Urinary tract infections of Escherichia coli strains of chaperone-usher system

• Autorzy: Zalewska-Piatek B.M.
• Języki publikacji: EN

Abstrakty

EN

Urinary tract infections are a very serious health and economic problem affecting millions of people each year worldwide. The most common etiologic agent of this type of bacterial infections, involving the upper and lower urinary tract, are E. coli strains representing approximately 80% of cases. Uropathogenic E. coli strains produce several urovirulence factors which can be divided into two main types, surface virulence factors and exported virulence factors. Surface-exposed structures include mainly extracellular adhesive organelles such as fimbriae/pili necessary in adhesion, invasion, biofilm formation and cytokine induction. Among the surface-exposed polymeric adhesive structures there are three most invasive groups, type 1 pili, type P pili and Dr family of adhesins which are bioassembled via the conserved, among Gram-negative bacteria, chaperone-usher secretion system. Type 1 and P-piliated E. coli cause cystitis and pyelonephritis. The Dr family of adhesins recognizing DAF receptor is responsible for cystitis, pyelonephritis (especially in pregnant women) and diarrhoea (in infants). In addition, Dr-positive E. coli strains carry the risk of recurrent urinary tract infections. Pyelonephritis in pregnant women leads to a series of complications such as bacteremia, urosepsis, acute respiratory distress syndrome and even death. In the era of increasing drug resistance of bacteria, the development of vaccines, drugs termed pilicides and inhibitors of adhesion may be a promising tool in the fight against urogenital infections.

Słowa kluczowe

EN

urinary tract; infection; Escherichia coli; bacterial strain; chaperone-usher system; kidney; human disease; etiological agent; virulence factor; clinical symptom; treatment; health problem

• Wydawca: -
• Czasopismo: Polish Journal of Microbiology
• Rocznik: 2011
• Tom: 60
• Numer: 4
• Opis fizyczny: s.279-285,ref.

Twórcy

autor

Zalewska-Piatek B.M.

• Department of Microbiology, Gdansk University of Technology, G.Narutowicza 11/12, 80-952 Gdansk, Poland

