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Review

Preventing urinary tract infection: progress toward an effective Escherichia coli vaccine

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Pages 663-676 | Published online: 09 Jan 2014

References

  • Foxman B. The epidemiology of urinary tract infection. Nat. Rev. Urol. 7(12), 653–660 (2010).
  • Foxman B, Brown P. Epidemiology of urinary tract infections: transmission and risk factors, incidence, and costs. Infect. Dis. Clin. North Am. 17(2), 227–241 (2003).
  • Foxman B, Gillespie B, Koopman J et al. Risk factors for second urinary tract infection among college women. Am. J. Epidemiol. 151(12), 1194–1205 (2000).
  • DeFrances CJ, Lucas CA, Buie VC, Golosinskiy A. 2006 National Hospital Discharge Survey. Natl Health Stat. Report. 5, 1–20 (2008).
  • Litwin MS, Saigal CS, Yano EM et al..; Urologic Diseases in America Project. Urologic diseases in America Project: analytical methods and principal findings. J. Urol. 173(3), 933–937 (2005).
  • Mühldorfer I. Emerging bacterial pathogens. Preface. Contrib. Microbiol. 8, XI–XIV (2001).
  • Mehnert-Kay SA. Diagnosis and management of uncomplicated urinary tract infections. Am. Fam. Physician 72(3), 451–456 (2005).
  • Zhang L, Foxman B. Molecular epidemiology of Escherichia coli mediated urinary tract infections. Front. Biosci. 8, e235–e244 (2003).
  • Johnson JR, Russo TA. Uropathogenic Escherichia coli as agents of diverse non-urinary tract extraintestinal infections. J. Infect. Dis. 186(6), 859–864 (2002).
  • Wiles TJ, Kulesus RR, Mulvey MA. Origins and virulence mechanisms of uropathogenic Escherichia coli. Exp. Mol. Pathol. 85(1), 11–19 (2008).
  • Welch RA, Burland V, Plunkett G 3rd et al. Extensive mosaic structure revealed by the complete genome sequence of uropathogenic Escherichia coli. Proc. Natl Acad. Sci. USA 99(26), 17020–17024 (2002).
  • Wright KJ, Hultgren SJ. Sticky fibers and uropathogenesis: bacterial adhesins in the urinary tract. Future Microbiol. 1(1), 75–87 (2006).
  • Kodner CM, Thomas Gupton EK. Recurrent urinary tract infections in women: diagnosis and management. Am. Fam. Physician 82(6), 638–643 (2010).
  • Gupta K, Hooton TM, Naber KG et al..; Infectious Diseases Society of America European Society for Microbiology and Infectious Diseases. International clinical practice guidelines for the treatment of acute uncomplicated cystitis and pyelonephritis in women: a 2010 update by the Infectious Diseases Society of America and the European Society for Microbiology and Infectious Diseases. Clin. Infect. Dis. 52(5), e103–e120 (2011).
  • Moura A, Nicolau A, Hooton T, Azeredo J. Antibiotherapy and pathogenesis of uncomplicated UTI: difficult relationships. J. Appl. Microbiol. 106(6), 1779–1791 (2009).
  • Foxman B, Ki M, Brown P. Antibiotic resistance and pyelonephritis. Clin. Infect. Dis. 45(3), 281–283 (2007).
  • Karaca Y, Coplu N, Gozalan A, Oncul O, Citil BE, Esen B. Co-trimoxazole and quinolone resistance in Escherichia coli isolated from urinary tract infections over the last 10 years. Int. J. Antimicrob. Agents 26(1), 75–77 (2005).
  • Gupta K, Hooton TM, Stamm WE. Increasing antimicrobial resistance and the management of uncomplicated community-acquired urinary tract infections. Ann. Intern. Med. 135(1), 41–50 (2001).
  • Zhanel GG, Hisanaga TL, Laing NM et al..; NAUTICA Group. Antibiotic resistance in outpatient urinary isolates: final results from the North American Urinary Tract Infection Collaborative Alliance (NAUTICA). Int. J. Antimicrob. Agents 26(5), 380–388 (2005).
  • Karlowsky JA, Hoban DJ, Decorby MR, Laing NM, Zhanel GG. Fluoroquinolone-resistant urinary isolates of Escherichia coli from outpatients are frequently multidrug resistant: results from the North American Urinary Tract Infection Collaborative Alliance-Quinolone Resistance study. Antimicrob. Agents Chemother. 50(6), 2251–2254 (2006).
