Human urine decreases function and expression of type 1 pili in uropathogenic Escherichia coli

mBio

Volumn 6, Issue 4, 2015, Pages

  Greene, Sarah E ^a   Hibbing, Michael E ^a   Janetk, James ^a   Chen, Swaine L ^a,b   Hultgren, Scott J ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Dept Medicine Endocrinol Diabet   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; FIMH PROTEIN; MANNOSIDE; UNCLASSIFIED DRUG; ADHESIN; FIMBRIA PROTEIN; FIMH PROTEIN, E COLI;

ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIUM ADHERENCE; BACTERIUM PILUS; BLADDER EPITHELIUM; CONTROLLED STUDY; DRUG TARGETING; EPIGENETICS; EPITHELIUM CELL; FIM GENE; GENE EXPRESSION; GENE FUNCTION; GENETIC REGULATION; HUMAN; HUMAN CELL; NONHUMAN; OPERON; PRIORITY JOURNAL; PROTEIN FUNCTION; URINARY TRACT INFECTION; URINE; UROPATHOGENIC ESCHERICHIA COLI; ANTAGONISTS AND INHIBITORS; CELL LINE; DRUG EFFECTS; FIMBRIA; GENE EXPRESSION REGULATION; MICROBIOLOGY; PHYSIOLOGY;

ADHESINS, BACTERIAL; ADHESINS, ESCHERICHIA COLI; CELL LINE; EPITHELIAL CELLS; FIMBRIAE PROTEINS; FIMBRIAE, BACTERIAL; GENE EXPRESSION REGULATION, BACTERIAL; HUMANS; URINE; UROPATHOGENIC ESCHERICHIA COLI;

EID: 84940854187     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.00820-15     Document Type: Article

References (39)