Bibliografia

• Anderson K.L., J. Billington, D. Pettigrew, E. Cota, P. Simpson, P. Roversi, H.A. Chen, P. Urvil, L. du Merle, P.N. Barlow and others. 2004. An atomic resolution model for assembly, architecture, and function of the Dr adhesins. Mol. Cell 15: 647–657.
• Arisoy M., D. Aysev, M. Ekim, D. Ozel, S.K. Köse, E.D. Ozsoy and N. Akar. 2006. Detection of virulence factors of Escherichia coli from children by multiplex polymerase chain reaction. Int. J. Clin. Pract. 60: 170–173.
• Avorn J., M. Monane, J.H. Gurwitz, R.J. Glynn, I. Choodnovskiy and L.A. Lipsitz. 1994. Reduction of bacteriuria and pyuria after ingestion of cranberry juice. JAMA. 271: 751–754.
• Bahrani-Mougeot F.K., E.L. Buckles, C.V. Lockatell, J.R. Hebel, D.E. Johnson, C.M. Tang and M.S. Donnenberg. 2002. Type 1 fimbriae and extracellular polysaccharides are preeminent uropathogenic Escherichia coli virulence determinants in the murine urinary tract. Mol. Microbiol. 45: 1079–1093.
• Barnhart M.M., J.S. Pinkner, G.E. Soto, F.G. Sauer, S. Langermann, G. Waksman, C. Frieden and S.J. Hultgren. PapD-like chaperones provide the missing information for folding of pilin proteins. Proc. Natl. Acad. Sci. USA. 97: 7709–7714.
• Berger C.N., O. Billker, T.F. Meyer, A.L. Servin and I. Kansau. 2004. Differential recognition of members of the carcinoembryonic antigen family by Afa/Dr adhesins of diffusely adhering Escherichia coli (Afa/Dr DAEC). Mol. Microbiol. 52: 963–983.
• Blum G., M. Ott, A. Lischewski, A. Ritter, H. Imrich, H. Tschäpe and J. Hacker. 1994. Excision of large DNA regions termed pathogenicity islands from tRNA-specific loci in the chromosome of an Escherichia coli wild-type pathogen. Infect. Immun. 62: 606–614.
• Bouckaert J., J. Berglund, M. Schembri, E. De Genst, L. Cools, M. Wuhrer, C.S. Hung, J. Pinkner, R. Slättegård, A. Zavialov and others. 2005. Receptor binding studies disclose a novel class of high-affinity inhibitors of the Escherichia coli FimH adhesin. Mol. Microbiol. 55: 441–455.
• Braun V., K. Hantke and W. Köster. 1998. Bacterial iron transport: mechanisms, genetics, and regulation. Met. Ions Biol. Syst. 35: 67–145.
• Capitani G., O. Eidam, R. Glockshuber and M.G. Grütter. 2006a. Structural and functional insights into the assembly of type 1 pili from Escherichia coli. Microbes Infect. 8: 2284–2290.
• Capitani G., O. Eidam and M.G. Grütter. 2006b. Evidence for a novel domain of bacterial outer membrane ushers. Proteins 65: 816–823.
• Caprioli A., V. Falbo, F.M. Ruggeri, L. Baldassarri, R. Bisicchia, G. Ippolito, E. Romoli and G. Donelli. 1987. Cytotoxic necrotizing factor production by hemolytic strains of Escherichia coli causing extraintestinal infections. J. Clin. Microbiol. 25: 146–149.
• Carnoy C. and S.L. Moseley. 1997. Mutational analysis of receptor binding mediated by the Dr family of Escherichia coli adhesins. Mol. Microbiol. 23: 365–379.
• Chorell E., J.S. Pinkner, G. Phan, S. Edvinsson, F. Buelens, H. Remaut, G. Waksman, S.J. Hultgren and F. Almqvist. 2010. Design and synthesis of C-2 substituted thiazolo and dihydrothiazolo ring-fused 2-pyridones: pilicides with increased antivirulence activity. J. Med. Chem. 53: 5690–5695.
• Connell I., W. Agace, P. Klemm, M. Schembri, S. Mărild and C. Svanborg. 1996. Type 1 fimbrial expression enhances Escherichia coli virulence for the urinary tract. Proc. Natl. Acad. Sci. USA. 93: 9827–9832.