  • Schito GC, Naber KG, Botto H et al. The ARESC study: an international survey on the antimicrobial resistance of pathogens involved in uncomplicated urinary tract infections. Int. J. Antimicrob. Agents 34(5), 407–413 (2009).
  • MacDonald TM, Beardon PH, McGilchrist MM, Duncan ID, McKendrick AD, McDevitt DG. The risks of symptomatic vaginal candidiasis after oral antibiotic therapy. Q. J. Med. 86(7), 419–424 (1993).
  • Bartlett JG. Narrative review: the new epidemic of Clostridium difficile-associated enteric disease. Ann. Intern. Med. 145(10), 758–764 (2006).
  • Dethlefsen L, Huse S, Sogin ML, Relman DA. The pervasive effects of an antibiotic on the human gut microbiota, as revealed by deep 16S rRNA sequencing. PLoS Biol. 6(11), e280 (2008).
  • Van Eldere J, Mera RM, Miller LA, Poupard JA, Amrine-Madsen H. Risk factors for development of multiple-class resistance to Streptococcus pneumoniae strains in Belgium over a 10-year period: antimicrobial consumption, population density, and geographic location. Antimicrob. Agents Chemother. 51(10), 3491–3497 (2007).
  • Billips BK, Schaeffer AJ, Klumpp DJ. Molecular basis of uropathogenic Escherichia coli evasion of the innate immune response in the bladder. Infect. Immun. 76(9), 3891–3900 (2008).
  • Sivick KE, Schaller MA, Smith SN, Mobley HL. The innate immune response to uropathogenic Escherichia coli involves IL-17A in a murine model of urinary tract infection. J. Immunol. 184(4), 2065–2075 (2010).
  • Kruze D, Holzbecher K, Andrial M, Bossart W. Urinary antibody response after immunisation with a vaccine against urinary tract infection. Urol. Res. 17(6), 361–366 (1989).
  • Kruze D, Biro K, Holzbecher K, Andrial M, Bossart W. Protection by a polyvalent vaccine against challenge infection and pyelonephritis. Urol. Res. 20(2), 177–181 (1992).
  • Uehling DT, James LJ, Hopkins WJ, Balish E. Immunization against urinary tract infection with a multi-valent vaginal vaccine. J. Urol. 146(1), 223–226 (1991).
  • Alteri CJ, Hagan EC, Sivick KE, Smith SN, Mobley HL. Mucosal immunization with iron receptor antigens protects against urinary tract infection. PLoS Pathog. 5(9), e1000586 (2009).
  • Thumbikat P, Waltenbaugh C, Schaeffer AJ, Klumpp DJ. Antigen-specific responses accelerate bacterial clearance in the bladder. J. Immunol. 176(5), 3080–3086 (2006).
  • Sivick KE, Mobley HL. An “omics” approach to uropathogenic Escherichia coli vaccinology. Trends Microbiol. 17(10), 431–432 (2009).
  • Lycke N. Targeted vaccine adjuvants based on modified cholera toxin. Curr. Mol. Med. 5(6), 591–597 (2005).
  • Holmgren J, Czerkinsky C, Eriksson K, Mharandi A. Mucosal immunisation and adjuvants: a brief overview of recent advances and challenges. Vaccine 21(Suppl. 2), S89–S95 (2003).
  • Scavone P, Rial A, Umpierrez A, Chabalgoity A, Zunino P. Effects of the administration of cholera toxin as a mucosal adjuvant on the immune and protective response induced by Proteus mirabilis MrpA fimbrial protein in the urinary tract. Microbiol. Immunol. 53(4), 233–240 (2009).
  • Chen DJ, Osterrieder N, Metzger SM et al. Delivery of foreign antigens by engineered outer membrane vesicle vaccines. Proc. Natl Acad. Sci. USA 107(7), 3099–3104 (2010).
  • McLachlan JB, Shelburne CP, Hart JP et al. Mast cell activators: a new class of highly effective vaccine adjuvants. Nat. Med. 14(5), 536–541 (2008).
  • Hung CS, Dodson KW, Hultgren SJ. A murine model of urinary tract infection. Nat. Protoc. 4(8), 1230–1243 (2009).
  • Fox JG. The Mouse in Biomedical Research. Elsevier, Amsterdam, The Netherlands (2007).
  • Hagan EC, Lloyd AL, Rasko DA, Faerber GJ, Mobley HL. Escherichia coli global gene expression in urine from women with urinary tract infection. PLoS Pathog. 6(11), e1001187 (2010).
