References
- Papers of special note have been highlighted as either of interest (•) or of considerable interest (••) to readers.
- Fronzes R, Remaut H, Waksman G. Architectures and biogenesis of non-flagellar protein appendages in Gram-negative bacteria. Embo J. 2008;27:2271–2280.
- Waksman G, Hultgren SJ. Structural biology of the chaperone-usher pathway of pilus biogenesis. Nat Rev Microbiol. 2009;7:765–774.
- Mulvey MA, Lopez-Boado YS, Wilson CL, et al. Induction and evasion of host defenses by type 1-piliated uropathogenic Escherichia coli. Science. 1998;282:1494–1497.
- Martinez JJ, Mulvey MA, Schilling JD, et al. Type 1 pilus-mediated bacterial invasion of bladder epithelial cells. Embo J. 2000;19:2803–2812.
- Knight SD, Bouckaert J. Structure, function, and assembly of type 1 fimbriae. Top Curr Chem. 2009;288:67–107.
- Nuccio S, Bäumler AJ. Evolution of the chaperone/usher assembly pathway: fimbrial classification goes Greek. Microbiol Mol Biol Rev. 2007;71:551–575.
- Wurpel DJ, Beatson SA, Totsika M, et al. Chaperone-usher fimbriae of Escherichia coli. PLoS One. 2013;8:e52835.
- Norinder BS, Köves B, Yadav M, et al. Do Escherichia coli strains causing acute cystitis have a distinct virulence repertoire? Microb Pathog. 2012;52:10–16.
- Foxman B, Zhang L, Palin K, et al. Bacterial virulence characteristics of Escherichia coli isolates from first-time urinary tract infection. J Infect Dis. 1995;171:1514–1521.
- Choudhury D, Thompson A, Stojanoff V, et al. X-ray structure of the FimC-FimH chaperone-adhesin complex from uropathogenic Escherichia coli. Science. 1999;285:1061–1066.
- Hung CS, Dodson KW, Hultgren SJ. A murine model of urinary tract infection. Nat Protoc. 2009;4:1230–1243.
- Hannan TJ, Mysorekar IU, Hung CS, et al. Early severe inflammatory responses to uropathogenic E. coli predispose to chronic and recurrent urinary tract infection. PLoS Pathog. 2010;6:e1001042.
- Guiton PS, Hung CS, Hancock L, et al. Enterococcal biofilm formation and virulence in an optimized murine model of foreign body-associated urinary tract infections. Infect Immun. 2010;78:4166–4175.
- Guiton PS, Cusumano CK, Kline KA, et al. Combinatorial small-molecule therapy prevents uropathogenic Escherichia coli catheter-associated urinary tract infections in mice. Antimicrob Agents Chemother. 2012;56:4738–4745.
- Yu J, Lin JH, Wu XR, et al. Uroplakins Ia and Ib, two major differentiation products of bladder epithelium, belong to a family of four transmembrane domain (4TM) proteins. J Cell Biol. 1994;125:171–182.
- 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 U S A. 1996;93:9630–9635.
- Anderson GG, Palermo JJ, Schilling JD, et al. Intracellular bacterial biofilm-like pods in urinary tract infections. Science. 2003;301:105–107.
- Song J, Bishop BL, Li G, et al. TLR4-mediated expulsion of bacteria from infected bladder epithelial cells. Proc Natl Acad Sci U S A. 2009;106:14966–14971.
- Allison KR, Brynildsen MP, Collins JJ. Metabolite-enabled eradication of bacterial persisters by aminoglycosides. Nature. 2011;473:216–220.
- Rosen DA, Hooton TM, Stamm WE, et al. Detection of intracellular bacterial communities in human urinary tract infection. PLoS Med. 2007;4:e329.
- Podolsky DK. Inflammatory bowel disease. N Engl J Med. 2002;347:417–429.
- Elson CO. Commensal bacteria as targets in Crohn’s disease. Gastroenterology. 2000;119:254–257.
