Reprint of "biogenesis and adhesion of type 1 and P pili"

Biochimica et Biophysica Acta - General Subjects

Volumn 1850, Issue 3, 2015, Pages 554-564

  Lillington, James ^a   Geibel, Sebastian ^a   Waksman, Gabriel ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Chaperone; Donor strand exchange; Macromolecular machine; Pilicides; Pilus; Usher

Indexed keywords

ADHESIN; ESCHERICHIA COLI PROTEIN; UNCLASSIFIED DRUG; USHER PROTEIN;

ARTICLE; BACTERIAL GROWTH; BACTERIAL STRUCTURES; BACTERIUM ADHERENCE; BACTERIUM PILUS; BIOGENESIS; CARBOXY TERMINAL SEQUENCE; CATALYSIS; CORRELATIONAL STUDY; CYTOPLASM; GROWTH INHIBITION; INHIBITION KINETICS; NONHUMAN; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN QUATERNARY STRUCTURE; REGULATORY MECHANISM; UROPATHOGENIC ESCHERICHIA COLI; UROPATHOGENIC ESCHERICHIA COLI TYPE 1;

ESCHERICHIA COLI;

EID: 84921059374     PISSN: 03044165     EISSN: 18728006     Source Type: Journal    
DOI: 10.1016/j.bbagen.2014.07.009     Document Type: Review

References (99)

1. G.C. Ulett, M. Totsika, K. Schaale, A.J. Carey, M.J. Sweet, and M.A. Schembri Uropathogenic Escherichia coli virulence and innate immune responses during urinary tract infection Curr. Opin. Microbiol. 16 2013 100 107
2. G.R. Nielubowicz, and H.L.T. Mobley Host-pathogen interactions in urinary tract infection Nat. Rev. Urol. 7 2010 430 441
3. K.E. Sivick, and H.L.T. Mobley Waging war against uropathogenic Escherichia coli: winning back the urinary tract Infect. Immun. 78 2010 568 585
4. P. O'Hanley, D. Lark, S. Falkow, and G. Schoolnik 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 1985 347 360
5. I. Connell, W. Agace, P. Klemm, M. Schembri, S. Mərild, and C. Svanborg Type 1 fimbrial expression enhances Escherichia coli virulence for the urinary tract Proc. Natl. Acad. Sci. U. S. A. 93 1996 9827 9832
6. A.W.H. Lo, K. Moonens, and H. Remaut Chemical attenuation of pilus function and assembly in Gram-negative bacteria Curr. Opin. Microbiol. 16 2013 85 92
7. D.G. Thanassi, J.B. Bliska, and P.J. Christie Surface organelles assembled by secretion systems of Gram-negative bacteria: diversity in structure and function FEMS Microbiol. Rev. 36 2012 1046 1082
8. S. Geibel, and G. Waksman The molecular dissection of the chaperone-usher pathway Biochim. Biophys. Acta. 1843 2014 1559 1567
9. J. Lillington, and G. Waksman Ordered and ushered; the assembly and translocation of the adhesive Type I and P Pili Biology (Basel) 2 2013 841 860
10. W.J. Allen, G. Phan, and G. Waksman Pilus biogenesis at the outer membrane of Gram-negative bacterial pathogens Curr. Opin. Struct. Biol. 22 2012 500 506
11. A. Busch, and G. Waksman Chaperone-usher pathways: diversity and pilus assembly mechanism Philos. Trans. R. Soc. Lond. B Biol. Sci. 367 2012 1112 1122
12. W.R. Schwan Regulation of fim genes in uropathogenic Escherichia coli World J. Clin. Infect. Dis. 1 2011 17 25
13. D. Choudhury, A. Thompson, V. Stojanoff, S. Langermann, J. Pinkner, S.J. Hultgren, and S.D. Knight X-ray structure of the FimC-FimH chaperone-adhesin complex from uropathogenic Escherichia coli Science 285 1999 1061 1066