  • Whitfield C. Biosynthesis and assembly of capsular polysaccharides in Escherichia coli. Annu. Rev. Biochem. 75, 39–68 (2006).
  • Buckles EL, Wang X, Lane MC et al. Role of the K2 capsule in Escherichia coli urinary tract infection and serum resistance. J. Infect. Dis. 199(11), 1689–1697 (2009).
  • Russo TA, Beanan JM, Olson R, MacDonald U, Cope JJ. Capsular polysaccharide and the O-specific antigen impede antibody binding: a potential obstacle for the successful development of an extraintestinal pathogenic Escherichia coli vaccine. Vaccine 27(3), 388–395 (2009).
  • Uehling DT, Wolf L. Enhancement of the bladder defense mechanism by immunization. Invest. Urol. 6(5), 520–526 (1969).
  • Kaijser B, Ahlstedt S. Protective capacity of antibodies against Escherichia coli and K antigens. Infect. Immun. 17(2), 286–289 (1977).
  • Kumar V, Ganguly N, Joshi K et al. Protective efficacy and immunogenicity of Escherichia coli K13 diphtheria toxoid conjugate against experimental ascending pyelonephritis. Med. Microbiol. Immunol. 194(4), 211–217 (2005).
  • Kaijser B, Larsson P, Olling S, Schneerson R. Protection against acute, ascending pyelonephritis caused by Escherichia coli in rats, using isolated capsular antigen conjugated to bovine serum albumin. Infect. Immun. 39(1), 142–146 (1983).
  • Kaijser B, Larsson P, Nimmich W, Söderström T. Antibodies to Escherichia coli K and O antigens in protection against acute pyelonephritis. Prog. Allergy 33, 275–288 (1983).
  • Whitfield C, Roberts IS. Structure, assembly and regulation of expression of capsules in Escherichia coli. Mol. Microbiol. 31(5), 1307–1319 (1999).
  • Johnson JR. Virulence factors in Escherichia coli urinary tract infection. Clin. Microbiol. Rev. 4(1), 80–128 (1991).
  • Hoffman S, Sorkin BC, White PC et al. Chemical characterization of a neural cell adhesion molecule purified from embryonic brain membranes. J. Biol. Chem. 257(13), 7720–7729 (1982).
  • Jann K, Jann B. Polysaccharide antigens of Escherichia coli. Rev. Infect. Dis. 9(Suppl. 5), S517–S526 (1987).
  • Vann WF, Schmidt MA, Jann B, Jann K. The structure of the capsular polysaccharide (K5 antigen) of urinary-tract-infective Escherichia coli 010:K5:H4. A polymer similar to desulfo-heparin. Eur. J. Biochem. 116(2), 359–364 (1981).
  • Rappuoli R, Bagnoli F. Vaccine Design: Innovative Approaches and Novel Strategies. Caister Academic, Norfolk, UK (2011).
  • Johnson JR, Kuskowski MA, Gajewski A et al. Extended virulence genotypes and phylogenetic background of Escherichia coli isolates from patients with cystitis, pyelonephritis, or prostatitis. J. Infect. Dis. 191(1), 46–50 (2005).
  • Grischke EM, Rüttgers H. Treatment of bacterial infections of the female urinary tract by immunization of the patients. Urol. Int. 42(5), 338–341 (1987).
  • Knuf M, Habermehl P, Faber J et al. Assessment of nine candidate DTP-vaccines with reduced amount of antigen and/or without adjuvant as a fourth (booster-) dose in the second year of life. Vaccine 24(27–28), 5627–5636 (2006).
  • Mestecky J. The common mucosal immune system and current strategies for induction of immune responses in external secretions. J. Clin. Immunol. 7(4), 265–276 (1987).
  • Uehling DT, Hopkins WJ, Balish E, Xing Y, Heisey DM. Vaginal mucosal immunization for recurrent urinary tract infection: Phase II clinical trial. J. Urol. 157(6), 2049–2052 (1997).
  • Uehling DT, Hopkins WJ, Beierle LM, Kryger JV, Heisey DM. Vaginal mucosal immunization for recurrent urinary tract infection: extended Phase II clinical trial. J. Infect. Dis. 183(Suppl. 1), S81–S83 (2001).
  • Uehling DT, Hopkins WJ, Elkahwaji JE, Schmidt DM, Leverson GE. Phase 2 clinical trial of a vaginal mucosal vaccine for urinary tract infections. J. Urol. 170(3), 867–869 (2003).