- Baumgart M, Dogan B, Rishniw M, et al. Culture independent analysis of ileal mucosa reveals a selective increase in invasive Escherichia coli of novel phylogeny relative to depletion of Clostridiales in Crohn’s disease involving the ileum. Isme J. 2007;1:403–418.
- Lopez-Siles M, Martinez-Medina M, Busquets D, et al. Mucosa-associated Faecalibacterium prausnitzii and Escherichia coli co-abundance can distinguish irritable bowel syndrome and inflammatory bowel disease phenotypes. Int J Med Microbiol. 2014;304:464–475.
- Darfeuille-Michaud A, Boudeau J, Bulois P, et al. High prevalence of adherent-invasive Escherichia coli associated with ileal mucosa in Crohn’s disease. Gastroenterology. 2004;127:412–421.
- Martinez-Medina M, Garcia-Gil LJ. Escherichia coli in chronic inflammatory bowel diseases: an update on adherent invasive Escherichia coli pathogenicity. World J Gastrointest Pathophysiol. 2014;5:213–227.
- Carvalho FA, Barnich N, Sivignon A, et al. Crohn’s disease adherent-invasive Escherichia coli colonize and induce strong gut inflammation in transgenic mice expressing human CEACAM. J Exp Med. 2009;206:2179–2189.
- Barnich N, Carvalho FA, Glasser AL, et al. CEACAM6 acts as a receptor for adherent-invasive E. coli, supporting ileal mucosa colonization in Crohn disease. J Clin Invest. 2007;117:1566–1574.
- Mimouna S, Goncalves D, Barnich N, et al. Crohn disease-associated Escherichia coli promote gastrointestinal inflammatory disorders by activation of HIF-dependent responses. Gut Microbes. 2011;2:335–346.
- Dethlefsen L, Relman DA. Incomplete recovery and individualized responses of the human distal gut microbiota to repeated antibiotic perturbation. Proc Natl Acad Sci U S A. 2011;108(Suppl 1):4554–4561.
- Sekirov I, Tam NM, Jogova M, et al. Antibiotic-induced perturbations of the intestinal microbiota alter host susceptibility to enteric infection. Infect Immun. 2008;76:4726–4736.
- Aronson M, Medalia O, Schori L, et al. 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. 1979;139:329–332.
• First paper describing mannosides as strategy to block type 1 pili in UTI.
- Firon N, Ashkenazis S, Mirelman D, et al. Aromatic a-glycosides of mannose are powerful inhibitors of the adherence of type 1 fimbriated Escherichia coli to yeast and intestinal cells. Infect Immun. 1987;55:472–476.
• Discovery of potent monomeric aryl mannosides.
- Bouckaert J, Berglund J, Schembri M, et al. Receptor binding studies disclose a novel class of high-affinity inhibitors of the Escherichia coli FimH adhesin. Mol Microbiol. 2005;55:441–455.
•• X-ray crystal structure of D-Mannose and butylmannoside bound to FimH enabling rational structure-based design of mannosides.
- Hung C-S, Bouckaert J, Hung D, et al. Structural basis of tropism of Escherichia coli to the bladder during urinary tract infection. Mol Microbiol. 2002;44:903–915.
- Wellens A, Lahmann M, Touaibia M, et al. The tyrosine gate as a potential entropic lever in the receptor-binding site of the bacterial adhesin FimH. Biochemistry. 2012;51:4790–4799.
- Roos G, Wellens A, Touaibia M, et al. Validation of reactivity descriptors to assess the aromatic stacking within the tyrosine gate of FimH. ACS Med Chem Lett. 2013;4:1085–1090.
- Gouin S, Roos G, Bouckaert J. Discovery and application of FimH antagonists. Top Med Chem. 2014;12:123–168.
•• Recent litearture review on FiimH antagonists.
- Wellens A, Garofalo C, Nguyen H, et al. Intervening with urinary tract infections using anti-adhesives based on the crystal structure of the FimH-oligomannose-3 complex. PLoS One. 2008;3:e2040.
