AFM in cellular and molecular microbiology.
adhesins
atomic force microscopy
cell adhesion
infection
pathogens
pilus
single cell microbiology
single molecules
Journal
Cellular microbiology
ISSN: 1462-5822
Titre abrégé: Cell Microbiol
Pays: India
ID NLM: 100883691
Informations de publication
Date de publication:
07 2021
07 2021
Historique:
revised:
22
02
2021
received:
18
12
2020
accepted:
23
02
2021
pubmed:
13
3
2021
medline:
1
1
2022
entrez:
12
3
2021
Statut:
ppublish
Résumé
The unique capabilities of the atomic force microscope (AFM), including super-resolution imaging, piconewton force-sensitivity, nanomanipulation and ability to work under physiological conditions, have offered exciting avenues for cellular and molecular biology research. AFM imaging has helped unravel the fine architectures of microbial cell envelopes at the nanoscale, and how these are altered by antimicrobial treatment. Nanomechanical measurements have shed new light on the elasticity, tensile strength and turgor pressure of single cells. Single-molecule and single-cell force spectroscopy experiments have revealed the forces and dynamics of receptor-ligand interactions, the nanoscale distribution of receptors on the cell surface and the elasticity and adhesiveness of bacterial pili. Importantly, recent force spectroscopy studies have demonstrated that extremely stable bonds are formed between bacterial adhesins and their cognate ligands, originating from a catch bond behaviour allowing the pathogen to reinforce adhesion under shear or tensile stress. Here, we survey how the versatility of AFM has enabled addressing crucial questions in microbiology, with emphasis on bacterial pathogens. TAKE AWAYS: AFM topographic imaging unravels the ultrastructure of bacterial envelopes. Nanomechanical mapping shows what makes cell envelopes stiff and resistant to drugs. Force spectroscopy characterises the molecular forces in pathogen adhesion. Stretching pili reveals a wealth of mechanical and adhesive responses.
Substances chimiques
Bacterial Proteins
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
e13324Subventions
Organisme : Fonds De La Recherche Scientifique - FNRS
ID : WELBIO-CR-2015A-05
Organisme : Horizon 2020 Framework Programme
ID : 693630
Informations de copyright
© 2021 John Wiley & Sons Ltd.
Références
Alsteens, D., Müller, D. J., & Dufrêne, Y. F. (2017). Multiparametric atomic force microscopy imaging of biomolecular and cellular systems. Accounts of Chemical Research, 50, 924-931.
Alsteens, D., Verbelen, C., Dague, E., Raze, D., Baulard, A. R., & Dufrêne, Y. F. (2008). Organization of the mycobacterial cell wall: A nanoscale view. Pflügers Archiv, 456, 117-125.
Ando, T., Uchihashi, T., & Scheuring, S. (2014). Filming biomolecular processes by high-speed atomic force microscopy. Chemical Reviews, 114, 3120-3188.
Andre, G., Kulakauskas, S., Chapot-Chartier, M.-P., Navet, B., Deghorain, M., Bernard, E., … Dufrêne, Y. F. (2010). Imaging the nanoscale organization of peptidoglycan in living Lactococcus lactis cells. Nature Communications, 1, 27.
Aubey, F., Corre, J.-P., Kong, Y., Xu, X., Obino, D., Goussard, S., … Duménil, G. (2019). Inhibitors of the Neisseria meningitidis PilF ATPase provoke type IV pilus disassembly. Proceedings of the National Academy of Sciences, 116, 8481-8486.
Beaussart, A., Abellán-Flos, M., El-Kirat-Chatel, S., Vincent, S. P., & Dufrêne, Y. F. (2016). Force nanoscopy as a versatile platform for quantifying the activity of antiadhesion compounds targeting bacterial pathogens. Nano Letters, 16, 1299-1307.
Beaussart, A., Baker, A. E., Kuchma, S. L., El-Kirat-Chatel, S., O'Toole, G. A., & Dufrêne, Y. F. (2014). Nanoscale adhesion forces of Pseudomonas aeruginosa type IV Pili. ACS Nano, 8, 10723-10733.