  • Hopkins WJ, Elkahwaji J, Beierle LM, Leverson GE, Uehling DT. Vaginal mucosal vaccine for recurrent urinary tract infections in women: results of a Phase 2 clinical trial. J. Urol. 177(4), 1349–1353; quiz 1591 (2007).
  • Frey C, Obolensky W, Wyss H. Treatment of recurrent urinary tract infections: efficacy of an orally administered biological response modifier. Urol. Int. 41(6), 444–446 (1986).
  • Hachen HJ. Oral immunotherapy in paraplegic patients with chronic urinary tract infections: a double-blind, placebo-controlled trial. J. Urol. 143(4), 759–762; discussion 762 (1990).
  • Schulman CC, Corbusier A, Michiels H, Taenzer HJ. Oral immunotherapy of recurrent urinary tract infections: a double-blind placebo-controlled multicenter study. J. Urol. 150(3), 917–921 (1993).
  • Bauer HW, Alloussi S, Egger G, Blümlein HM, Cozma G, Schulman CC; Multicenter UTI Study Group. A long-term, multicenter, double-blind study of an Escherichia coli extract (OM-89) in female patients with recurrent urinary tract infections. Eur. Urol. 47(4), 542–548; discussion 548 (2005).
  • Kim KS, Kim JY, Jeong IG et al. A prospective multi-center trial of Escherichia coli extract for the prophylactic treatment of patients with chronically recurrent cystitis. J. Korean Med. Sci. 25(3), 435–439 (2010).
  • Bauer HW, Rahlfs VW, Lauener PA, Blessmann GS. Prevention of recurrent urinary tract infections with immuno-active E. coli fractions: a meta-analysis of five placebo-controlled double-blind studies. Int. J. Antimicrob. Agents 19(6), 451–456 (2002).
  • Koukalova D, Krocova Z, Vitek P, Macela A, Hajek V. [Immunostimulatory activity of the vaccine used in the treatment of recurrent urinary infections. II]. Bratisl. Lek. Listy 100(4), 215–217 (1999).
  • Koukalová D, Reif R, Hájek V et al. [Immunomodulation of recurrent urinary tract infections with Urvakol vaccine]. Bratisl. Lek. Listy 100(5), 246–251 (1999).
  • Marinova S, Nenkov P, Markova R et al. Cellular and humoral systemic and mucosal immune responses stimulated by an oral polybacterial immunomodulator in patients with chronic urinary tract infections. Int. J. Immunopathol. Pharmacol. 18(3), 457–473 (2005).
  • Russo TA, Beanan JM, Olson R et al. A killed, genetically engineered derivative of a wild-type extraintestinal pathogenic E. coli strain is a vaccine candidate. Vaccine 25(19), 3859–3870 (2007).
  • Billips BK, Yaggie RE, Cashy JP, Schaeffer AJ, Klumpp DJ. A live-attenuated vaccine for the treatment of urinary tract infection by uropathogenic Escherichia coli. J. Infect. Dis. 200(2), 263–272 (2009).
  • Spurbeck RR, Stapleton AE, Johnson JR, Walk ST, Hooton TM, Mobley HL. Fimbrial profiles predict virulence of uropathogenic Escherichia coli strains: contribution of ygi and yad fimbriae. Infect. Immun. 79(12), 4753–4763 (2011).
  • Thankavel K, Madison B, Ikeda T et al. 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. J. Clin. Invest. 100(5), 1123–1136 (1997).
  • Lane MC, Mobley HL. Role of P-fimbrial-mediated adherence in pyelonephritis and persistence of uropathogenic Escherichia coli (UPEC) in the mammalian kidney. Kidney Int. 72(1), 19–25 (2007).
  • O’Hanley P, Lark D, Falkow S, Schoolnik G. Molecular basis of Escherichia coli colonization of the upper urinary tract in BALB/c mice. Gal-Gal pili immunization prevents Escherichia coli pyelonephritis in the BALB/c mouse model of human pyelonephritis. J. Clin. Invest. 75(2), 347–360 (1985).
  • Roberts JA, Hardaway K, Kaack B, Fussell EN, Baskin G. Prevention of pyelonephritis by immunization with P-fimbriae. J. Urol. 131(3), 602–607 (1984).
  • Roberts JA, Kaack MB, Baskin G et al. Antibody responses and protection from pyelonephritis following vaccination with purified Escherichia coli PapDG protein. J. Urol. 171(4), 1682–1685 (2004).