14. K.W. Dodson, J.S. Pinkner, T. Rose, G. Magnusson, S.J. Hultgren, and G. Waksman Structural basis of the interaction of the pyelonephritic E. coli adhesin to its human kidney receptor Cell 105 2001 733 743
15. X. Mu, and E. Bullitt Structure and assembly of P-pili: a protruding hinge region used for assembly of a bacterial adhesion filament Proc. Natl. Acad. Sci. U. S. A. 103 2006 9861 9866
16. E. Hahn, P. Wild, U. Hermanns, P. Sebbel, R. Glockshuber, M. Häner, N. Taschner, P. Burkhard, U. Aebi, and S.A. Müller Exploring the 3D molecular architecture of Escherichia coli type 1 pili J. Mol. Biol. 323 2002 845 857
17. D. Verger, E. Miller, H. Remaut, G. Waksman, and S. Hultgren Molecular mechanism of P pilus termination in uropathogenic Escherichia coli EMBO Rep. 7 2006 1228 1232
18. G.M. Rossolini, P. Muscas, A. Chiesurin, and G. Satta Analysis of the Salmonella fim gene cluster: identification of a new gene (fimI) encoding a fimbrin-like protein and located downstream from the fimA gene FEMS Microbiol. Lett. 114 1993 259 265
19. M.L. Valenski, S.L. Harris, P.A. Spears, J.R. Horton, and P.E. Orndorff The product of the fimI gene is necessary for Escherichia coli type 1 pilus biosynthesis J. Bacteriol. 185 2003 5007 5011
20. C. Stathopoulos, D.R. Hendrixson, D.G. Thanassi, S.J. Hultgren, J.W. St. Geme III, and R. Curtiss III Secretion of virulence determinants by the general secretory pathway in Gram-negative pathogens: an evolving story Microbes Infect. 2 2000 1061 1072
21. M.D. Crespo, C. Puorger, M.A. Schärer, O. Eidam, M.G. Grütter, G. Capitani, and R. Glockshuber Quality control of disulfide bond formation in pilus subunits by the chaperone FimC Nat. Chem. Biol. 8 2012 707 713
22. F.G. Sauer, K. Fütterer, J.S. Pinkner, K.W. Dodson, S.J. Hultgren, and G. Waksman Structural basis of chaperone function and pilus biogenesis Science 285 1999 1058 1061
23. A.V. Zavialov, J. Berglund, A.F. Pudney, L.J. Fooks, T.M. Ibrahim, S. MacIntyre, and S.D. Knight Structure and biogenesis of the capsular F1 antigen from Yersinia pestis: preserved folding energy drives fiber formation Cell 113 2003 587 596
24. T.W. Ng, L. Akman, M. Osisami, and D.G. Thanassi The usher N terminus is the initial targeting site for chaperone-subunit complexes and participates in subsequent pilus biogenesis events J. Bacteriol. 186 2004 5321 5331
25. M. Nishiyama, M. Vetsch, C. Puorger, I. Jelesarov, and R. Glockshuber Identification and characterization of the chaperone-subunit complex-binding domain from the type 1 pilus assembly platform FimD J. Mol. Biol. 330 2003 513 525
26. N.S. Henderson, T.W. Ng, I. Talukder, and D.G. Thanassi Function of the usher N-terminus in catalysing pilus assembly Mol. Microbiol. 79 2011 954 967
27. F.G. Sauer, J.S. Pinkner, G. Waksman, and S.J. Hultgren Chaperone priming of pilus subunits facilitates a topological transition that drives fiber formation Cell 111 2002 543 551
28. A.V. Zavialov, V.M. Tischenko, L.J. Fooks, B.O. Brandsdal, J. Aqvist, V.P. Zav'yalov, S. Macintyre, and S.D. Knight Resolving the energy paradox of chaperone/usher-mediated fibre assembly Biochem. J. 389 2005 685 694
29. C. Puorger, O. Eidam, G. Capitani, D. Erilov, M.G. Grütter, and R. Glockshuber Infinite kinetic stability against dissociation of supramolecular protein complexes through donor strand complementation Structure 16 2008 631 642