Beaussart, A., El-Kirat-Chatel, S., Sullan, R. M. A., Alsteens, D., Herman, P., Derclaye, S., & Dufrêne, Y. F. (2014). Quantifying the forces guiding microbial cell adhesion using single-cell force spectroscopy. Nature Protocols, 9, 1049-1055.
Biais, N., Ladoux, B., Higashi, D., So, M., & Sheetz, M. (2008). Cooperative retraction of bundled type IV pili enables nanonewton force generation. PLoS Biology, 6, e87.
Bowden, M. G., Heuck, A. P., Ponnuraj, K., Kolosova, E., Choe, D., Gurusiddappa, S., … Höök, M. (2008). Evidence for the “dock, lock, and latch” ligand binding mechanism of the Staphylococcal microbial surface component recognizing adhesive matrix molecules (MSCRAMM) SdrG. The Journal of Biological Chemistry, 283, 638-647.
Brooks, D. E., & Trust, T. J. (1983). Interactions of erythrocytes with bacteria under shear. Annals of the New York Academy of Sciences, 416, 319-331.
Buck, A. W., Fowler, V. G., Yongsunthon, R., Liu, J., DiBartola, A. C., Que, Y. -A., … Lower, S. K. (2010) Bonds between Fibronectin and Fibronectin-Binding Proteins on Staphylococcus aureus and Lactococcus lactis. Langmuir 26: 10764-10770.
Casillas-Ituarte, N. N., Lower, B. H., Lamlertthon, S., Fowler, V. G., & Lower, S. K. (2012). Dissociation rate constants of human fibronectin binding to fibronectin-binding proteins on living Staphylococcus aureus isolated from clinical patients. The Journal of Biological Chemistry, 287, 6693-6701.
Chagnot, C., Listrat, A., Astruc, T., & Desvaux, M. (2012). Bacterial adhesion to animal tissues: Protein determinants for recognition of extracellular matrix components. Cellular Microbiology, 14, 1687-1696.
Clausen, M., Koomey, M., & Maier, B. (2009). Dynamics of type IV pili is controlled by switching between multiple states. Biophysical Journal, 96, 1169-1177.
Craig, L., Forest, K. T., & Maier, B. (2019). Type IV pili: Dynamics, biophysics and functional consequences. Nature Reviews. Microbiology, 17, 429-440.
da Silva, A., & Teschke, O. (2003). Effects of the antimicrobial peptide PGLa on live Escherichia coli. Biochimica et Biophysica Acta - Molecular Cell Research, 1643, 95-103.
Dague, E., Alsteens, D., Latgé, J.-P., & Dufrêne, Y. F. (2008). High-resolution cell surface dynamics of germinating Aspergillus fumigatus conidia. Biophysical Journal, 94, 656-660.
Dembo, M., Torney, D. C., Saxman, K., Hammer, D., & Murray, J. D. (1988). The reaction-limited kinetics of membrane-to-surface adhesion and detachment. Proceedings of the Royal Society of London - Series B: Biological Sciences, 234, 55-83.
Denis, K., Le Bris, M., Le Guennec, L., Barnier, J.-P., Faure, C., Gouge, A., … Bourdoulous, S. (2019). Targeting Type IV pili as an antivirulence strategy against invasive meningococcal disease. Nature Microbiology, 4, 972-984.
Denise, R., Abby, S. S., & Rocha, E. P. C. (2019). Diversification of the type IV filament superfamily into machines for adhesion, protein secretion, DNA uptake, and motility. PLoS Biology, 17, e3000390.
Dufrêne, Y. F., Ando, T., Garcia, R., Alsteens, D., Martinez-Martin, D., Engel, A., … Müller, D. J. (2017). Imaging modes of atomic force microscopy for application in molecular and cell biology. Nature Nanotechnology, 12, 295-307.
