38. Mobley H. L. , Green D. M. , Trifillis A. L. , Johnson D. E. , Chippendale G. R. , Lockatell C. V. , Jones B. D. , Warren J. W. . ( 1990;). Pyelonephritogenic Escherichia coli and killing of cultured human renal proximal tubular epithelial cells: role of hemolysin in some strains. . Infect Immun 58:, 1281–1289 Medline.
    [Google Scholar]
  39. Mulvey M. A. , Schilling J. D. , Hultgren S. J. . ( 2001;). Establishment of a persistent Escherichia coli reservoir during the acute phase of a bladder infection. . Infect Immun 69:, 4572–4579 doi:10.1128/IAI.69.7.4572-4579.2001 Medline.[CrossRef]
    [Google Scholar]
  40. Mysorekar I. U. , Hultgren S. J. . ( 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 Medline.[CrossRef]
    [Google Scholar]
  41. Nowicki B. , Barrish J. P. , Korhonen T. , Hull R. A. , Hull S. I. . ( 1987;). Molecular cloning of the Escherichia coli O75X adhesin. . Infect Immun 55:, 3168–3173 Medline.
    [Google Scholar]
  42. Nowicki B. , Truong L. , Moulds J. , Hull R. . ( 1988;). Presence of the Dr receptor in normal human tissues and its possible role in the pathogenesis of ascending urinary tract infection. . Am J Pathol 133:, 1–4 Medline.
    [Google Scholar]
  43. Nowicki B. , Svanborg-Edén C. , Hull R. , Hull S. . ( 1989;). Molecular analysis and epidemiology of the Dr hemagglutinin of uropathogenic Escherichia coli . . Infect Immun 57:, 446–451 Medline.
    [Google Scholar]
  44. Nowicki B. , Fang L. , Singhal J. , Nowicki S. , Yallampalli C. . ( 1997;). Lethal outcome of uterine infection in pregnant but not in nonpregnant rats and increased death rate with inhibition of nitric oxide. . Am J Reprod Immunol 38:, 309–312 doi:10.1111/j.1600-0897.1997.tb00521.x Medline.[CrossRef]
    [Google Scholar]
  45. Nowicki B. , Singhal J. , Fang L. , Nowicki S. , Yallampalli C. . ( 1999;). Inverse relationship between severity of experimental pyelonephritis and nitric oxide production in C3H/HeJ mice. . Infect Immun 67:, 2421–2427 Medline.
    [Google Scholar]
  46. Nowicki B. , Selvarangan R. , Nowicki S. . ( 2001;). Family of Escherichia coli Dr adhesins: decay-accelerating factor receptor recognition and invasiveness. . J Infect Dis 183: (Suppl 1), S24–S27 doi:10.1086/318846 Medline.[CrossRef]
    [Google Scholar]
  47. Oelschlaeger T. A. , Dobrindt U. , Hacker J. . ( 2002;). Pathogenicity islands of uropathogenic E. coli and the evolution of virulence. . Int J Antimicrob Agents 19:, 517–521 doi:10.1016/S0924-8579(02)00092-4 Medline.[CrossRef]
    [Google Scholar]
  48. Owen P. , Kaback H. R. . ( 1978;). Molecular structure of membrane vesicles from Escherichia coli . . Proc Natl Acad Sci U S A 75:, 3148–3152 doi:10.1073/pnas.75.7.3148 Medline.[CrossRef]
    [Google Scholar]
  49. Owen P. , Meehan M. , de Loughry-Doherty H. , Henderson I. . ( 1996;). Phase-variable outer membrane proteins in Escherichia coli . . FEMS Immunol Med Microbiol 16:, 63–76 doi:10.1111/j.1574-695X.1996.tb00124.x Medline.[CrossRef]
    [Google Scholar]
  50. Perutka J. , Wang W. , Goerlitz D. , Lambowitz A. M. . ( 2004;). Use of computer-designed group II introns to disrupt Escherichia coli DExH/D-box protein and DNA helicase genes. . J Mol Biol 336:, 421–439 doi:10.1016/j.jmb.2003.12.009 Medline.[CrossRef]
    [Google Scholar]