  • Carnoy C, Moseley SL. Mutational analysis of receptor binding mediated by the Dr family of Escherichia coli adhesins. Mol. Microbiol. 23(2), 365–379 (1997).
  • Westerlund B, Kuusela P, Risteli J et al. The O75X adhesin of uropathogenic Escherichia coli is a type IV collagen-binding protein. Mol. Microbiol. 3(3), 329–337 (1989).
  • Goluszko P, Moseley SL, Truong LD et al. 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(7), 1662–1672 (1997).
  • Goluszko P, Goluszko E, Nowicki B, Nowicki S, Popov V, Wang HQ. Vaccination with purified Dr fimbriae reduces mortality associated with chronic urinary tract infection due to Escherichia coli bearing Dr adhesin. Infect. Immun. 73(1), 627–631 (2005).
  • Zhou G, Mo WJ, Sebbel P et al. Uroplakin Ia is the urothelial receptor for uropathogenic Escherichia coli: evidence from in vitro FimH binding. J. Cell. Sci. 114(Pt 22), 4095–4103 (2001).
  • 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. USA 93(18), 9827–9832 (1996).
  • Iwahi T, Abe Y, Nakao M, Imada A, Tsuchiya K. Role of type 1 fimbriae in the pathogenesis of ascending urinary tract infection induced by Escherichia coli in mice. Infect. Immun. 39(3), 1307–1315 (1983).
  • Aronson M, Medalia O, Schori L, Mirelman D, Sharon N, Ofek I. Prevention of colonization of the urinary tract of mice with Escherichia coli by blocking of bacterial adherence with methyl alpha-d-mannopyranoside. J. Infect. Dis. 139(3), 329–332 (1979).
  • Langermann S, Palaszynski S, Barnhart M et al. Prevention of mucosal Escherichia coli infection by FimH-adhesin-based systemic vaccination. Science 276(5312), 607–611 (1997).
  • Langermann S, Möllby R, Burlein JE et al. Vaccination with FimH adhesin protects cynomolgus monkeys from colonization and infection by uropathogenic Escherichia coli. J. Infect. Dis. 181(2), 774–778 (2000).
  • Langermann S, Ballou WR Jr. Vaccination utilizing the FimCH complex as a strategy to prevent Escherichia coli urinary tract infections. J. Infect. Dis. 183(Suppl. 1), S84–S86 (2001).
  • Meiland R, Geerlings SE, Langermann S, Brouwer EC, Coenjaerts FE, Hoepelman AI. Fimch antiserum inhibits the adherence of Escherichia coli to cells collected by voided urine specimens of diabetic women. J. Urol. 171(4), 1589–1593 (2004).
  • Lim JK, Gunther NW 4th, Zhao H, Johnson DE, Keay SK, Mobley HL. In vivo phase variation of Escherichia coli type 1 fimbrial genes in women with urinary tract infection. Infect. Immun. 66(7), 3303–3310 (1998).
  • Eisenstein BI. Phase variation of type 1 fimbriae in Escherichia coli is under transcriptional control. Science 214(4518), 337–339 (1981).
  • Nowicki B, Rhen M, Väisänen-Rhen V, Pere A, Korhonen TK. Immunofluorescence study of fimbrial phase variation in Escherichia coli KS71. J. Bacteriol. 160(2), 691–695 (1984).
  • Tchesnokova V, Aprikian P, Kisiela D et al. type 1 fimbrial adhesin FimH elicits an immune response that enhances cell adhesion of Escherichia coli. Infect. Immun. 79(10), 3895–3904 (2011).
  • Nielubowicz GR, Mobley HL. Host–pathogen interactions in urinary tract infection. Nat. Rev. Urol. 7(8), 430–441 (2010).
  • Rippere-Lampe KE, Lang M, Ceri H, Olson M, Lockman HA, O’Brien AD. Cytotoxic necrotizing factor type 1-positive Escherichia coli causes increased inflammation and tissue damage to the prostate in a rat prostatitis model. Infect. Immun. 69(10), 6515–6519 (2001).
  • 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. 76(7), 2978–2990 (2008).
  • O’Hanley P, Lalonde G, Ji G. Alpha-hemolysin contributes to the pathogenicity of piliated digalactoside-binding Escherichia coli in the kidney: efficacy of an alpha-hemolysin vaccine in preventing renal injury in the BALB/c mouse model of pyelonephritis. Infect. Immun. 59(3), 1153–1161 (1991).
  • 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. 69(10), 6179–6185 (2001).
