Force nanoscopy as a versatile platform for quantifying the activity of antiadhesion compounds targeting bacterial pathogens

Nano Letters

Volumn 16, Issue 2, 2016, Pages 1299-1307

  Beaussart, Audrey ^a,d   Abellán Flos, Marta ^b   El Kirat Chatel, Sofiane ^a,e,f   Vincent, Stéphane P ^b   Dufrêne, Yves F ^a,c  

^a UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

^b UNIVERSITY OF NAMUR   (Belgium)

^c Walloon Excellence in Life Sciences and Biotechnology (WELBIO)   (Belgium)

^d CNRS   (France)

^e UNIVERSITÉ DE LORRAINE   (France)

^f Laboratoire de Chimie Physique et Microbiologie pour l'Environnement   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESION; ATOMIC FORCE MICROSCOPY; CARBOHYDRATES; DISEASE CONTROL; ESCHERICHIA COLI; FULLERENES;

BACTERIAL DISEASE; BACTERIAL PATHOGENS; BACTERIAL STRAINS; CARBOHYDRATE LIGANDS; CARBOHYDRATE RECEPTORS; MICROBIAL INFECTIONS; MULTIDRUG RESISTANTS; UROPATHOGENIC ESCHERICHIA COLI;

BACTERIA;

ANTIINFECTIVE AGENT; NANOPARTICLE; THIOL DERIVATIVE;

ANTIBIOTIC RESISTANCE; ATOMIC FORCE MICROSCOPY; BACTERIUM; BACTERIUM ADHERENCE; CHEMISTRY; DRUG EFFECTS; HUMAN; PATHOGENICITY;

ANTI-BACTERIAL AGENTS; BACTERIA; BACTERIAL ADHESION; DRUG RESISTANCE, BACTERIAL; HUMANS; MICROSCOPY, ATOMIC FORCE; NANOPARTICLES; SULFHYDRYL COMPOUNDS;

EID: 84958206689     PISSN: 15306984     EISSN: 15306992     Source Type: Journal    
DOI: 10.1021/acs.nanolett.5b04689     Document Type: Article

References (36)