1. Hooton TM, Stamm WE. 1997. Diagnosis and treatment of uncomplicated urinary tract infection. Infect Dis Clin NorthAm 11:551–581. http://dx.doi.org/10.1016/S0891-5520(05)70373-1
2. Eto DS, Jones TA, Sundsbak JL, Mulvey MA. 2007. Integrin-mediated host cell invasion by type 1-piliated uropathogenic Escherichia coli. PLoS Pathog 3:e100. http://dx.doi.org/10.1371/journal.ppat.0030100
3. Martinez JJ, Mulvey MA, Schilling JD, Pinkner JS, Hultgren SJ. 2000. Type 1 pilus-mediated bacterial invasion of bladder epithelial cells. EMBO J 19:2803–2812. http://dx.doi.org/10.1093/emboj/19.12.2803
4. Mulvey MA, Lopez-Boado YS, Wilson CL, Roth R, Parks WC, Heuser J, Hultgren SJ. 1998. Induction and evasion of host defenses by type 1-piliated uropathogenic Escherichia coli. Science 282:1494–1497. http://dx.doi.org/10.1126/science.282.5393.1494
5. Song J, Bishop BL, Li G, Grady R, Stapleton A, Abraham SN. 2009. TLR4-mediated expulsion of bacteria from infected bladder epithelial cells. Proc Natl Acad Sci U S A 106:14966–14971. http://dx.doi.org/10.1073/pnas.0900527106
6. Anderson GG, Dodson KW, Hooton TM, Hultgren SJ. 2004. Intracellular bacterial communities of uropathogenic Escherichia coli in urinary tract pathogenesis. Trends Microbiol 12:424–430. http://dx.doi.org/10.1016/j.tim.2004.07.005
7. Wright KJ, Seed PC, Hultgren SJ. 2007. Development of intracellular bacterial communities of uropathogenic Escherichia coli depends on type 1 pili. Cell Microbiol 9:2230–2241. http://dx.doi.org/10.1111/j.1462-5822.2007.00952.x
8. 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. http://dx.doi.org/10.1371/journal.pmed.0040329
9. Robino L, Scavone P, Araujo L, Algorta G, Zunino P, Pírez MC, Vignoli R. 2014. Intracellular bacteria in the pathogenesis of Escherichia coli urinary tract infection in children. Clin Infect Dis 59:e158–e164. http://dx.doi.org/10.1093/cid/ciu634
10. Connell I, Agace W, Klemm P, Schembri M, Mărild S, Svanborg C. 1996. Type 1 fimbrial expression enhances Escherichia coli virulence for the urinary tract. Proc Natl Acad Sci U S A 93:9827–9832. http://dx.doi.org/10.1073/pnas.93.18.9827
11. Bahrani-Mougeot FK, Buckles EL, Lockatell CV, Hebel JR, Johnson DE, Tang CM, Donnenberg MS. 2002. Type 1 fimbriae and extracellular polysaccharides are preeminent uropathogenic Escherichia coli virulence determinants in the murine urinary tract. Mol Microbiol 45:1079–1093. http://dx.doi.org/10.1046/j.1365-2958.2002.03078.x
12. Abraham JM, Freitag CS, Clements JR, Eisenstein BI. 1985. An invertible element of DNA controls phase variation of type 1 fimbriae of Escherichia coli. Proc Natl Acad Sci U S A 82:5724–5727. http://dx.doi.org/10.1073/pnas.82.17.5724
13. Klemm P. 1986. Two regulatory fim genes, fimB and fimE, control the phase variation of type 1 fimbriae in Escherichia coli. EMBO J 5:1389–1393
14. Schwan WR. 2011. Regulation of genes in uropathogenic. World J Clin Infect Dis 1:17–25
15. Sauer FG, Fütterer K, Pinkner JS, Dodson KW, Hultgren SJ, Waksman G. 1999. Structural basis of chaperone function and pilus biogenesis. Science 285:1058–1061. http://dx.doi.org/10.1126/science.285.5430.1058
16. Remaut H, Rose RJ, Hannan TJ, Hultgren SJ, Radford SE, Ashcroft AE, Waksman G. 2006. Donor-strand exchange in chaperone-assisted pilus assembly proceeds through a concerted beta strand displacement mechanism. Mol Cell 22:831–842. http://dx.doi.org/10.1016/j.molcel.2006.05.033
17. Remaut H, Tang C, Henderson NS, Pinkner JS, Wang T, Hultgren SJ, Thanassi DG, Waksman G, Li H. 2008. Fiber formation across the bacterial outer membrane by the chaperone/usher pathway. Cell 133: 640–652. http://dx.doi.org/10.1016/j.cell.2008.03.033
18. Rose RJ, Welsh TS, Waksman G, Ashcroft AE, Radford SE, Paci E. 2008. Donor-strand exchange in chaperone-assisted pilus assembly revealed in atomic detail by molecular dynamics. J Mol Biol 375:908–919. http://dx.doi.org/10.1016/j.jmb.2007.10.077
19. Greene SE, Pinkner JS, Chorell E, Dodson KW, Shaffer CL, Conover MS, Livny J, Hadjifrangiskou M, Almqvist F, Hultgren SJ. 2014. Pilicide ec240 disrupts virulence circuits in uropathogenic Escherichia coli. mBio 5:e02038-14. http://dx.doi.org/10.1128/mBio.02038-14
20. Bouatra S, Aziat F, Mandal R, Guo AC, Wilson MR, Knox C, Bjorndahl TC, Krishnamurthy R, Saleem F, Liu P, Dame ZT, Poelzer J, Huynh J, Yallou FS, Psychogios N, Dong E, Bogumil R, Roehring C, Wishart DS. 2013. The human urine metabolome. PLoS One 8:e73076. http://dx.doi.org/10.1371/journal.pone.0073076
21. Kisielius PV, Schwan WR, Amundsen SK, Duncan JL, Schaeffer AJ. 1989. In vivo expression and variation of Escherichia coli type 1 and P pili in the urine of adults with acute urinary tract infections. Infect Immun 57:1656–1662