- Berglund J, Bouckaert J, De Greve H, et al. Anti-adhesive compounds to prevent and treat bacterial infections. WO/2005/089733. 2005.
- Sperling O, Fuchs A, Lindhorst TK. Evaluation of the carbohydrate recognition domain of the bacterial adhesin FimH: design, synthesis and binding properties of mannoside ligands. Org Biomol Chem. 2006;4:3913–3922.
- Janetka JW, Han Z, Hultgren S, et al. Compounds and methods for treating bacterial infections. WO/2011/050323. 2010.
• First patent publication on aryl and biaryl mannosides as monomeric FimH antagonists.
- Han Z, Pinkner JS, Ford B, et al. Lead optimization studies on FimH antagonists: discovery of potent and orally bioavailable ortho-substituted biphenyl mannosides. J Med Chem. 2012;55:3945–3959.
- Han Z, Pinkner JS, Ford B, et al. Structure-based drug design and optimization of mannoside bacterial FimH antagonists. J Med Chem. 2010;53:4779–4792.
•• Discovery of biphenyl/biaryl mannosides, X-ray structure and key SAR.
- Klein T, Abgottspon D, Wittwer M, et al. FimH antagonists for the oral treatment of urinary tract infections: from design and synthesis to in vitro and in vivo evaluation. J Med Chem. 2010;53:8627–8641.
- Ernst B, Herold J. Mannose derivatives as antagonists of bacterial adhesion. WO/2011/073112. 2010.
- Janetka JW, Han Z, Hultgren S, et al. Mannoside compounds and methods of use thereof. WO/2012/109263. 2012.
- Janetka JW, Han Z, Hultgren S, et al. Compounds and methods for treating bacterial infections. WO/2014/194270. 2014.
- Bennani YL, Cadilhac C, Das SK, et al. Mannose derivatives for treating bacterial infections. WO/2013/134415. 2014.
- Bennani YL, Liu B. Mannose derivatives for treating bacterial infections. WO/2014/055474. 2013.
- Dietrich E, Poisson C, Gallant M, et al. Mannose derivatives for treating bacterial infections. WO/2014/165107. 2014.
- Ernst B. Mannose phosphate derivatives as antagonists of bacterial adhesion. WO/2012/164074. 2012.
• Prodrug approach to mannosides.
- Ramtohul YK, Das SK, Cadilhac C, et al. Mannose derivatives for treating bacterial infections. WO/2014/100158. 2013.
- Bouckaert J, Gouin S, Deniaud D, et al. Multimeric mannosides, a process for preparing the same and their uses as a drug. WO/2014/016361. 2013.
- Bouckaert J, Gouin S, Sivignon A. Orally available compounds, A process for preparing the same and their uses as anti-adhesive drugs for treating E. coli induced inflammatory bowel diseases such as Crohn’s disease. WO/2015/110609. 2015.
• Demonstration of in vivo efficacy of a FimH antagonist in Crohn’s disease.
- Durka M, Buffet K, Iehl J, et al. The functional valency of dodecamannosylated fullerenes with Escherichia coli FimH–towards novel bacterial antiadhesives. Chem Communications. 2011;47:1321–1323.
- Jiang X, Abgottspon D, Kleeb S, et al. Antiadhesion therapy for urinary tract infections–a balanced PK/PD profile proved to be key for success. J Med Chem. 2012;55:4700–4713.
• Paper systematically profiling PK and PD of FimH antagonists for UTI.
- Scharenberg M, Abgottspon D, Cicek E, et al. A flow cytometry-based assay for screening FimH antagonists. Assay Drug Dev Technol. 2011;9:455–464.
- Abgottspon D, Rolli G, Hosch L, et al. Development of an aggregation assay to screen FimH antagonists. J Microbiol Methods. 2010;82:249–255.