30. H. Remaut, C. Tang, N.S. Henderson, J.S. Pinkner, T. Wang, S.J. Hultgren, D.G. Thanassi, G. Waksman, and H. Li Fiber formation across the bacterial outer membrane by the chaperone/usher pathway Cell 133 2008 640 652
31. Y. Huang, B.S. Smith, L.X. Chen, R.H.G. Baxter, and J. Deisenhofer Insights into pilus assembly and secretion from the structure and functional characterization of usher PapC Proc. Natl. Acad. Sci. U. S. A. 106 2009 7403 7407
32. G. Phan, H. Remaut, T. Wang, W.J. Allen, K.F. Pirker, A. Lebedev, N.S. Henderson, S. Geibel, E. Volkan, J. Yan, M.B.A. Kunze, J.S. Pinkner, B. Ford, C.W.M. Kay, H. Li, S.J. Hultgren, D.G. Thanassi, and G. Waksman Crystal structure of the FimD usher bound to its cognate FimC: FimH substrate Nature 474 2011 49 53
33. E. Volkan, B.A. Ford, J.S. Pinkner, K.W. Dodson, N.S. Henderson, D.G. Thanassi, G. Waksman, and S.J. Hultgren Domain activities of PapC usher reveal the mechanism of action of an Escherichia coli molecular machine Proc. Natl. Acad. Sci. U. S. A. 109 2012 9563 9568
34. M. Nishiyama, R. Horst, O. Eidam, T. Herrmann, O. Ignatov, M. Vetsch, P. Bettendorff, I. Jelesarov, M.G. Grütter, K. Wüthrich, R. Glockshuber, and G. Capitani Structural basis of chaperone-subunit complex recognition by the type 1 pilus assembly platform FimD EMBO J. 24 2005 2075 2086
35. B. Ford, A.T. Rêgo, T.J. Ragan, J. Pinkner, K. Dodson, P.C. Driscoll, S. Hultgren, and G. Waksman Structural homology between the C-terminal domain of the PapC usher and its plug J. Bacteriol. 192 2010 1824 1831
36. B. Morrissey, A.C. Leney, A. Toste Rêgo, G. Phan, W.J. Allen, D. Verger, G. Waksman, A.E. Ashcroft, and S.E. Radford The role of chaperone-subunit usher domain interactions in the mechanism of bacterial pilus biogenesis revealed by ESI-MS Mol. Cell. Proteomics 11 2012 (M111.015289)
37. O. Eidam, F.S.N. Dworkowski, R. Glockshuber, M.G. Grütter, and G. Capitani Crystal structure of the ternary FimC-FimFt-FimDN complex indicates conserved pilus chaperone-subunit complex recognition by the usher FimD 2008
38. M. Nishiyama, and R. Glockshuber The outer membrane usher guarantees the formation of functional pili by selectively catalyzing donor-strand exchange between subunits that are adjacent in the mature pilus J. Mol. Biol. 396 2010 1 8
39. H. Remaut, R.J. Rose, T.J. Hannan, S.J. Hultgren, S.E. Radford, A.E. Ashcroft, and G. Waksman Donor-strand exchange in chaperone-assisted pilus assembly proceeds through a concerted beta strand displacement mechanism Mol. Cell 22 2006 831 842
40. R.J. Rose, T.S. Welsh, G. Waksman, A.E. Ashcroft, S.E. Radford, and E. Paci Donor-strand exchange in chaperone-assisted pilus assembly revealed in atomic detail by molecular dynamics J. Mol. Biol. 375 2008 908 919
41. S. Geibel, E. Procko, S.J. Hultgren, D. Baker, and G. Waksman Structural and energetic basis of folded-protein transport by the FimD usher Nature 496 2013 243 246
42. X. Di Yu, A. Dubnovitsky, A.F. Pudney, S. Macintyre, S.D. Knight, and A.V. Zavialov Allosteric mechanism controls traffic in the chaperone/usher pathway Structure 20 2012 1861 1871