Dufrêne, Y. F., Martínez-Martín, D., Medalsy, I., Alsteens, D., & Müller, D. J. (2013). Multiparametric imaging of biological systems by force-distance curve-based AFM. Nature Methods, 10, 847-854.
Dufrêne, Y. F., & Persat, A. (2020). Mechanomicrobiology: How bacteria sense and respond to forces. Nature Reviews. Microbiology, 18, 227-240.
Duménil, G. (2019). Type IV Pili as a therapeutic target. Trends in Microbiology, 27, 658-661.
Dupres, V., Alsteens, D., Pauwels, K., & Dufrêne, Y. F. (2009). In vivo imaging of S-Layer nanoarrays on Corynebacterium glutamicum. Langmuir, 25, 9653-9655.
Dupres, V., Menozzi, F. D., Locht, C., Clare, B. H., Abbott, N. L., Cuenot, S., … Dufrêne, Y. F. (2005). Nanoscale mapping and functional analysis of individual adhesins on living bacteria. Nature Methods, 2, 515-520.
Eaton, P., Fernandes, J. C., Pereira, E., Pintado, M. E., & Xavier Malcata, F. (2008). Atomic force microscopy study of the antibacterial effects of chitosans on Escherichia coli and Staphylococcus aureus. Ultramicroscopy, 108, 1128-1134.
Echelman, D. J., Alegre-Cebollada, J., Badilla, C. L., Chang, C., Ton-That, H., & Fernández, J. M. (2016). CnaA domains in bacterial pili are efficient dissipaters of large mechanical shocks. Proceedings of the National Academy of Sciences of the United States of America, 113, 2490-2495.
Ellison, C. K., Kan, J., Chlebek, J. L., Hummels, K. R., Panis, G., Viollier, P. H., … Brun, Y. V. (2019). A bifunctional ATPase drives tad pilus extension and retraction. Science Advances, 5, eaay2591.
Eskandarian, H. A., Odermatt, P. D., Ven, J. X. Y., Hannebelle, M. T. M., Nievergelt, A. P., Dhar, N., … Fantner, G. E. (2017). Division site selection linked to inherited cell surface wave troughs in mycobacteria. Nature Microbiology, 2, 17094.
Fantner, G. E., Barbero, R. J., Gray, D. S., & Belcher, A. M. (2010). Kinetics of antimicrobial peptide activity measured on individual bacterial cells using high-speed atomic force microscopy. Nature Nanotechnology, 5, 280-285.
Formosa, C., Grare, M., Duval, R. E., & Dague, E. (2012). Nanoscale effects of antibiotics on P. aeruginosa. Nanomedicine Nanotechnol Biol Med, 8, 12-16.
Forero, M., Yakovenko, O., Sokurenko, E. V., Thomas, W. E., & Vogel, V. (2006). Uncoiling mechanics of Escherichia coli type I fimbriae are optimized for catch bonds. PLoS Biology, 4, e298.
Foster, T. J. (2004). The Staphylococcus aureus “superbug.”. The Journal of Clinical Investigation, 114, 1693-1696.
Foster, T. J. (2016). The remarkably multifunctional fibronectin binding proteins of Staphylococcus aureus. European Journal of Clinical Microbiology & Infectious Diseases, 35, 1923-1931.
Foster, T. J., Geoghegan, J. A., Ganesh, V. K., & Höök, M. (2014). Adhesion, invasion and evasion: the many functions of the surface proteins of Staphylococcus aureus. Nature Reviews. Microbiology, 12, 49-62.
Francius, G., Domenech, O., Mingeot-Leclercq, M. P., & Dufrêne, Y. F. (2008). Direct observation of Staphylococcus aureus cell wall digestion by lysostaphin. Journal of Bacteriology, 190, 7904-7909.
Geoghegan, J. A., Foster, T. J., Speziale, P., & Dufrêne, Y. F. (2017). Live-cell nanoscopy in antiadhesion therapy. Trends in Microbiology, 25, 512-514.
