A FimH inhibitor prevents acute bladder infection and treats chronic cystitis caused by multidrug-resistant uropathogenic escherichia coli ST131

Journal of Infectious Diseases

Volumn 208, Issue 6, 2013, Pages 921-928

  Totsika, Makrina ^a,b   Kostakioti, Maria ^c   Hannan, Thomas J ^c   Upton, Mathew ^e   Beatson, Scott A ^a,b   Janetka, James W ^c   Hultgren, Scott J ^c,d   Schembri, Mark A ^a,b  

^a The University of Queensland and QIMR Berghofer Medical Research Institute   (Australia)

^b UNIVERSITY OF QUEENSLAND   (Australia)

^c Department of Molecular Microbiology ^*  (Australia)

^d WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

antibiotic resistance; biofilm; E. coli ST131; mannoside; type 1 fimbriae; urinary tract infection; uropathogenic E. coli

Indexed keywords

4' (A DEXTRO MANNOPYRANOSYLOXY) N,3' DIMETHYLBIPHENYL 3 CARBOXAMIDE; PROTEIN INHIBITOR; UNCLASSIFIED DRUG; ZFH 04269;

ACUTE BLADDER INFECTION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL LOAD; BACTERIAL STRAIN; BACTERIUM ISOLATE; BLADDER DISEASE; BLADDER EPITHELIUM; CHRONIC DISEASE; CYSTITIS; DRUG EFFECT; DRUG TREATMENT FAILURE; EPITHELIUM CELL; FEMALE; MICROBIAL COMMUNITY; MOUSE; MULTIDRUG RESISTANCE; NONHUMAN; PRIORITY JOURNAL; UROPATHOGENIC ESCHERICHIA COLI;

ANTIBIOTIC RESISTANCE; BIOFILM; E. COLI ST131; MANNOSIDE; TYPE 1 FIMBRIAE; URINARY TRACT INFECTION; UROPATHOGENIC E. COLI;

ACUTE DISEASE; ADHESINS, ESCHERICHIA COLI; ADMINISTRATION, ORAL; ANIMALS; ANTI-BACTERIAL AGENTS; CHRONIC DISEASE; CYSTITIS; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG RESISTANCE, MULTIPLE, BACTERIAL; FEMALE; FIMBRIAE PROTEINS; FIMBRIAE, BACTERIAL; HUMANS; MICE; MICE, INBRED C3H; URINARY BLADDER; UROPATHOGENIC ESCHERICHIA COLI;

EID: 84883237676     PISSN: 00221899     EISSN: None     Source Type: Journal    
DOI: 10.1093/infdis/jit245     Document Type: Article

References (42)