• Cunningham F.G. and M.J. Lucas. 1994. Urinary tract infections complicating pregnancy. Baillieres Clin. Obstet. Gynaecol. 8: 353–373.
• Di Martino P., R. Agniel, K. David, C. Templer, J.L. Gaillard, P. Denys and H. Botto. 2006. Reduction of Escherichia coli adherence to uroepithelial bladder cells after consumption of cranberry juice: a double-blind randomized placebo-controlled cross-over trial. World J. Urol. 4: 21–27.
• Emödy L., M. Kerényi and G. Nagy. 2003. Virulence factors of uropathogenic Escherichia coli. Int. J. Antimicrob. Agents. 2: 29–33.
• Fiorentini C., A. Fabbri, P. Matarrese, L. Falzano, P. Boquet and W. Malorni. 1997. Hinderance of apoptosis and phagocytic behaviour induced by Escherichia coli cytotoxic necrotizing factor 1: two related activities in epithelial cells. Biochem. Biophys. Res. Commun. 241: 341–346.
• Firon N., S. Ashkenazi, D. Mirelman, I. Ofek and N. Sharon. 1987. Aromatic alpha-glycosides of mannose are powerful inhibitors of the adherence of type 1 fimbriated Escherichia coli to yeast and intestinal epithelial cells. Infect. Immun. 55: 472–476.
• Foxman B., L. Zhang, P. Tallman, K. Palin, C. Rode, C. Bloch, B. Gillespie and C.F. Marrs. 1995. Virulence characteristics of Esche richia coli causing first urinary tract infection predict risk of second infection. J. Infect. Dis. 172: 1536–1541.
• Foxman B. 2002. Epidemiology of urinary tract infections: incidence, morbidity, and economic costs. Am. J. Med. 113 Suppl. 1A: 5S–13S.
• Foxman B. 2003a. Epidemiology of urinary tract infections: incidence, morbidity, and economic costs. Dis. Mon. 49: 53–70.
• Foxman B. and P. Brown. 2003b. Epidemiology of urinary tract infections: transmission and risk factors, incidence, and costs. Infect. Dis. Clin. North. Am. 17: 227–241.
• Goluszko P., S.L. Moseley, L.D. Truong, A. Kaul, J.R. Williford, R. Selvarangan, S. Nowicki and B. Nowicki. 1997. 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.
• Goluszko P., R. Selvarangan, V. Popov, T. Pham, J.W. Wen and J. Singhal. 1999. Decay-accelerating factor and cytoskeleton redistribution pattern in HeLa cells infected with recombinant Escherichia coli strains expressing Dr family of adhesins. Infect. Immun. 67: 3989–3997.
• Guerinot M.L. 1994. Microbial iron transport. Annu. Rev. Microbiol. 48: 743–772.
• Guignot J., S. Hudault, I. Kansau, I. Chau and A.L. Servin. 2009. DAF and CEACAMs receptor-mediated internalization and lifestyle of Afa/Dr diffusely adhering Escherichia coli into epithelial cells. Infect. Immun. 77: 517–531.
• Gupta K. 2003. Emerging antibiotic resistance in urinary tract pathogens. Infect. Dis. Clin. North. Am. 17: 243–259.
• Gutierrez K. 1996. Continuation of antibiotic therapy for serious bacterial infections outside of the hospital. Pediatr. Ann. 25: 639–645.
• Guyer D.M., S. Radulovic, F.E. Jones and H.L. Mobley. 2002. Sat, the secreted autotransporter toxin of uropathogenic Escherichia coli, is a vacuolating cytotoxin for bladder and kidney epithelial cells. Infect. Immun. 70: 4539–4546.
• Hedenström M., H. Emtenäs, N. Pemberton, V. Aberg, S.J. Hultgren, J.S. Pinkner, V. Tegman, F. Almqvist, I. Sethson and J. Kihlberg. 2005. NMR studies of interactions between periplasmic chaperones from uropathogenic E. coli and pilicides that interfere with chaperone function and pilus assembly. Org. Biomol. Chem. 3: 4193–4200.
• Hacker J. and J.B. Kaper. 2000. Pathogenicity islands and the evolution of microbes. Annu. Rev. Microbiol. 54: 641–679.