Gibiansky, M. L., Conrad, J. C., Jin, F., Gordon, V. D., Motto, D. A., Mathewson, M. A., … Wong, G. C. L. (2010). Bacteria use type IV pili to walk upright and detach from surfaces. Science, 330, 197-197.
Giltner, C. L., Nguyen, Y., & Burrows, L. L. (2012). Type IV pilin proteins: Versatile molecular modules. Microbiology and Molecular Biology Reviews, 76, 740-772.
Hahn, E., Wild, P., Hermanns, U., Sebbel, P., Glockshuber, R., Häner, M., … Müller, S. A. (2002). Exploring the 3D molecular architecture of Escherichia coli type 1 pili. Journal of Molecular Biology, 323, 845-857.
Hannebelle, M. T. M., Ven, J. X. Y., Toniolo, C., Eskandarian, H. A., Vuaridel-Thurre, G., McKinney, J. D., & Fantner, G. E. (2020). A biphasic growth model for cell pole elongation in mycobacteria. Nature Communications, 11, 452.
Hendrickx, A. P. A., Poor, C. B., Jureller, J. E., Budzik, J. M., He, C., & Schneewind, O. (2012). Isopeptide bonds of the major pilin protein BcpA influence pilus structure and bundle formation on the surface of Bacillus cereus. Molecular Microbiology, 85, 152-163.
Herman, P., El-Kirat-Chatel, S., Beaussart, A., Geoghegan, J. A., Foster, T. J., & Dufrêne, Y. F. (2014). The binding force of the staphylococcal adhesin SdrG is remarkably strong. Molecular Microbiology, 93, 356-368.
Herman-Bausier, P., Labate, C., Towell, A. M., Derclaye, S., Geoghegan, J. A., & Dufrêne, Y. F. (2018). Staphylococcus aureus clumping factor A is a force-sensitive molecular switch that activates bacterial adhesion. Proceedings of the National Academy of Sciences, 115, 5564-5569.
Hockenberry, A. M., Hutchens, D. M., Agellon, A., & So, M. (2016). Attenuation of the type IV pilus retraction motor influences Neisseria gonorrhoeae social and infection behavior. MBio, 7, e01994-e01916.
Höltje, J. V. (1998). Growth of the stress-bearing and shape-maintaining murein sacculus of Escherichia coli. Microbiology and Molecular Biology Reviews: MMBR, 62, 181-203.
Kankainen, M., Paulin, L., Tynkkynen, S., von Ossowski, I., Reunanen, J., Partanen, P., … de Vos, W. M. (2009). Comparative genomic analysis of Lactobacillus rhamnosus GG reveals pili containing a human-mucus binding protein. Proceedings of the National Academy of Sciences, 106, 17193-17198.
Koch, A. L. (1988). Biophysics of bacterial walls viewed as stress-bearing fabric. Microbiological Reviews, 52, 337-353.
Konto-Ghiorghi, Y., Mairey, E., Mallet, A., Duménil, G., Caliot, E., Trieu-Cuot, P., & Dramsi, S. (2009). Dual role for pilus in adherence to epithelial cells and biofilm formation in Streptococcus agalactiae. PLoS Pathogens, 5, e1000422.
Krieg, M., Fläschner, G., Alsteens, D., Gaub, B. M., Roos, W. H., Wuite, G. J. L., … Müller, D. J. (2019). Atomic force microscopy-based mechanobiology. Nature Reviews Physics, 1, 41-57.
Le Trong, I., Aprikian, P., Kidd, B. A., Forero-Shelton, M., Tchesnokova, V., Rajagopal, P., … Thomas, W. E. (2010). Structural basis for mechanical force regulation of the adhesin FimH via finger trap-like β sheet twisting. Cell, 141, 645-655.
Li, M., Gan, C., Shao, W., Yu, C., Wang, X., & Chen, Y. (2016). Effects of membrane lipid composition and antibacterial drugs on the rigidity of Escherichia coli: Different contributions of various bacterial substructures. Scanning, 38, 70-79.