1. Harding GKM, Ronald AR. The management of urinary infections; what have we learned in the past decade? Int J Antimicrob Agents 1994; 4:83-8.
2. Foxman B. Epidemiology of urinary tract infections: incidence, morbidity, and economic costs. Am J Med 2002; 113:5-13.
3. Foxman B. The epidemiology of urinary tract infection. Nat Rev Urol 2010; 7:653-60.
4. Ferry SA, Holm SE, Stenlund H, Lundholm R, Monsen TJ. The natural course of uncomplicated lower urinary tract infection in women illustrated by a randomized placebo controlled study. Scand J Infect Dis 2004; 36:296-301.
5. Mabeck CE. Treatment of uncomplicated urinary tract infection in non-pregnant women. Postgrad Med J 1972; 48:69-75.
6. Hannan TJ, Totsika M, Mansfield KJ, Moore KH, Schembri MA, Hultgren SJ. Host-pathogen checkpoints and population bottlenecks in persistent and intracellular uropathogenic Escherichia coli bladder infection. FEMS Microbiol Rev 2012; 36:616-48.
7. Totsika M, Moriel DG, Idris A, et al. Uropathogenic Escherichia coli mediated urinary tract infection. Curr Drug Targets 2012; 13:1386-99.
8. Wu XR, Sun TT, Medina JJ. In vitro binding of type 1-fimbriated Escherichia coli to uroplakins Ia and Ib: relation to urinary tract infections. Proc Natl Acad Sci USA 1996; 93:9630-5.
9. Martinez JJ, Mulvey MA, Schilling JD, Pinkner JS, Hultgren SJ. Type 1 pilus-mediated bacterial invasion of bladder epithelial cells. Embo J 2000; 19:2803-12.
10. Anderson GG, Palermo JJ, Schilling JD, Roth R, Heuser J, Hultgren SJ. Intracellular bacterial biofilm-like pods in urinary tract infections. Science 2003; 301:105-7.
11. Wright KJ, Seed PC, Hultgren SJ. Development of intracellular bacterial communities of uropathogenic Escherichia coli depends on type 1 pili. Cell Microbiol 2007; 9:2230-41.
12. Justice SS, Hung C, Theriot JA, et al. Differentiation and developmental pathways of uropathogenic Escherichia coli in urinary tract pathogenesis. Proc Natl Acad Sci USA 2004; 101:1333-8.
13. Mulvey MA, Lopez-Boado YS, Wilson CL, et al. Induction and evasion of host defenses by type 1-piliated uropathogenic Escherichia coli. Science 1998; 282:1494-7.
14. Blango MG, Mulvey MA. Persistence of uropathogenic Escherichia coli in the face of multiple antibiotics. Antimicrob Agents Chemother 2010; 54:1855-63.
15. Hunstad DA, Justice SS. Intracellular lifestyles and immune evasion strategies of uropathogenic Escherichia coli. Annu Rev Microbiol 2010; 64:203-21.
16. Mysorekar IU, Hultgren SJ. Mechanisms of uropathogenic Escherichia coli persistence and eradication from the urinary tract. Proc Natl Acad Sci USA 2006; 103:14170-5.
17. Rosen DA, Hooton TM, Stamm WE, Humphrey PA, Hultgren SJ. Detection of intracellular bacterial communities in human urinary tract infection. PLoS Med 2007; 4:e329.
18. Hannan TJ, Mysorekar IU, Hung CS, Isaacson-Schmid ML, Hultgren SJ. Early severe inflammatory responses to uropathogenic E. coli predispose to chronic and recurrent urinary tract infection. PLoS Pathog 2010; 6:e1001042.
19. Chen SL, Hung CS, Pinkner JS, et al. Positive selection identifies an in vivo role for FimH during urinary tract infection in addition to mannose binding. Proc Natl Acad Sci USA 2009; 106:22439-44.
20. Han Z, Pinkner JS, Ford B, et al. Structure-based drug design and optimization of mannoside bacterial FimH antagonists. J Med Chem 2010; 53:4779-92.
21. Cusumano CK, Pinkner JS, Han Z, et al. Treatment and prevention of urinary tract infection with orally active FimH inhibitors. Sci Transl Med 2011; 3:109ra15.
22. Rogers BA, Sidjabat HE, Paterson DL. Escherichia coli O25b-ST131: a pandemic, multiresistant, community-associated strain. J Antimicrob Chemother 2011; 66:1-14.
23. Canton R, Coque TM. The CTX-M beta-lactamase pandemic. Curr Opin Microbiol 2006; 9:466-75.