43. R.J. Rose, D. Verger, T. Daviter, H. Remaut, E. Paci, G. Waksman, A.E. Ashcroft, and S.E. Radford Unraveling the molecular basis of subunit specificity in P pilus assembly by mass spectrometry Proc. Natl. Acad. Sci. U. S. A. 105 2008 12873 12878
44. M. Nishiyama, T. Ishikawa, H. Rechsteiner, and R. Glockshuber Reconstitution of pilus assembly reveals a bacterial outer membrane catalyst Science 320 2008 376 379
45. W.J. Allen, G. Phan, S.J. Hultgren, and G. Waksman Dissection of pilus tip assembly by the FimD usher monomer J. Mol. Biol. 425 2013 958 967
46. E.T. Saulino, D.G. Thanassi, J.S. Pinkner, and S.J. Hultgren Ramifications of kinetic partitioning on usher-mediated pilus biogenesis EMBO J. 17 1998 2177 2185
47. A.C. Leney, G. Phan, W. Allen, D. Verger, G. Waksman, S.E. Radford, and A.E. Ashcroft Second order rate constants of donor-strand exchange reveal individual amino acid residues important in determining the subunit specificity of pilus biogenesis J. Am. Soc. Mass Spectrom. 22 2011 1214 1223
48. D. Verger, R.J. Rose, E. Paci, G. Costakes, T. Daviter, S. Hultgren, H. Remaut, A.E. Ashcroft, S.E. Radford, and G. Waksman Structural determinants of polymerization reactivity of the P pilus adaptor subunit PapF Structure 16 2008 1724 1731
49. M. Båga, M. Norgren, and S. Normark Biogenesis of E. coli Pap pili: papH, a minor pilin subunit involved in cell anchoring and length modulation Cell 49 1987 241 251
50. O.S. Mapingire, N.S. Henderson, G. Duret, D.G. Thanassi, and A.H. Delcour Modulating effects of the plug, helix, and N- and C-terminal domains on channel properties of the PapC usher J. Biol. Chem. 284 2009 36324 36333
51. B. Wullt, G. Bergsten, H. Connell, P. Röllano, N. Gebretsadik, R. Hull, and C. Svanborg P fimbriae enhance the early establishment of Escherichia coli in the human urinary tract Mol. Microbiol. 38 2000 456 464
52. A. Svensson, A. Larsson, H. Emtenäs, M. Hedenström, T. Fex, S.J. Hultgren, J.S. Pinkner, F. Almqvist, and J. Kihlberg Design and evaluation of pilicides: potential novel antibacterial agents directed against uropathogenic Escherichia coli Chembiochem 2 2001 915 918
53. J.S. Pinkner, H. Remaut, F. Buelens, E. Miller, V. Aberg, N. Pemberton, M. Hedenström, A. Larsson, P. Seed, G. Waksman, S.J. Hultgren, and F. Almqvist Rationally designed small compounds inhibit pilus biogenesis in uropathogenic bacteria Proc. Natl. Acad. Sci. U. S. A. 103 2006 17897 17902
54. E. Chorell, J.S. Pinkner, G. Phan, S. Edvinsson, F. Buelens, H. Remaut, G. Waksman, S.J. Hultgren, and F. Almqvist Design and synthesis of C-2 substituted thiazolo and dihydrothiazolo ring-fused 2-pyridones: pilicides with increased antivirulence activity J. Med. Chem. 53 2010 5690 5695
55. A.W.H. Lo, K. Van de Water, P.J. Gane, A.W.E. Chan, D. Steadman, K. Stevens, D.L. Selwood, G. Waksman, and H. Remaut Suppression of type 1 pilus assembly in uropathogenic Escherichia coli by chemical inhibition of subunit polymerization J. Antimicrob. Chemother. 69 2014 1017 1026
56. G.G. Anderson, J.J. Palermo, J.D. Schilling, R. Roth, J. Heuser, and S.J. Hultgren Intracellular bacterial biofilm-like pods in urinary tract infections Science 301 2003 105 107