• Hooton T. M. 2001. Recurrent urinary tract infection in women. Int. J. Antimicrob. Agents. 17: 259–268.
• Hooton T.M. and S.B. Levy. 2001. Antimicrobial resistance: a plan of action for community practice. Am. Fam. Physician. 63: 1087–1098.
• Hung D.L., S.D. Knight, R.M. Woods, J.S. Pinkner and S.J. Hultgren. 1996. Molecular basis of two subfamilies of immunoglobulinlike chaperones. EMBO J. 15: 3792–3805.
• Johnson J.R. and M. Kuskowski. 2000. Clonal origin, virulence factors, and virulence. Infect. Immun. 68: 424–425.
• Johnson J.R. 2003. Microbial virulence determinants and the pathogenesis of urinary tract infection. Infect. Dis. Clin. North. Am. 17: 261–278.
• Källenius G., R. Möllby, S.B. Svenson, I. Helin, H. Hultberg, B. Cedergren and J. Winberg. 1981. Occurrence of P-fimbriated Escherichia coli in urinary tract infections. Lancet. 2: 1369–1372.
• Keane W.F., R. Welch, G. Gekker and P.K. Peterson. 1987. Mechanism of Escherichia coli alpha-hemolysin-induced injury to isolated renal tubular cells. Am. J. Pathol. 126: 350–357.
• Knight S.D., J. Berglund and D. Choudhury. 2000. Bacterial adhesins: structural studies reveal chaperone function and pilus biogenesis. Curr. Opin. Chem. Biol. 4: 653–660.
• Kontiokari T., K. Sundqvist, M. Nuutinen, T. Pokka, M. Koskela and M. Uhari. 2001. Randomised trial of cranberry-lingonberry juice and Lactobacillus GG drink for the prevention of urinary tract infections in women. BMJ. 322:1571.
• Korotkova N., Y. Yang, I. Le Trong, E. Cota, B. Demeler, J. Marchant, W.E. Thomas, R.E. Stenkamp, S.L. Moseley and S. Matthews. 2008a. Binding of Dr adhesins of Escherichia coli to carcinoem bryonic antigen triggers receptor disssociation. Mol. Microbiol. 67: 420–434.
• Korotkova N., Y. Yarova-Yarovaya, V. Tchesnokova, N. Yazvenko, M.A. Carl, A.E. Stapleton and S.L. Moseley. 2008b. Escherichia coli DraE adhesin-associated bacterial internalization by epithelial cells is promoted independently by decay-accelerating factor and carcinoembryonic antigen-related cell adhesion molecule binding and does not require the DraD invasin. Infect. Immun. 76: 3869–3880.
• Labigne-Roussel A. and S. Falkow. 1988. Distribution and degree of heterogeneity of the afimbrial-adhesin-encoding operon (afa) among uropathogenic Escherichia coli isolates. Infect. Immun. 56: 640–648.
• Langermann S., R. Möllby, J.E. Burlein, S.R. Palaszynski, C.G. Auguste, A. DeFusco, R. Strouse, M.A. Schenerman, S.J. Hultgren, J.S. Pinkner and others. 2000. Vaccination with FimH adhesin protects cynomolgus monkeys from colonization and infection by uropathogenic Escherichia coli. J. Infect. Dis. 181: 774–778.
• Langermann S. and W.R. Jr Ballou. 2001. Vaccination utilizing the FimCH complex as a strategy to prevent Escherichia coli urinary tract infections. J. Infect. Dis. 183 Suppl 1: S84–S86.
• Le Bouguénec C. and A.L. Servin. 2006. Diffusely adherent Escherichia coli strains expressing Afa/Dr adhesins (Afa/Dr DAEC): hitherto unrecognized pathogens. FEMS Microbiol. Lett. 256: 185–194. Lewczyk E. and S. Jankowski. 2003. Urinary tract infections in children (in Polish). Adv. Clin. Exp. Med. 12: 375–380.
• Lund B., F. Lindberg, B.I. Marklund and S. Normark. 1987. The PapG protein is the alpha-D-galactopyranosyl-(1→4)-beta-Dgalactopyranose-binding adhesin of uropathogenic Escherichia coli. Proc. Natl. Acad. Sci. USA. 84: 5898–5902.
• Millar L.K. and S. M. Cox. 1997. Urinary tract infections complicating pregnancy. Infect. Dis. Clin. North. Am. 11: 13–26.