- Cusumano CK, Pinkner JS, Han Z, et al. Treatment and prevention of urinary tract infection with orally active FimH inhibitors. Sci Transl Med. 2011;3:109–115.
•• Demonstration of oral efficacy of a FimH antagonist in acute and chronic animal models of UTI. First reported in vivo efficacy of any anti-virulence therapeutic in a bacterial infection.
- Brument S, Sivignon A, Dumych TI, et al. Thiazolylaminomannosides as potent antiadhesives of type 1 piliated Escherichia coli isolated from Crohn’s disease patients. J Med Chem. 2013;56:5395–5406.
• Identification of N-mannoside FimH ligands in Crohn’s disease, AIEC bacteria.
- Cecioni S, Imberty A, Vidal S. Glycomimetics versus multivalent glycoconjugates for the design of high affinity lectin ligands. Chem Rev. 2015;115:525–561.
• Excellent review on the glycodendrimer inhibitors of lectins in drug discovery.
- Parera Pera N, Branderhorst HM, Kooij R, et al. Rapid screening of lectins for multivalency effects with a glycodendrimer microarray. Chembiochem. 2010;11:1896–1904.
- Lindhorst TK, Kieburg C, Krallmann-Wenzel U. Inhibition of the type 1 fimbriae-mediated adhesion of Escherichia coli to erythrocytes by multiantennary alpha-mannosyl clusters: the effect of multivalency. Glycoconj J. 1998;15:605–613.
- Lindhorst TK, Bruegge K, Fuchs A, et al. A bivalent glycopeptide to target two putative carbohydrate binding sites on FimH. Beilstein J Org Chem. 2010;6:801–809.
- Bouckaert J, Li Z, Xavier C, et al. Heptyl alpha-D-mannosides grafted on a beta-cyclodextrin core to interfere with Escherichia coli adhesion: an in vivo multivalent effect. Chemistry. 2013;19:7847–7855.
- Janetka JW, Han Z, Hultgren S, et al. Compounds and methods for treating bacterial infections. US 8,937,167 B2. 2015 Jan 20.
- Sivignon A, Yan X, Alvarez Dorta D, et al. Development of heptylmannoside-based glycoconjugate antiadhesive compounds against adherent-invasive escherichia coli bacteria associated with Crohn’s disease. Mbio. 2015;6(6):pii:e01298-15. DOI:10.1128/mBio.01298-15.
- Walsh C. Where will new antibiotics come from? Nat Rev Microbiol. 2003;1:65–70.
- Varma MV, Feng B, Obach RS, et al. Physicochemical determinants of human renal clearance. J Med Chem. 2009;52:4844–4852.
- Ito S, Ando H, Ose A, et al. Relationship between the urinary excretion mechanisms of drugs and their physicochemical properties. J Pharm Sci. 2013;102:3294–3301.
- Ernst B, Magnani JL. From carbohydrate leads to glycomimetic drugs. Nat Rev Drug Discov. 2009;8:661–677.
• Excellent review on the use of carbohydrates and glycomimetics in drug discovery.
- Hartmann M, Papavlassopoulos H, Chandrasekaran V, et al. Inhibition of bacterial adhesion to live human cells: activity and cytotoxicity of synthetic mannosides. FEBS Lett. 2012;586:1459–1465.
- Kadam RU, Bergmann M, Garg D, et al. Structure-based optimization of the terminal tripeptide in glycopeptide dendrimer inhibitors of Pseudomonas aeruginosa biofilms targeting LecA. Chemistry. 2013;19:17054–17063.
- Hauck D, Joachim I, Frommeyer B, et al. Discovery of two classes of potent glycomimetic inhibitors of Pseudomonas aeruginosa LecB with distinct binding modes. ACS Chem Biol. 2013;8:1775–1784.
- Hofmann A, Sommer R, Hauck D, et al. Synthesis of mannoheptose derivatives and their evaluation as inhibitors of the lectin LecB from the opportunistic pathogen Pseudomonas aeruginosa. Carbohydr Res. 2015;412:34–42.