22. Bielecki P, Muthukumarasamy U, Eckweiler D, Bielecka A, Pohl S, Schanz A, Niemeyer U, Oumeraci T, von Neuhoff N, Ghigo JM, Häussler S. 2014. In vivo mRNA profiling of uropathogenic Escherichia coli from diverse phylogroups reveals common and group-specific gene expression profiles. mBio 5:e01075-14. http://dx.doi.org/10.1128/mBio.01075-14
23. Hagan EC, Lloyd AL, Rasko DA, Faerber GJ, Mobley HL. 2010. Escherichia coli global gene expression in urine from women with urinary tract infection. PLoS Pathog 6:e1001187. http://dx.doi.org/10.1371/journal.ppat.1001187
24. Subashchandrabose S, Hazen TH, Brumbaugh AR, Himpsl SD, Smith SN, Ernst RD, Rasko DA, Mobley HL. 2014. Host-specific induction of Escherichia coli fitness genes during human urinary tract infection. Proc Natl Acad Sci U S A 111:18327–18332. http://dx.doi.org/10.1073/pnas.1415959112
25. Gunther NW, Lockatell V, Johnson DE, Mobley HL. 2001. In vivo dynamics of type 1 fimbria regulation in uropathogenic Escherichia coli during experimental urinary tract infection. Infect Immun 69:2838–2846. http://dx.doi.org/10.1128/IAI.69.5.2838-2846.2001
26. Hultgren SJ, Porter TN, Schaeffer AJ, Duncan JL. 1985. Role of type 1 pili and effects of phase variation on lower urinary tract infections produced by Escherichia coli. Infect Immun 50:370–377
27. Mulvey MA, Schilling JD, Hultgren SJ. 2001. Establishment of a persistent Escherichia coli reservoir during the acute phase of a bladder infection. Infect Immun 69:4572–4579. http://dx.doi.org/10.1128/IAI.69.7.4572-4579.2001
28. Parkkinen J, Virkola R, Korhonen TK. 1988. Identification of factors in human urine that inhibit the binding of Escherichia coli adhesins. Infect Immun 56:2623–2630
29. Chen SL, Hung CS, Pinkner JS, Walker JN, Cusumano CK, Li Z, Bouckaert J, Gordon JI, Hultgren SJ. 2009. Positive selection identifies an in vivo role for FimH during urinary tract infection in addition to mannose binding. Proc Natl Acad Sci U S A 106:22439–22444. http://dx.doi.org/10.1073/pnas.0902179106
30. Volkan E, Ford BA, Pinkner JS, Dodson KW, Henderson NS, Thanassi DG, Waksman G, Hultgren SJ. 2012. Domain activities of PapC usher reveal the mechanism of action of an Escherichia coli molecular machine. Proc Natl Acad Sci U S A 109:9563–9568. http://dx.doi.org/10.1073/pnas.1207085109
31. Saulino ET, Thanassi DG, Pinkner JS, Hultgren SJ. 1998. Ramifications of kinetic partitioning on usher-mediated pilus biogenesis. EMBO J 17: 2177–2185. http://dx.doi.org/10.1093/emboj/17.8.2177
32. Cusumano CK, Pinkner JS, Han Z, Greene SE, Ford BA, Crowley JR, Henderson JP, Janetka JW, Hultgren SJ. 2011. Treatment and prevention of urinary tract infection with orally active FimH inhibitors. Sci Transl Med 3:109ra115. http://dx.doi.org/10.1126/scitranslmed.3003021
33. Han Z, Pinkner JS, Ford B, Chorell E, Crowley JM, Cusumano CK, Campbell S, Henderson JP, Hultgren SJ, Janetka JW. 2012. Lead optimization studies on FimH antagonists: discovery of potent and orally bioavailable ortho-substituted biphenyl mannosides. J Med Chem 55: 3945–3959. http://dx.doi.org/10.1021/jm300165m
34. Hannan TJ, Mysorekar IU, Chen SL, Walker JN, Jones JM, Pinkner JS, Hultgren SJ, Seed PC. 2008. LeuX tRNA-dependent and -independent mechanisms of Escherichia coli pathogenesis in acute cystitis. Mol Microbiol 67:116–128. http://dx.doi.org/10.1111/j.1365-2958.2007.06025.x
35. Hultgren SJ, Schwan WR, Schaeffer AJ, Duncan JL. 1986. Regulation of production of type 1 pili among urinary tract isolates of Escherichia coli. Infect Immun 54:613–620
36. Chen SL, Hung CS, Xu J, Reigstad CS, Magrini V, Sabo A, Blasiar D, Bieri T, Meyer RR, Ozersky P, Armstrong JR, Fulton RS, Latreille JP, Spieth J, Hooton TM, Mardis ER, Hultgren SJ, Gordon JI. 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. http://dx.doi.org/10.1073/pnas.0600938103
37. Metcalf WW, Steed PM, Wanner BL. 1990. Identification of phosphate starvation-inducible genes in Escherichia coli K-12 by DNA sequence analysis of psi::lacZ(Mu d1) transcriptional fusions. J Bacteriol 172: 3191–3200
38. Mobley HL, Green DM, Trifillis AL, Johnson DE, Chippendale GR, Lockatell CV, Jones BD, Warren JW. 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
39. Kostakioti M, Hadjifrangiskou M, Cusumano CK, Hannan TJ, Janetka JW, Hultgren SJ. 2012. Distinguishing the contribution of type 1 pili from that of other QseB-misregulated factors when QseC is absent during urinary tract infection. Infect Immun 80:2826–2834. http://dx.doi.org/10.1128/IAI.00283-12.