• Morrisom D.C. and J.L. Ryan. 1987. Endotoxins and disease mechanisms. Annu. Rev. Med. 38: 417–432.
• Mulvey M.A., Y.S. Lopez-Boado, C.L. Wilson, R. Roth, W.C. Parks, J. Heuser and S.J. Hultgren. 1998. Induction and evasion of host defenses by type 1-piliated uropathogenic Escherichia coli. Science. 282: 1494–1497.
• Nishiyama M., R. Horst, O. Eidam, T. Herrmann, O. Ignatov, M. Vetsch, P. Bettendorff, I. Jelesarov, M.G. Grütter, K. Wüthrich and others. 2005. Structural basis of chaperone-subunit complex recognition by the type 1 pilus assembly platform FimD. EMBO J. 24: 2075–2086.
• Nowicki B., J. Moulds, R. Hull and S. Hull. 1988. A hemagglutinin of uropathogenic Escherichia coli recognizes the Dr blood group antigen. Infect. Immun. 56: 1057–1060.
• Nowicki B., M. Martens, A. Hart and S. Nowicki. 1994. Gestational age-dependent distribution of Escherichia coli fimbriae in pregnant patients with pyelonephritis. Ann. NY Acad. Sci. 730: 290–91.
• Nowicki B., R. Selvarangan and S. Nowicki. 2001. Family of Escherichia coli Dr adhesins: decay-accelerating factor receptor recognition and invasiveness. J. Infect. Dis. Suppl 1 183: S24–27.
• Oelschlaeger T.A., U. Dobrindt and J. Hacker. 2002. Pathogenicity islands of uropathogenic E. coli and the evolution of virulence. Int. J. Antimicrob. Agents. 19: 517–521.
• Ofek I., D.L. Hasty and N. Sharon. 2003. Anti-adhesion therapy of bacterial diseases: prospects and problems. FEMS Immunol. Med. Microbiol. 38: 181–191.
• Ohlsson J., J. Jass, B.E. Uhlin, J. Kihlberg and U.J. Nilsson. 2002. Discovery of potent inhibitors of PapG adhesins from uropathogenic Escherichia coli through synthesis and evaluation of galabiose derivatives. Chembiochem. 3: 772–779.
• Piątek R., B. Zalewska, O. Kolaj, M. Ferens, B. Nowicki and J. Kur. 2005a. Molecular aspects of biogenesis of Escherichia coli Dr fimbriae: characterization of DraB-DraE complexes. Infect. Immun. 73: 135–145.
• Piątek R., B. Zalewska, K. Bury and J. Kur. 2005b. The chaperoneusher pathway of bacterial adhesin biogenesis – from molecular mechanism to strategies of anti-bacterial prevention and modern vaccine design. Acta Biochim. Pol. 52: 639–46.
• Picard B., J.S. Garcia, S. Gouriou, P. Duriez, N. Brahimi, E. Bingen, J. Elion and E. Denamur. 1999. The link between phylogeny and virulence in Escherichia coli extraintestinal infection. Infect. Immun. 67: 546–553.
• Pinkner J.S., H. Remaut, F. Buelens, E. Miller, V. Aberg, N. Pemberton, M. Hendenström, A. Larsson, P. Seed, G. Waksaman and others. 2006. Rationally designed small compounds inhibit pilus biogenesis in uropathogenic bacteria. Proc. Natl. Acad. Sci. USA. 103: 17897–17902.
• Pettigrew D., K.L. Anderson, J. Billington, E. Cota, P. Simpson, P. Urvil, F. Rabuzin, P. Roversi, B. Nowicki, L. du Merle and others. 2004. High resolution studies of the Afa/Dr adhesin DraE and its interaction with chloramphenicol. J. Biol. Chem. 279: 46851–46857.
• Remaut H., R.J. Rose, T.J. Hannan, S.J. Hultgren, S.E. Radford, A.E. Ashcroft and G. Waksman. 2006. Donor-strand exchange in chaperone-assisted pilus assembly proceeds through a concerted beta strand displacement mechanism. Mol. Cell. 22: 831–842.
• Rietschel E.T., H. Brade, O. Holst, L. Brade, S. Müller-Loennies, U. Mamat, U. Zähringer, F. Beckmann, U. Seydel, K. Brandenburg and others. 1996. Bacterial endotoxin: chemical constitution, biological recognition, host response, and immunological detoxification. Curr. Top Microbiol. Immunol. 216: 39–81.