  51. Pettit R. K. , Weber C. A. , Kean M. J. , Hoffmann H. , Pettit G. R. , Tan R. , Franks K. S. , Horton M. L. . ( 2005;). Microplate Alamar blue assay for Staphylococcus epidermidis biofilm susceptibility testing. . Antimicrob Agents Chemother 49:, 2612–2617 doi:10.1128/AAC.49.7.2612-2617.2005 Medline.[CrossRef]
    [Google Scholar]
  52. Pia˛tek R. , Zalewska B. , Kolaj O. , Ferens M. , Nowicki B. , Kur J. . ( 2005;). Molecular aspects of biogenesis of Escherichia coli Dr fimbriae: characterization of DraB–DraE complexes. . Infect Immun 73:, 135–145 doi:10.1128/IAI.73.1.135-145.2005 Medline.[CrossRef]
    [Google Scholar]
  53. Plançon L. , Du Merle L. , Le Friec S. , Gounon P. , Jouve M. , Guignot J. , Servin A. , Le Bouguénec C. . ( 2003;). Recognition of the cellular beta1-chain integrin by the bacterial AfaD invasin is implicated in the internalization of afa-expressing pathogenic Escherichia coli strains. . Cell Microbiol 5:, 681–693 doi:10.1046/j.1462-5822.2003.00308.x Medline.[CrossRef]
    [Google Scholar]
  54. Rana T. , Hasan R. J. , Nowicki S. , Venkatarajan M. S. , Singh R. , Urvil P. T. , Popov V. , Braun W. A. , Popik W. , other authors . ( 2014;). Complement protective epitopes and CD55–microtubule complexes facilitate the invasion and intracellular persistence of uropathogenic Escherichia coli . . J Infect Dis 209:, 1066–1076 doi:10.1093/infdis/jit619 Medline.[CrossRef]
    [Google Scholar]
  55. Schembri M. A. , Klemm P. . ( 2001;). Coordinate gene regulation by fimbriae-induced signal transduction. . EMBO J 20:, 3074–3081 doi:10.1093/emboj/20.12.3074 Medline.[CrossRef]
    [Google Scholar]
  56. Schembri M. A. , Kjaergaard K. , Klemm P. . ( 2003;). Global gene expression in Escherichia coli biofilms. . Mol Microbiol 48:, 253–267 doi:10.1046/j.1365-2958.2003.03432.x Medline.[CrossRef]
    [Google Scholar]
  57. Servin A. L. . ( 2005;). Pathogenesis of Afa/Dr diffusely adhering Escherichia coli . . Clin Microbiol Rev 18:, 264–292 doi:10.1128/CMR.18.2.264-292.2005 Medline.[CrossRef]
    [Google Scholar]
  58. Sherlock O. , Schembri M. A. , Reisner A. , Klemm P. . ( 2004;). Novel roles for the AIDA adhesin from diarrheagenic Escherichia coli: cell aggregation and biofilm formation. . J Bacteriol 186:, 8058–8065 doi:10.1128/JB.186.23.8058-8065.2004 Medline.[CrossRef]
    [Google Scholar]
  59. Ulett G. C. , Valle J. , Beloin C. , Sherlock O. , Ghigo J. M. , Schembri M. A. . ( 2007;). Functional analysis of antigen 43 in uropathogenic Escherichia coli reveals a role in long-term persistence in the urinary tract. . Infect Immun 75:, 3233–3244 doi:10.1128/IAI.01952-06 Medline.[CrossRef]
    [Google Scholar]
  60. van der Woude M. W. , Henderson I. R. . ( 2008;). Regulation and function of Ag43 (flu). . Annu Rev Microbiol 62:, 153–169 doi:10.1146/annurev.micro.62.081307.162938 Medline.[CrossRef]
    [Google Scholar]
  61. van der Woude M. W. , Braaten B. A. , Low D. A. . ( 1992;). Evidence for global regulatory control of pilus expression in Escherichia coli by Lrp and DNA methylation: model building based on analysis of pap . . Mol Microbiol 6:, 2429–2435 doi:10.1111/j.1365-2958.1992.tb01418.x Medline.[CrossRef]
    [Google Scholar]