57. Bacterial Secreted Proteins: Secretory Mechanisms and Role in Pathogenesis 2009 Horizon Scientific Press
58. T.J. Hannan, M. Totsika, K.J. Mansfield, K.H. Moore, M.A. Schembri, and S.J. Hultgren Host-pathogen checkpoints and population bottlenecks in persistent and intracellular uropathogenic Escherichia coli bladder infection FEMS Microbiol. Rev. 36 2012 616 648
59. M.A. Mulvey, Y.S. Lopez-Boado, C.L. Wilson, R. Roth, W.C. Parks, J. Heuser, and S.J. Hultgren Induction and evasion of host defenses by type 1-piliated uropathogenic Escherichia coli Science 282 1998 1494 1497
60. J.A. Roberts, B.I. Marklund, D. Ilver, D. Haslam, M.B. Kaack, G. Baskin, M. Louis, R. Möllby, J. Winberg, and S. Normark The Gal(alpha 1-4)Gal-specific tip adhesin of Escherichia coli P-fimbriae is needed for pyelonephritis to occur in the normal urinary tract Proc. Natl. Acad. Sci. U. S. A. 91 1994 11889 11893
61. N.J. Holden, M. Totsika, E. Mahler, A.J. Roe, K. Catherwood, K. Lindner, U. Dobrindt, and D.L. Gally Demonstration of regulatory cross-talk between P fimbriae and type 1 fimbriae in uropathogenic Escherichia coli Microbiology 152 2006 1143 1153
62. K. Melican, R.M. Sandoval, A. Kader, L. Josefsson, G.A. Tanner, B.A. Molitoris, and A. Richter-Dahlfors Uropathogenic Escherichia coli P and Type 1 fimbriae act in synergy in a living host to facilitate renal colonization leading to nephron obstruction PLoS Pathog. 7 2011 e1001298
63. O. Yakovenko, S. Sharma, M. Forero, V. Tchesnokova, P. Aprikian, B. Kidd, A. Mach, V. Vogel, E. Sokurenko, and W.E. Thomas FimH forms catch bonds that are enhanced by mechanical force due to allosteric regulation J. Biol. Chem. 283 2008 11596 11605
64. O. Björnham, H. Nilsson, M. Andersson, and S. Schedin Physical properties of the specific PapG-galabiose binding in E. coli P pili-mediated adhesion Eur. Biophys. J. 38 2009 245 254
65. D.E. Rangel, N. Marín-Medina, J.E. Castro, A. González-Mancera, and M. Forero-Shelton Observation of bacterial type I pili extension and contraction under fluid flow PLoS One 8 2013 e65563
66. A. Larsson, J. Ohlsson, K.W. Dodson, S.J. Hultgren, U. Nilsson, and J. Kihlberg Quantitative studies of the binding of the class II PapG adhesin from uropathogenic Escherichia coli to oligosaccharides Bioorg. Med. Chem. 11 2003 2255 2261
67. R.A. Lugmaier, S. Schedin, F. Kühner, and M. Benoit Dynamic restacking of Escherichia coli P pili Eur. Biophys. J. 37 2008 111 120
68. N. Strömberg, B.I. Marklund, B. Lund, D. Ilver, A. Hamers, W. Gaastra, K.A. Karlsson, and S. Normark Host-specificity of uropathogenic Escherichia coli depends on differences in binding specificity to Gal alpha 1-4Gal-containing isoreceptors EMBO J. 9 1990 2001 2010
69. A. Wellens, M. Lahmann, M. Touaibia, J. Vaucher, S. Oscarson, R. Roy, H. Remaut, and J. Bouckaert The tyrosine gate as a potential entropic lever in the receptor-binding site of the bacterial adhesin FimH Biochemistry 51 2012 4790 4799
70. I. Le Trong, P. Aprikian, B.A. Kidd, M. Forero-Shelton, V. Tchesnokova, P. Rajagopal, V. Rodriguez, G. Interlandi, R. Klevit, V. Vogel, R.E. Stenkamp, E.V. Sokurenko, and W.E. Thomas Structural basis for mechanical force regulation of the adhesin FimH via finger trap-like beta sheet twisting Cell 141 2010 645 655
