Combinatorial small-molecule therapy prevents uropathogenic Escherichia coli catheter-associated urinary tract infections in mice

Antimicrobial Agents and Chemotherapy

Volumn 56, Issue 9, 2012, Pages 4738-4745

  Guiton, Pascale S ^a   Cusumano, Corinne K ^a   Kline, Kimberly A ^a,b   Dodson, Karen W ^a   Han, Zhenfu ^a   Janetka, James W ^a   Henderson, Jeffrey P ^a   Caparon, Michael G ^a   Hultgren, Scott J ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; COTRIMOXAZOLE; FIMH PROTEIN; GENTAMICIN; MANNOSIDE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL COLONIZATION; BACTERIURIA; BLADDER CATHETERIZATION; CATHETER ASSOCIATED URINARY TRACT INFECTION; CATHETER INFECTION; CONTROLLED STUDY; DRUG EFFICACY; DRUG MECHANISM; DRUG POTENTIATION; ESCHERICHIA COLI INFECTION; FEMALE; HISTOLOGY; MOUSE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; URINARY CATHETER; URINARY TRACT INFECTION; UROPATHOGENIC ESCHERICHIA COLI;

ADHESINS, ESCHERICHIA COLI; ANIMALS; BACTERIAL ADHESION; BIOFILMS; CATHETER-RELATED INFECTIONS; CROSS INFECTION; DRUG THERAPY, COMBINATION; ESCHERICHIA COLI INFECTIONS; FEMALE; FIMBRIAE PROTEINS; GENE DELETION; MANNOSIDES; MICE; MICE, INBRED C57BL; MOLECULAR WEIGHT; TRIMETHOPRIM-SULFAMETHOXAZOLE COMBINATION; URINARY BLADDER; URINARY CATHETERS; URINARY TRACT INFECTIONS; UROPATHOGENIC ESCHERICHIA COLI;

EID: 84865436489     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.00447-12     Document Type: Article

References (65)