  62. Van Loy C. P. , Sokurenko E. V. , Moseley S. L. . ( 2002;). The major structural subunits of Dr and fig1845 fimbriae are adhesins. . Infect Immun 70:, 1694–1702 doi:10.1128/IAI.70.4.1694-1702.2002 Medline.[CrossRef]
    [Google Scholar]
  63. Welch R. A. , Burland V. , Plunkett G. III , Redford P. , Roesch P. , Rasko D. , Buckles E. L. , Liou S. R. , Boutin A. , other authors . ( 2002;). Extensive mosaic structure revealed by the complete genome sequence of uropathogenic Escherichia coli . . Proc Natl Acad Sci U S A 99:, 17020–17024 doi:10.1073/pnas.252529799 Medline.[CrossRef]
    [Google Scholar]
  64. Wells T. J. , Totsika M. , Schembri M. A. . ( 2010;). Autotransporters of Escherichia coli: a sequence-based characterization. . Microbiology 156:, 2459–2469 doi:10.1099/mic.0.039024-0 Medline.[CrossRef]
    [Google Scholar]
  65. Wróblewska-Seniuk K. , Selvarangan R. , Hart A. , Pladzyk R. , Goluszko P. , Jafari A. , duMerle L. , Nowicki S. , Yallampalli C. , other authors . ( 2005;). Dra/AfaE adhesin of uropathogenic Dr/Afa+ Escherichia coli mediates mortality in pregnant rats. . Infect Immun 73:, 7597–7601 doi:10.1128/IAI.73.11.7597-7601.2005 Medline.[CrossRef]
    [Google Scholar]
  66. Wróblewska-Seniuk K. , Nowicki S. , Le Bouguénec C. , Nowicki B. , Yallampalli C. . ( 2011;). Maternal/fetal mortality and fetal growth restriction: role of nitric oxide and virulence factors in intrauterine infection in rats. . Am J Obstet Gynecol 205:, 83e1–83e7 doi:10.1016/j.ajog.2011.02.049 Medline.[CrossRef]
    [Google Scholar]
  67. Zalewska B. , Pia˛tek R. , Konopa G. , Nowicki B. , Nowicki S. , Kur J. . ( 2003;). Chimeric Dr fimbriae with a herpes simplex virus type 1 epitope as a model for a recombinant vaccine. . Infect Immun 71:, 5505–5513 doi:10.1128/IAI.71.10.5505-5513.2003 Medline.[CrossRef]
    [Google Scholar]
  68. Zalewska B. , Pia˛tek R. , Bury K. , Samet A. , Nowicki B. , Nowicki S. , Kur J. . ( 2005;). A surface-exposed DraD protein of uropathogenic Escherichia coli bearing Dr fimbriae may be expressed and secreted independently from DraC usher and DraE adhesin. . Microbiology 151:, 2477–2486 doi:10.1099/mic.0.28083-0 Medline.[CrossRef]
    [Google Scholar]
  69. Zalewska-Pia˛tek B. , Bury K. , Pia˛tek R. , Bruździak P. , Kur J. . ( 2008;). Type II secretory pathway for surface secretion of DraD invasin from the uropathogenic Escherichia coli Dr+ strain. . J Bacteriol 190:, 5044–5056 doi:10.1128/JB.00224-08 Medline.[CrossRef]
    [Google Scholar]
  70. Zalewska-Pia˛tek B. M. , Wilkanowicz S. I. , Pia˛tek R. J. , Kur J. W. . ( 2009;). Biofilm formation as a virulence determinant of uropathogenic Escherichia coli Dr+ strains. . Pol J Microbiol 58:, 223–229 Medline.
    [Google Scholar]
  71. Zalewska-Pia˛tek B. , Wilkanowicz S. , Bruździak P. , Pia˛tek R. , Kur J. . ( 2013;). Biochemical characteristic of biofilm of uropathogenic Escherichia coli Dr+ strains. . Microbiol Res 168:, 367–378 doi:10.1016/j.micres.2013.01.001 Medline.[CrossRef]
    [Google Scholar]
  72. Zhong J. , Karberg M. , Lambowitz A. M. . ( 2003;). Targeted and random bacterial gene disruption using a group II intron (targetron) vector containing a retrotransposition-activated selectable marker. . Nucleic Acids Res 31:, 1656–1664 doi:10.1093/nar/gkg248 Medline.[CrossRef]
    [Google Scholar]
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