1. Ofek, I.; Hasty, D. L.; Sharon, N. Anti-adhesion therapy of bacterial diseases: prospects and problems FEMS Immunol. Med. Microbiol. 2003, 38, 181-191 10.1016/S0928-8244(03)00228-1
2. Sharon, N. Carbohydrates as future anti-adhesion drugs for infectious diseases Biochim. Biophys. Acta, Gen. Subj. 2006, 1760, 527-537 10.1016/j.bbagen.2005.12.008
3. Shoaf-Sweeney, K. D.; Hutkins, R. W. Adherence, anti-adherence, and oligosaccharides preventing pathogens from sticking to the host Adv. Food Nutr. Res. 2008, 55, 101-161 10.1016/S1043-4526(08)00402-6
4. Shmuely, H.; Ofek, I.; Weiss, E. I.; Rones, Z.; Houri-Haddad, Y. Cranberry components for the therapy of infectious disease Curr. Opin. Biotechnol. 2012, 23, 148-152 10.1016/j.copbio.2011.10.009
5. Krachler, A. M.; Orth, K. Targeting the bacteria-host interface Virulence 2013, 4, 284-294 10.4161/viru.24606
6. Aronson, M.; Medalia, O.; Schori, L.; Mirelman, D.; Sharon, N.; Ofek, I. 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 10.1093/infdis/139.3.329
7. Lindhorst, T. K.; 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 Glycoconjugate J. 1998, 15, 605-613 10.1023/A:1006920027641
8. Lindhorst, T. K.; Dubber, M. Octopus glycosides: multivalent molecular platforms for testing carbohydrate recognition and bacterial adhesion Carbohydr. Res. 2015, 403, 90-97 10.1016/j.carres.2014.06.032
9. Touaibia, M.; Roy, R. Glycodendrimers as anti-adhesion drugs against type 1 fimbriated E. coli uropathogenic infections Mini-Rev. Med. Chem. 2007, 7, 1270-1283 10.2174/138955707782795610
10. Touaibia, M.; Wellens, A.; Shiao, T. C.; Wang, Q.; Sirois, S.; Bouckaert, J.; Roy, R. Mannosylated G(0) Dendrimers with Nanomolar Affinities to Escherichia coli FimH ChemMedChem 2007, 2, 1190-1201 10.1002/cmdc.200700063
11. Durka, M.; Buffet, K.; Iehl, J.; Holler, M.; Nierengarten, J.-F.; Taganna, J.; Bouckaert, J.; Vincent, S. P. The functional valency of dodecamannosylated fullerenes with Escherichia coli FimH - towards novel bacterial antiadhesives Chem. Commun. 2011, 47, 1321-1323 10.1039/C0CC04468G
12. Hahn, E.; Wild, P.; Hermanns, U.; Sebbel, P.; Glockshuber, R.; Häner, M.; Taschner, N.; Burkhard, P.; Aebi, U.; Müller, S. A. Exploring the 3D molecular architecture of Escherichia coli type 1 pili J. Mol. Biol. 2002, 323, 845-857 10.1016/S0022-2836(02)01005-7
13. Iehl, J.; Nierengarten, J. F. A Click-Click Approach for the Preparation of Functionalized [5:1]-Hexaadducts of C60 Chem.-Eur. J. 2009, 15, 7306-7309 10.1002/chem.200901291
14. Fortgang, P.; Maisonhaute, E.; Amatore, C.; Delavaux-Nicot, B.; Iehl, J.; Nierengarten, J. F. Molecular Motion Inside an Adsorbed [5:1] Fullerene Hexaadduct Observed by Ultrafast Cyclic Voltammetry Angew. Chem., Int. Ed. 2011, 50, 2364-2367 10.1002/anie.201007289
15. MunÌoz, A.; Sigwalt, D.; Illescas, B. M.; Luczkowiak, J.; Rodriguez-Perez, L.; Nierengarten, I.; Holler, M.; Remy, J.-S.; Buffet, K.; Vincent, S. P.; Rojo, J.; Delgado, R.; Nierengarten, J. F.; Martín, N. Nat. Chem. 2015, 8, 50-57 10.1038/nchem.2387
16. Bouckaert, J.; Li, Z.; Xavier, C.; Almant, M.; Caveliers, V.; Lahoutte, T.; Weeks, S. D.; Kovensky, J.; Gouin, S. G. Heptyl α- D-Mannosides Grafted on a β-Cyclodextrin Core To Interfere with Escherichia coli Adhesion: An In Vivo Multivalent Effect Chem.-Eur. J. 2013, 19, 7847-7855 10.1002/chem.201204015
17. Gobbo, P.; Workentin, M. S. Improved methodology for the preparation of water-soluble maleimide-functionalized small gold nanoparticles Langmuir 2012, 28, 12357-12363 10.1021/la302168g
18. Gobbo, P.; Novoa, S.; Biesinger, M. C.; Workentin, M. S. Interfacial strain-promoted alkyne-azide cycloaddition (I-SPAAC) for the synthesis of nanomaterial hybrids Chem. Commun. 2013, 49, 3982-3984 10.1039/c3cc41634h
19. Nierengarten, J.-F.; Iehl, J.; Oerthel, V.; Holler, M.; Illescas, B. M.; Munìoz, A.; Martín, N.; Rojo, J.; Sánchez-Navarro, M.; Cecioni, S.; Vidal, S.; Buffet, K.; Durka, M.; Vincent, S. P. Fullerene sugar balls Chem. Commun. 2010, 46, 3860-3862 10.1039/c0cc00034e