1. Alton G, Kjaergaard S, Etchison JR, Skovby F, Freeze HH. 1997. Oral ingestion of mannose elevates blood mannose levels: a first step toward a potential therapy for carbohydrate-deficient glycoprotein syndrome type I. Biochem. Mol. Med. 60:127-133. (Pubitemid 27198135)
2. Anderson GG, et al. 2003. Intracellular bacterial biofilm-like pods in urinary tract infections. Science 301:105-107. (Pubitemid 36801572)
3. Bi XC, et al. 2009. Pathogen incidence and antibiotic resistance patterns of catheter-associated urinary tract infection in children. J. Chemother. 21:661-665.
4. Cegelski L, et al. 2009. Small-molecule inhibitors target Escherichia coli amyloid biogenesis and biofilm formation. Nat. Chem. Biol. 5:913-919.
5. Chen SL, et al. 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.
6. Christensen BB, et al. 1999. Molecular tools for study of biofilm physiology. Methods Enzymol. 310:20-42.
7. Conway LJ, Larson EL. 2012. Guidelines to prevent catheter-associated urinary tract infection: 1980 to 2010. Heart Lung 41:271-283.
8. Cusumano CK, et al. 2011. Treatment and prevention of urinary tract infection with orally active FimH inhibitors. Sci. Transl. Med. 3:109-115.
9. Delnay KM, Stonehill WH, Goldman H, Jukkola AF, Dmochowski RR. 1999. Bladder histological changes associated with chronic indwelling urinary catheter. J. Urol. 161:1106-1109. (Pubitemid 29426096)
10. Dodson KW, et al. 2001. Structural basis of the interaction of the pyelonephritic Escherichia coli adhesin to its human kidney receptor. Cell 105:733-743. (Pubitemid 32635103)
11. Ejernaes K. 2011. Bacterial characteristics of importance for recurrent urinary tract infections caused by Escherichia coli. Danish Med. Bull. 58:B4187.
12. Elliott TS, Reid L, Rao GG, Rigby RC, Woodhouse K. 1989. Bladder irrigation or irritation? Br. J. Urol. 64:391-394. (Pubitemid 19252928)
13. 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. doi:10.1371/journal.ppat.0030100.
14. Ferrieres L, Hancock V, Klemm P. 2007. Specific selection for virulent urinary tract infectious Escherichia coli strains during catheter-associated biofilm formation. FEMS Immunol. Med. Microbiol. 51:212-219. (Pubitemid 47387496)
15. Firon N, Ashkenazi S, Mirelman D, Ofek I, Sharon N. 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. (Pubitemid 17004131)
16. Garibaldi RA, Burke JP, Britt MR, Miller MA, Smith CB. 1980. Meatal colonization and catheter-associated bacteriuria. N. Engl. J. Med. 303:316-318. (Pubitemid 10040020)
17. Goble NM, Clarke T, Hammonds JC. 1989. Histological changes in the urinary bladder secondary to urethral catheterisation. Br. J. Urol. 63:354-357. (Pubitemid 19109927)
18. Guiton PS, Hung CS, Hancock LE, Caparon MG, Hultgren SJ. 2010. Enterococcal biofilm formation and virulence in an optimized murine model of foreign body-associated urinary tract infections. Infect. Immun. 78:4166-4175.
19. Han Z, et al. 2012. Lead optimization studies on FimH antagonists: discovery of potent and orally bioavailable ortho-substituted biphenyl mannosides. J. Med. Chem. 55:3945-3959.
20. Han Z, et al. 2010. Structure-based drug design and optimization of mannoside bacterial FimH antagonists. J. Med. Chem. 53:4779-4792.
21. Hannan TJ, Mysorekar IU, Hung CS, Isaacson-Schmid ML, Hultgren SJ. 2010. Early severe inflammatory responses to uropathogenic Escherichia coli predispose to chronic and recurrent urinary tract infection. PLoS Pathog. 6:e1001042. doi:10.1371/journal.ppat.1001042.
22. Hidron AI, et al. 2008. NHSN annual update: antimicrobial-resistant pathogens associated with healthcare-associated infections: annual summary of data reported to the national health care safety network at the Centers for Disease Control and Prevention, 2006-2007. Infect. Control Hosp. Epidemiol. 29:996-1011.
23. Hung CS, et al. 2002. Structural basis of tropism of Escherichia coli to the bladder during urinary tract infection. Mol. Microbiol. 44:903-915.
24. Jacobsen SM, Stickler DJ, Mobley HL, Shirtliff ME. 2008. Complicated catheter-associated urinary tract infections due to Escherichia coli and Proteus mirabilis. Clin. Microbiol. Rev. 21:26-59. (Pubitemid 351160009)
25. Justice SS, et al. 2004. Differentiation and developmental pathways of uropathogenic Escherichia coli in urinary tract pathogenesis. Proc. Natl. Acad. Sci. U. S. A. 101:1333-1338. (Pubitemid 38182689)
26. Justice SS, Lauer SR, Hultgren SJ, Hunstad DA. 2006. Maturation of intracellular Escherichia coli communities requires SurA. Infect. Immun. 74:4793-4800. (Pubitemid 44157266)
27. Kucheria R, Dasgupta P, Sacks SH, Khan MS, Sheerin NS. 2005. Urinary tract infections: new insights into a common problem. Postgrad. Med. J. 81:83-86. (Pubitemid 40282870)
28. Kurosaka Y, et al. 2001. A non-surgical rat model of foreign body-associated urinary tract infection with Pseudomonas aeruginosa. Microbiol. Immunol. 45:9-15. (Pubitemid 32143746)
29. Magoha GA. 1997. Nosocomial infection of the urinary tract: pattern of antibiotic use and drug resistance. East African Med. J. 74:190-192.
30. Martinez JJ, Hultgren SJ. 2002. Requirement of Rho-family GTPases in the invasion of type 1-piliated uropathogenic Escherichia coli. Cell. Microbiol. 4:19-28. (Pubitemid 34121275)
31. 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. (Pubitemid 30386753)