• Roberts J.A., B.I. Marklund, D. Ilver, D. Haslam, M.B. Kaack, G. Baskin, M. Louis, R. Möllby, J. Winberg and S. Normark. 1994. The Gal(alpha 1–4)Gal-specific tip adhesin of Escherichia coli P-fimbriae is needed for pyelonephritis to occur in the normal urinary tract. Proc. Natl. Acad. Sci. USA. 91: 11889–11893.
• Ronald A. 2002. The etiology of urinary tract infection: traditional and emerging pathogens. Am. J. Med. 113 Suppl 1A: 14S–19S.
• Selvarangan R., P. Goluszko, J. Singhal, C. Carnoy, S. Moseley, B. Hudson, S. Nowicki and B. Nowicki. 2004. Interaction of Dr adhesin with collagen type IV is a critical step in Escherichia coli renal persistence. Infect. Immun. 72: 4827–4835.
• Saulino E.T., E. Bullitt and S.J. Hultgren. 2000. Snapshots of ushermediated protein secretion and ordered pilus assembly. Proc. Natl. Acad. Sci.USA. 97: 9240–9245.
• Sauer F.G., K. Futterer, J.S. Pinkner, K.W. Dodson, S.J. Hultgren and G. Waksman. 1999. Structural basis of chaperone function and pilus biogenesis. Science 285: 1058–1061.
• Sauer F.G., M. Barnhart, D. Choudhury, S.D. Knight, G. Waksman and S.J. Hultgren. 2000. Chaperone-assisted pilus assembly and bacterial attachment. Curr. Opin Struct Biol. 10: 548–556.
• Sauer F.G., H. Remaut, S.J. Hultgren and G. Waksman. 2004. Fiber assembly by the chaperone-usher pathway. Biochim. Biophys. Acta. 1694: 259–267.
• Schubert S., B. Picard, S. Gouriou, J. Heesemann and E. Denamur. 2002. Yersinia high-pathogenicity island contributes to virulence in Escherichia coli causing extraintestinal infections. Infect. Immun. 70: 5335–5337.
• Servin A.L. 2005. Pathogenesis of Afa/Dr diffusely adhering Escherichia coli. Int. J. Med. Microbiol. 295: 471–478.
• Selvarangan R., P. Goluszko, J. Singhal, C. Carnoy, S. Moseley, B. Hudson, S. Nowicki and B. Nowicki. 2004. Interaction of Dr adhesin with collagen type IV is a critical step in Escherichia coli renal persistence. Infect. Immun. 72: 4827–4835.
• Smith H.W. 1963. The haemolysins of Escherichia coli. J. Pathol. Bacteriol. 85: 197–211.
• Sobotová D. 2011. Urinary tract infections and chronic renal failure. Vnitr. Lek. 57: 626–630.
• Sokurenko E.V., V. Chesnokova, R.J. Doyle and D.L. Hasty. 1997. Diversity of the Escherichia coli type 1 fimbrial lectin. Differential binding to mannosides and uroepithelial cells. J. Biol. Chem. 272: 17880–17886.
• Stamm W.E. and T.M. Hooton. 1993. Management of urinary tract infections in adults. N. Engl. J. Med. 329: 1328–1334.
• Striker R., U. Nilsson, A. Stonecipher, G. Magnusson and S.J. Hultgren. 1995. Structural requirements for the glycolipid receptor of human uropathogenic Escherichia coli. 6: 1021–1029.
• Strömberg N., B.I. Marklund, B. Lund, D. Ilver, A. Hamers, W. Gaastra, K.A. Karlsson and S. Normark. 1990. Host-specificity of uropathogenic Escherichia coli depends on differences in binding specificity to Gal alpha 1-4Gal-containing isoreceptors. EMBO J. 9: 2001–2010.
• Strömberg N., P.G. Nyholm, I. Pascher and S. Normark. 1991. Saccharide orientation at the cell surface affects glycolipid receptor function. Proc. Natl. Acad. Sci. USA. 88: 9340–9344.
• Svensson A., A. Larsson, H. Emtenäs, M. Hedenström, T. Fex, S.J. Hultgren, J.S. Pinkner, F. Almqvist and J. Kihlberg. 2001. Design and evaluation of pilicides: potential novel antibacterial agents directed against uropathogenic Escherichia coli. Chembiochem. 2: 915–918.