20. Durka, M.; Buffet, K.; Iehl, J.; Holler, M.; Nierengarten, J.-F.; Vincent, S. P. The Inhibition of Liposaccharide Heptosyltransferase WaaC with Multivalent Glycosylated Fullerenes: A New Mode of Glycosyltransferase Inhibition Chem.-Eur. J. 2012, 18, 641-651 10.1002/chem.201102052
21. Buffet, K.; Gillon, E.; Holler, M.; Nierengarten, J.-F.; Imberty, A.; Vincent, S. P. Fucofullerenes as tight ligands of RSL and LecB, two bacterial lectins Org. Biomol. Chem. 2015, 13, 6482-6492 10.1039/C5OB00689A
22. Abellán-Flos, M.; Tanç, M.; Supuran, C. T.; Vincent, S. P. Exploring carbonic anhydrase inhibition with multimeric coumarins displayed on a fullerene scaffold Org. Biomol. Chem. 2015, 13, 7445-7451 10.1039/C5OB01005E
23. Bryan, M. C.; Fazio, F.; Lee, H.-K.; Huang, C.-Y.; Chang, A.; Best, M. D.; Calarese, D. A.; Blixt, O.; Paulson, J. C.; Burton, D.; Wilson, I. A.; Wong, C.-H. Covalent display of oligosaccharide arrays in microtiter plates J. Am. Chem. Soc. 2004, 126, 8640-8641 10.1021/ja048433f
24. Huang, C.-Y.; Thayer, D. A.; Chang, A. Y.; Best, M. D.; Hoffmann, J.; Head, S.; Wong, C.-H. Carbohydrate Microarray for Profiling the Antibodies Interacting with Globo H Tumor Antigen Proc. Natl. Acad. Sci. U. S. A. 2006, 103, 15-20 10.1073/pnas.0509693102
25. El-Kirat-Chatel, S.; Beaussart, A.; Vincent, S. P.; Abellán Flos, M.; Hols, P.; Lipke, P. N.; Dufrêne, Y. F. Forces in yeast flocculation Nanoscale 2015, 7, 1760-1767 10.1039/C4NR06315E
26. Bouckaert, J.; Berglund, J.; Schembri, M.; De Genst, E.; Cools, L.; Wuhrer, M.; Hung, C.-S.; Pinkner, J.; Slättegard, R.; Zavialov, A.; Choudhury, D.; Langermann, S.; Hultgren, S. J.; Wyns, L.; Klemm, P.; Oscarson, S.; Knight, S. D.; De Greve, H. Receptor binding studies disclose a novel class of high-affinity inhibitors of the Escherichia coli FimH adhesin Mol. Microbiol. 2005, 55, 441-455 10.1111/j.1365-2958.2004.04415.x
27. Dupres, V.; Menozzi, F. D.; Locht, C.; Clare, B. H.; Abbott, N. L.; Cuenot, S.; Bompard, C.; Raze, D.; Dufrene, Y. F. Nanoscale mapping and functional analysis of individual adhesins on living bacteria Nat. Methods 2005, 2, 515-520 10.1038/nmeth769
28. Alsteens, D.; Garcia, M. C.; Lipke, P. N.; Dufrene, Y. F. Force-induced formation and propagation of adhesion nanodomains in living fungal cells Proc. Natl. Acad. Sci. U. S. A. 2010, 107, 20744-20749 10.1073/pnas.1013893107
29. Andre, G.; Kulakauskas, S.; Chapot-Chartier, M. P.; Navet, B.; Deghorain, M.; Bernard, E.; Hols, P.; Dufrene, Y. F. Imaging the nanoscale organization of peptidoglycan in living Lactococcus lactis cells Nat. Commun. 2010, 1, 27 10.1038/ncomms1027
30. Forero, M.; Yakovenko, O.; Sokurenko, E. V.; Thomas, W. E.; Vogel, V. Uncoiling mechanics of Escherichia coli type I fimbriae are optimized for catch bonds PLoS Biol. 2006, 4, e298 10.1371/journal.pbio.0040298
31. Miller, E.; Garcia, T.; Hultgren, S.; Oberhauser, A. F. The mechanical properties of E. coli type 1 pili measured by atomic force microscopy techniques Biophys. J. 2006, 91, 3848-3456 10.1529/biophysj.106.088989
32. Helenius, J.; Heisenberg, C. P.; Gaub, H. E.; Muller, D. J. Single-cell force spectroscopy J. Cell Sci. 2008, 121, 1785-1791 10.1242/jcs.030999
33. Beaussart, A.; El-Kirat-Chatel, S.; Herman, P.; Alsteens, D.; Mahillon, J.; Hols, P.; Dufrene, Y. F. Single-cell force spectroscopy of probiotic bacteria Biophys. J. 2013, 104, 1886-1892 10.1016/j.bpj.2013.03.046
34. Guillaume-Gentil, O.; Potthoff, E.; Ossola, D.; Franz, C. M.; Zambelli, T.; Vorholt, J. A. Force-controlled manipulation of single cells: from AFM to FluidFM Trends Biotechnol. 2014, 32, 381-388 10.1016/j.tibtech.2014.04.008
35. Gouin, S. G.; Wellens, A.; Bouckaert, J.; Kovensky, J. Synthetic multimeric heptyl mannosides as potent antiadhesives of uropathogenic Escherichia coli ChemMedChem 2009, 4, 749-755 10.1002/cmdc.200900034
36. Beaussart, A.; El-Kirat-Chatel, S.; Sullan, R. M. A.; Alsteens, D.; Herman, P.; Derclaye, S.; Dufrêne, Y. F. Quantifying the forces guiding microbial cell adhesion using single-cell force spectroscopy Nat. Protoc. 2014, 9, 1049-1055 10.1038/nprot.2014.066