32. Martinez-Medina M, et al. 2009. Biofilm formation as a novel phenotypic feature of adherent-invasive Escherichia coli (AIEC). BMC Microbiol. 9:202. doi:10.1186/1471-2180-9-202.
33. McTaggart LA, Rigby RC, Elliott TS. 1990. The pathogenesis of urinary tract infections associated with Escherichia coli, Staphylococcus saprophyticus, and S. epidermidis. J. Med. Microbiol. 32:135-141. (Pubitemid 20178820)
34. Mobley HL, Chippendale GR, Tenney JH, Hull RA, Warren JW. 1987. Expression of type 1 fimbriae may be required for persistence of Escherichia coli in the catheterized urinary tract. J. Clin. Microbiol. 25:2253-2257.
35. Mulvey MA, et al. 1998. Induction and evasion of host defenses by type 1-piliated uropathogenic Escherichia coli. Science 282:1494-1497. (Pubitemid 28538612)
36. 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. (Pubitemid 32574459)
37. 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. (Pubitemid 44452998)
38. Mysorekar IU, Mulvey MA, Hultgren SJ, Gordon JI. 2002. Molecular regulation of urothelial renewal and host defenses during infection with uropathogenic Escherichia coli. J. Biol. Chem. 277:7412-7419. (Pubitemid 34953138)
39. Naves P, et al. 2008. Correlation between virulence factors and in vitro biofilm formation by Escherichia coli strains. Microb. Pathog. 45:86-91.
40. Nazarko L. 2011. Should antibiotics be prescribed when urinary catheters are removed? Br. J. Community Nursing 16:374-380.
41. Nicholson TF, Watts KM, Hunstad DA. 2009. OmpA of uropathogenic Escherichia coli promotes postinvasion pathogenesis of cystitis. Infect. Immun. 77:5245-5251.
42. Nielubowicz GR, Mobley HL. 2010. Host-pathogen interactions in urinary tract infection. Nat. Rev. Urol. 7:430-441.
43. Parsons CL. 1986. Pathogenesis of urinary tract infections: bacterial adherence, bladder defense mechanisms. Urol. C. N. Am. 13:563-568. (Pubitemid 17182515)
44. Peychl L, Zalud R. 2008. Changes in the urinary bladder caused by short-term permanent catheter insertion. Casopis Lekaru Ceskych. 147:325-329. (In Czech.)
45. Pinkner JS, et al. 2006. Rationally designed small compounds inhibit pilus biogenesis in uropathogenic bacteria. Proc. Natl. Acad. Sci. U. S. A. 103:17897-17902. (Pubitemid 44852257)
46. Ronald LS, et al. 2008. Adaptive mutations in the signal peptide of the type 1 fimbrial adhesin of uropathogenic Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 105:10937-10942.
47. 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.
48. Rosen DA, 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.
49. Saint S, Chenoweth CE. 2003. Biofilms and catheter-associated urinary tract infections. Infect. Dis. Clin. N. Am. 17:411-432. (Pubitemid 36760190)
50. Sauer FG, et al. 1999. Structural basis of chaperone function and pilus biogenesis. Science 285:1058-1061.
51. Schaeffer AJ, Schwan WR, Hultgren SJ, Duncan JL. 1987. Relationship of type 1 pilus expression in Escherichia coli to ascending urinary tract infections in mice. Infect. Immun. 55:373-380. (Pubitemid 17004115)
52. Schilling JD, Lorenz RG, Hultgren SJ. 2002. Effect of trimethoprimsulfamethoxazole on recurrent bacteriuria and bacterial persistence in mice infected with uropathogenic Escherichia coli. Infect. Immun. 70:7042-7049. (Pubitemid 35387940)
53. Siddiq DM, Darouiche RO. 2012. New strategies to prevent catheter-associated urinary tract infections. Nat. Rev. Urol. 9:305-314.
54. Song J, et al. 2009. TLR4-mediated expulsion of bacteria from infected bladder epithelial cells. Proc. Natl. Acad. Sci. U. S. A. 106:14966-14971.
55. Sun TT, Zhao H, Provet J, Aebi U, Wu XR. 1996. Formation of asymmetric unit membrane during urothelial differentiation. Mol. Biol. Rep. 23:3-11. (Pubitemid 27015464)
56. Trautner BW. 2010. Management of catheter-associated urinary tract infection. Curr. Opin. Infect. Dis. 23:76-82.
57. Trautner BW, Darouiche RO. 2004. Role of biofilm in catheter-associated urinary tract infection. Am. J. Infect. Control 32:177-183. (Pubitemid 38620840)
58. Waksman G, Hultgren SJ. 2009. Structural biology of the chaperone-usher pathway of pilus biogenesis. Nat. Rev. Microbiol. 7:765-774.
59. Warren JW. 2001. Catheter-associated urinary tract infections. Int. J. Antimicrob. Agents 17:299-303. (Pubitemid 32288748)
60. Weissman SJ, et al. 2007. Differential stability and trade-off effects of pathoadaptive mutations in the Escherichia coli FimH adhesin. Infect. Immun. 75:3548-3555. (Pubitemid 47040957)
61. Wellens A, et al. 2008. Intervening with urinary tract infections using anti-adhesives based on the crystal structure of the FimH-oligomannose-3 complex. PLoS One 3:e2040. doi:10.1371/journal.pone.0002040.
62. 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. (Pubitemid 47250294)
63. Wright KJ, Seed PC, Hultgren SJ. 2005. Uropathogenic Escherichia coli flagella aid in efficient urinary tract colonization. Infect. Immun. 73:7657-7668. (Pubitemid 41587672)
64. Yu J, Lin JH, Wu XR, Sun TT. 1994. Uroplakins Ia and Ib, two major differentiation products of bladder epithelium, belong to a family of four transmembrane domain (4TM) proteins. J. Cell Biol. 125:171-182. (Pubitemid 24100047)
65. Zhou G, et al. 2001. Uroplakin Ia is the urothelial receptor for uropathogenic Escherichia coli: evidence from in vitro FimH binding. J. Cell Sci. 114:4095-4103. (Pubitemid 33115030)