• Thanassi D.G., E.T. Saulino and S.J. Hultgren. 1998. The chaperone/usher pathway: a major terminal branch of the general secretory pathway. Curr. Opin. Microbiol. 1: 223–231.
• Thanassi D.G., C. Stathopoulos, K. Dodson, D. Geiger and S.J. Hultgren. 2002. Bacterial outer membrane ushers contain distinct targeting and assembly domains for pilus biogenesis. J. Bacteriol. 184: 6260–6269.
• Thankavel K., B. Madison, T. Ikeda, R. Malaviya, A.H. Shah, P.M. Arumugam and S.N. Abraham. 1997. Localization of a domain in the FimH adhesin of Escherichia coli type 1 fimbriae capable of receptor recognition and use of a domain-specific antibody to confer protection against experimental urinary tract infection. Clin. Invest. 100: 1123–3116.
• Torres A.G. and S.M. Payne. 1997. Haem iron-transport system in enterohaemorrhagic Escherichia coli O157:H7. Mol. Microbiol. 23: 825–833.
• Ventura J.E., M. Villa, R. Mizraji and R. Ferreiros. 1997. Acute renal failure in pregnancy. Ren. Fail. 19: 217–220.
• Watson A.R. 1994. Urinary tract infection in early childhood. J. Antimicrob. Chemother. 34 Suppl A: 53–60.
• Westerlund B., P. Kuusela, J. Risteli, L. Risteli, T. Vartio, H. Rauvala, R. Virkola and T.K. Korhonen. 1989. The O75X adhesin of uropathogenic Escherichia coli is a type IV collagen-binding protein. Mol. Microbiol. 3: 329–337.
• White D.G. and P.F. McDrmott. 2001. Biocides, drug resistance and microbial evolution. Curr. Opin. Microbiol. 4: 313–317.
• Wright K.J. and S.J. Hultgren. 2006. Sticky fibers and uropathogenesis: bacterial adhesins in the urinary tract. Future Microbiol. 1: 75–87.
• Wyszyńska T. 1994. Urinary tract infections in children (in Polish). Klin. Pediatr. 2: 17–24.
• Yamamoto S. 2007. Molecular epidemiology of uropathogenic Esche richia coli. J. Infect. Chemother. 13: 68–73.
• Zafriri D., I. Ofek, R. Adar, M. Pocino and N. Sharon. 1989. Inhibitory activity of cranberry juice on adherence of type 1 and type P fimbriated Escherichia coli to eucaryotic cells. Antimicrob. Agents Chemother. 33: 92–98.
• Zavialov A.V., N.V. Batchikova, P. Korpela, L.E. Petrovskaya, V.G. Korobko, J. Kersley, S. MacIntyre and V.P. Zav’yalov. 2001. Secretion of recombinant proteins via the chaperone/usher pathway in Escherichia coli. Appl. Environ. Microbiol. 67: 1805–1814.
• Zavialov A.V., J. Kersley, T. Korpela, V.P. Zav’yalov, S. MacIntyre and S.D. Knight. 2002. Donor strand complementation mechanism in the biogenesis of non-pilus systems. Mol. Microbiol. 45: 983–995.
• Zavialov A.V., J. Berglund, A.F. Pudney, L.J. Fooks, T.M. Ibrahim, S. MacIntyre and S.D. Knight. 2003. Structure and biogenesis of the capsular F1 antigen from Yersinia pestis: preserved folding energy drives fiber formation. Cell 113: 587–596.
• Zavialov A.V., V.M. Tischenko, L.J. Fooks, B.O. Brandsdal, J. Aqvist, V.P. Zav’yalov, S. Macintyre and S.D. Knight. 2005. Resolving the energy paradox of chaperone/usher-mediated fibre assembly. Biochem. J. 389: 685–694.
• Zavialov A., G. Zav’yalova, T. Korpela and V. Zav’yalov. 2007. FGL chaperone-assembled fimbrial polyadhesins: anti-immune armament of Gram-negative bacterial pathogens. FEMS Microbiol. Rev. 31: 478–514.
• Zav’yalov V.P., G.A. Zav’yalova, A.I. Denesyuk, M. Gaestel and T. Korpela. 1995. Structural and functional homology between periplasmic bacterial molecular chaperones and small heat shock proteins. FEMS Immunol. Med. Microbiol. 11: 265–272.