71. E.V. Sokurenko, V. Vogel, and W.E. Thomas Catch-bond mechanism of force-enhanced adhesion: counterintuitive, elusive, but widespread? Cell Host Microbe 4 2008 314 323
72. V. Tchesnokova, P. Aprikian, D. Kisiela, S. Gowey, N. Korotkova, W. Thomas, and E. Sokurenko Type 1 fimbrial adhesin FimH elicits an immune response that enhances cell adhesion of Escherichia coli Infect. Immun. 79 2011 3895 3904
73. P. Aprikian, V. Tchesnokova, B. Kidd, O. Yakovenko, V. Yarov-Yarovoy, E. Trinchina, V. Vogel, W. Thomas, and E. Sokurenko Interdomain interaction in the FimH adhesin of Escherichia coli regulates the affinity to mannose J. Biol. Chem. 282 2007 23437 23446
74. W.E. Thomas, E. Trintchina, M. Forero, V. Vogel, and E.V. Sokurenko Bacterial adhesion to target cells enhanced by shear force Cell 109 2002 913 923
75. V. Tchesnokova, P. Aprikian, O. Yakovenko, C. Larock, B. Kidd, V. Vogel, W. Thomas, and E. Sokurenko Integrin-like allosteric properties of the catch bond-forming FimH adhesin of Escherichia coli J. Biol. Chem. 283 2008 7823 7833
76. V.B. Rodriguez, B.A. Kidd, G. Interlandi, V. Tchesnokova, E.V. Sokurenko, and W.E. Thomas Allosteric coupling in the bacterial adhesive protein FimH J. Biol. Chem. 288 2013 24128 24139
77. L.M. Nilsson, W.E. Thomas, E.V. Sokurenko, and V. Vogel Elevated shear stress protects Escherichia coli cells adhering to surfaces via catch bonds from detachment by soluble inhibitors Appl. Environ. Microbiol. 72 2006 3005 3010
78. D.J. Schwartz, V. Kalas, J.S. Pinkner, S.L. Chen, C.N. Spaulding, K.W. Dodson, and S.J. Hultgren Positively selected FimH residues enhance virulence during urinary tract infection by altering FimH conformation Proc. Natl. Acad. Sci. U. S. A. 110 2013 15530 15537
79. J. Zakrisson, K. Wiklund, O. Axner, and M. Andersson The shaft of the type 1 fimbriae regulates an external force to match the FimH catch bond Biophys. J. 104 2013 2137 2148
80. J. Jass, S. Schedin, E. Fällman, J. Ohlsson, U.J. Nilsson, B.E. Uhlin, and O. Axner Physical properties of Escherichia coli P pili measured by optical tweezers Biophys. J. 87 2004 4271 4283
81. M. Andersson, O. Axner, F. Almqvist, B.E. Uhlin, and E. Fällman Physical properties of biopolymers assessed by optical tweezers: analysis of folding and refolding of bacterial pili ChemPhysChem 9 2008 221 235
82. I.L. Jäger The "sticky chain": a kinetic model for the deformation of biological macromolecules Biophys. J. 81 2001 1897 1906
83. M. Andersson, E. Fällman, B.E. Uhlin, and O. Axner A sticky chain model of the elongation and unfolding of Escherichia coli P pili under stress Biophys. J. 90 2006 1521 1534
84. M. Andersson, E. Fällman, B.E. Uhlin, and O. Axner Dynamic force spectroscopy of E. coli P pili Biophys. J. 91 2006 2717 2725
85. E. Fällman, S. Schedin, J. Jass, B.-E. Uhlin, and O. Axner The unfolding of the P pili quaternary structure by stretching is reversible, not plastic EMBO Rep. 6 2005 52 56
86. M. Andersson, B.E. Uhlin, and E. Fällman The biomechanical properties of E. coli pili for urinary tract attachment reflect the host environment Biophys. J. 93 2007 3008 3014