  • Chu BC, Garcia-Herrero A, Johanson TH et al. Siderophore uptake in bacteria and the battle for iron with the host; a bird’s eye view. Biometals 23(4), 601–611 (2010).
  • Snyder JA, Haugen BJ, Buckles EL et al. Transcriptome of uropathogenic Escherichia coli during urinary tract infection. Infect. Immun. 72(11), 6373–6381 (2004).
  • Faraldo-Gómez JD, Sansom MS. Acquisition of siderophores in gram-negative bacteria. Nat. Rev. Mol. Cell Biol. 4(2), 105–116 (2003).
  • Henderson JP, Crowley JR, Pinkner JS et al. Quantitative metabolomics reveals an epigenetic blueprint for iron acquisition in uropathogenic Escherichia coli. PLoS Pathog. 5(2), e1000305 (2009).
  • Russo TA, McFadden CD, Carlino-MacDonald UB, Beanan JM, Olson R, Wilding GE. The Siderophore receptor IroN of extraintestinal pathogenic Escherichia coli is a potential vaccine candidate. Infect. Immun. 71(12), 7164–7169 (2003).
  • Durant L, Metais A, Soulama-Mouze C, Genevard JM, Nassif X, Escaich S. Identification of candidates for a subunit vaccine against extraintestinal pathogenic Escherichia coli. Infect. Immun. 75(4), 1916–1925 (2007).
  • Carbonetti NH, Boonchai S, Parry SH, Väisänen-Rhen V, Korhonen TK, Williams PH. Aerobactin-mediated iron uptake by Escherichia coli isolates from human extraintestinal infections. Infect. Immun. 51(3), 966–968 (1986).
  • Garcia EC, Brumbaugh AR, Mobley HL. Redundancy and specificity of Escherichia coli iron acquisition systems during urinary tract infection. Infect. Immun. 79(3), 1225–1235 (2011).
  • Watts RE, Totsika M, Challinor VL et al. Contribution of siderophore systems to growth and urinary tract colonization of asymptomatic bacteriuria Escherichia coli. Infect. Immun. 80(1), 333–344 (2012).
  • Wieser A, Romann E, Magistro G et al. A multiepitope subunit vaccine conveys protection against extraintestinal pathogenic Escherichia coli in mice. Infect. Immun. 78(8), 3432–3442 (2010).
  • Wieser A, Magistro G, Nörenberg D, Hoffmann C, Schubert S. First multi-epitope subunit vaccine against extraintestinal pathogenic Escherichia coli delivered by a bacterial type-3 secretion system (T3SS). Int. J. Med. Microbiol. 302(1), 10–18 (2012).
  • Anderson GG, Palermo JJ, Schilling JD, Roth R, Heuser J, Hultgren SJ. Intracellular bacterial biofilm-like pods in urinary tract infections. Science 301(5629), 105–107 (2003).
  • Rice JC, Peng T, Spence JS et al. Pyelonephritic Escherichia coli expressing P fimbriae decrease immune response of the mouse kidney. J. Am. Soc. Nephrol. 16(12), 3583–3591 (2005).
  • Cirl C, Wieser A, Yadav M et al. Subversion of Toll-like receptor signaling by a unique family of bacterial Toll/interleukin-1 receptor domain-containing proteins. Nat. Med. 14(4), 399–406 (2008).
  • He Y, Xiang Z, Mobley HL. Vaxign: the first web-based vaccine design program for reverse vaccinology and applications for vaccine development. J. Biomed. Biotechnol. 2010, 297 (2010).
  • Moriel DG, Bertoldi I, Spagnuolo A et al. Identification of protective and broadly conserved vaccine antigens from the genome of extraintestinal pathogenic Escherichia coli. Proc. Natl Acad. Sci. USA 107(20), 9072–9077 (2010).
  • Foxman B. Recurring urinary tract infection: incidence and risk factors. Am. J. Public Health 80(3), 331–333 (1990).
  • Uehling DT, Hopkins WJ, Dahmer LA, Balish E. Phase I clinical trial of vaginal mucosal immunization for recurrent urinary tract infection. J. Urol. 152(6 Pt 2), 2308–2311 (1994).
  • Uehling DT, Hopkins WJ, James LJ, Balish E. Vaginal immunization of monkeys against urinary tract infection with a multi-strain vaccine. J. Urol. 151(1), 214–216 (1994).
  • Sivick KE, Mobley HL. Waging war against uropathogenic Escherichia coli: winning back the urinary tract. Infect. Immun. 78(2), 568–585 (2010).

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