24. Johnson JR, Johnston B, Clabots C, Kuskowski MA, Castanheira M. Escherichia coli sequence type ST131 as the major cause of serious multidrug-resistant E. coli infections in the United States. Clin Infect Dis 2010; 51:286-94.
25. Nicolas-Chanoine MH, Blanco J, Leflon-Guibout V, et al. Intercontinental emergence of Escherichia coli clone O25:H4-ST131 producing CTX-M-15. J Antimicrob Chemother 2008; 61:273-81.
26. Pitout JD, Gregson DB, Campbell L, Laupland KB. Molecular characteristics of extended-spectrum-beta-lactamase-producing Escherichia coli isolates causing bacteremia in the Calgary Health Region from 2000 to 2007: emergence of clone ST131 as a cause of communityacquired infections. Antimicrob Agents Chemother 2009; 53:2846-51.
27. Johnson JR, Menard M, Johnston B, Kuskowski MA, Nichol K, Zhanel GG. Epidemic clonal groups of Escherichia coli as a cause of antimicrobial-resistant urinary tract infections in Canada, 2002 to 2004. Antimicrob Agents Chemother 2009; 53:2733-9.
28. Totsika M, Beatson SA, Sarkar S, et al. Insights into a multidrug resistant Escherichia coli pathogen of the globally disseminated ST131 lineage: genome analysis and virulence mechanisms. PLoS One 2011; 6:e26578.
29. Ender PT, Gajanana D, Johnston B, Clabots C, Tamarkin FJ, Johnson JR. Transmission of an extended-spectrum-beta-lactamase-producing Escherichia coli (sequence type ST131) strain between a father and daughter resulting in septic shock and emphysematous pyelonephritis. J Clin Microbiol 2009; 47:3780-2.
30. Johnson JR, Anderson JT, Clabots C, Johnston B, Cooperstock M. Within-household sharing of a fluoroquinolone-resistant Escherichia coli sequence type st131 strain causing pediatric osteoarticular infection. Pediatr Infect Dis J 2009; 29:473-5.
31. Lau SH, Kaufmann ME, Livermore DM, et al. UK epidemic Escherichia coli strains A-E, with CTX-M-15 {beta}-lactamase, all belong to the international O25:H4-ST131 clone. J Antimicrob Chemother 2008; 62:1241-4.
32. Schembri MA, Sokurenko EV, Klemm P. Functional flexibility of the FimH adhesin: insights from a random mutant library 10.1128/IAI.68.5.2638-2646.2000. Infect Immun 2000; 68:2638-46.
33. Hung CS, Dodson KW, Hultgren SJ. A murine model of urinary tract infection. Nat Protoc 2009; 4:1230-43.
34. Kostakioti M, Hadjifrangiskou M, Pinkner JS, Hultgren SJ. QseCmediated dephosphorylation of QseB is required for expression of genes associated with virulence in uropathogenic Escherichia coli. Mol Microbiol 2009; 73:1020-31.
35. Murawski IJ, Maina RW, Malo D, et al. The C3H/HeJ inbred mouse is a model of vesico-ureteric reflux with a susceptibility locus on chromosome 12. Kidney Int 2010; 78:269-78.
36. Lane MC, Alteri CJ, Smith SN, Mobley HLT. Expression of flagella is coincident with uropathogenic Escherichia coli ascension to the upper urinary tract. Proc Natl Acad Sci 2007; 104:16669-74.
37. Gupta K, Hooton TM, Naber KG, et al. 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 2011; 52:e103-20.
38. Livermore DM. Fourteen years in resistance. Int J Antimicrob Agents 2012; 39:283-94.
39. Talbot GH, Bradley J, Edwards JE, Gilbert D, Scheld M, Bartlett JG. Bad bugs need drugs: an update on the development pipeline from the Antimicrobial Availability Task Force of the Infectious Diseases Society of America. Clin Infect Dis 2006; 42:657-68.
40. Woodford N, Turton JF, Livermore DM. Multiresistant Gram-negative bacteria: the role of high-risk clones in the dissemination of antibiotic resistance. FEMS Microbiol Rev 2011; 35:736-55.
41. Norinder BS, Koves B, Yadav M, Brauner A, Svanborg C. Do Escherichia coli strains causing acute cystitis have a distinct virulence repertoire? Microb Pathog 2012; 52:10-6.
42. Rasko DA, Sperandio V. Anti-virulence strategies to combat bacteriamediated disease. Nat Rev Drug Discov 2010; 9:117-28.