87. M. Forero, O. Yakovenko, E.V. Sokurenko, W.E. Thomas, and V. Vogel Uncoiling mechanics of Escherichia coli type I fimbriae are optimized for catch bonds PLoS Biol. 4 2006 e298
88. J. Gosline, M. Lillie, E. Carrington, P. Guerette, C. Ortlepp, and K. Savage Elastic proteins: biological roles and mechanical properties Philos. Trans. R. Soc. Lond. B Biol. Sci. 357 2002 121 132
89. K.L. Anderson, J. Billington, D. Pettigrew, E. Cota, P. Simpson, P. Roversi, H.A. Chen, P. Urvil, L. du Merle, P.N. Barlow, M.E. Medof, R.A.G. Smith, B. Nowicki, C. Le Bouguénec, S.M. Lea, and S. Matthews An atomic resolution model for assembly, architecture, and function of the Dr adhesins Mol. Cell 15 2004 647 657
90. J.A. Silverman, H.L. Schreiber, T.M. Hooton, and S.J. Hultgren From physiology to pharmacy: developments in the pathogenesis and treatment of recurrent urinary tract infections Curr. Urol. Rep. 14 2013 448 456
91. S. Brument, A. Sivignon, T.I. Dumych, N. Moreau, G. Roos, Y. Guérardel, T. Chalopin, D. Deniaud, R.O. Bilyy, A. Darfeuille-Michaud, J. Bouckaert, and S.G. Gouin Thiazolylaminomannosides as potent antiadhesives of type 1 piliated Escherichia coli isolated from Crohn's disease patients J. Med. Chem. 56 2013 5395 5406
92. J. Bouckaert, Z. Li, C. Xavier, M. Almant, V. Caveliers, T. Lahoutte, S.D. Weeks, J. Kovensky, and S.G. Gouin Heptyl α-d-mannosides grafted on a β-cyclodextrin core to interfere with Escherichia coli adhesion: an in vivo multivalent effect Chemistry 19 2013 7847 7855
93. V. Chandrasekaran, K. Kolbe, F. Beiroth, and T.K. Lindhorst Synthesis and testing of the first azobenzene mannobioside as photoswitchable ligand for the bacterial lectin FimH Beilstein J. Org. Chem. 9 2013 223 233
94. C.K. Cusumano, J.S. Pinkner, Z. Han, S.E. Greene, B.A. Ford, J.R. Crowley, J.P. Henderson, J.W. Janetka, and S.J. Hultgren Treatment and prevention of urinary tract infection with orally active FimH inhibitors Sci. Transl. Med. 3 2011 109ra115
95. R.E. Watts, C.K. Tan, G.C. Ulett, A.J. Carey, M. Totsika, A. Idris, A.W. Paton, R. Morona, J.C. Paton, and M.A. Schembri Escherichia coli 83972 expressing a P fimbriae oligosaccharide receptor mimic impairs adhesion of uropathogenic E. coli J. Infect. Dis. 206 2012 1242 1249
96. S. Martin-Sosa, M.-J. Martin, and P. Hueso The sialylated fraction of milk oligosaccharides is partially responsible for binding to enterotoxigenic and uropathogenic Escherichia coli human strains J. Nutr. 132 2002 3067 3072
97. J. Ohlsson, J. Jass, B.E. Uhlin, J. Kihlberg, and U.J. Nilsson Discovery of potent inhibitors of PapG adhesins from uropathogenic Escherichia coli through synthesis and evaluation of galabiose derivatives Chembiochem 3 2002 772 779
98. J.E. Klinth, J.S. Pinkner, S.J. Hultgren, F. Almqvist, B.E. Uhlin, and O. Axner Impairment of the biomechanical compliance of P pili: a novel means of inhibiting uropathogenic bacterial infections? Eur. Biophys. J. 41 2012 285 295
99. N. Mortezaei, B. Singh, E. Bullitt, B.E. Uhlin, and M. Andersson P-fimbriae in the presence of anti-PapA antibodies: new insight of antibodies action against pathogens Sci. Rep. 3 2013 3393