Liu, Z., Liu, H., Vera, A. M., Bernardi, R. C., Tinnefeld, P., & Nash, M. A. (2020). High force catch bond mechanism of bacterial adhesion in the human gut. Nature Communications, 11, 4321.
Lo Giudice, C., Dumitru, A. C., & Alsteens, D. (2019). Probing ligand-receptor bonds in physiologically relevant conditions using AFM. Analytical and Bioanalytical Chemistry, 411, 6549-6559.
Longo, G., Rio, L. M., Trampuz, A., Dietler, G., Bizzini, A., & Kasas, S. (2013). Antibiotic-induced modifications of the stiffness of bacterial membranes. Journal of Microbiological Methods, 93, 80-84.
Loskill, P., Pereira, P. M., Jung, P., Bischoff, M., Herrmann, M., Pinho, M. G., & Jacobs, K. (2014). Reduction of the peptidoglycan crosslinking causes a decrease in stiffness of the Staphylococcus aureus cell envelope. Biophysical Journal, 107, 1082-1089.
Lower, S. K., Lamlertthon, S., Casillas-Ituarte, N. N., Lins, R. D., Yongsunthon, R., Taylor, E. S., … Fowler, V. G. (2011). Polymorphisms in fibronectin binding protein A of Staphylococcus aureus are associated with infection of cardiovascular devices. Proceedings of the National Academy of Sciences, 108, 18372-18377.
Lu, S., Giuliani, M., Harvey, H., Burrows, L. L., Wickham, R. A., & Dutcher, J. R. (2015). Nanoscale pulling of type IV pili reveals their flexibility and adhesion to surfaces over extended lengths of the pili. Biophysical Journal, 108, 2865-2875.
Lugmaier, R. A., Schedin, S., Kühner, F., & Benoit, M. (2008). Dynamic restacking of Escherichia coli P-pili. European Biophysics Journal, 37, 111-120.
Marshall, B. T., Long, M., Piper, J. W., Yago, T., McEver, R. P., & Zhu, C. (2003). Direct observation of catch bonds involving cell-adhesion molecules. Nature, 423, 190-193.
Mathelié-Guinlet, M., Asmar, A. T., Collet, J.-F., & Dufrêne, Y. F. (2020). Lipoprotein Lpp regulates the mechanical properties of the E. coli cell envelope. Nature Communications, 11, 1789.
Mathelié-Guinlet, M., Viela, F., Pietrocola, G., Speziale, P., Alsteens, D., & Dufrêne, Y. F. (2020). Force-clamp spectroscopy identifies a catch bond mechanism in a Gram-positive pathogen. Nature Communications, 11, 5431.
Memmi, G., Filipe, S. R., Pinho, M. G., Fu, Z., & Cheung, A. (2008). Staphylococcus aureus PBP4 is essential for beta-lactam resistance in community-acquired methicillin-resistant strains. Antimicrobial Agents and Chemotherapy, 52, 3955-3966.
Mignolet, J., Holden, S., Bergé, M., Panis, G., Eroglu, E., Théraulaz, L., … Viollier, P. H. (2016). Functional dichotomy and distinct nanoscale assemblies of a cell cycle-controlled bipolar zinc-finger regulator. eLife, 5, e18647.
Mignolet, J., Panis, G., & Viollier, P. H. (2018). More than a Tad: Spatiotemporal control of Caulobacter pili. Current Opinion in Microbiology, 42, 79-86.
Milles, L. F., & Gaub, H. E. (2020). Extreme mechanical stability in protein complexes. Current Opinion in Structural Biology, 60, 124-130.
Milles, L. F., Schulten, K., Gaub, H. E., & Bernardi, R. C. (2018). Molecular mechanism of extreme mechanostability in a pathogen adhesin. Science, 359, 1527-1533.
Milles, L. F., Unterauer, E. M., Nicolaus, T., & Gaub, H. E. (2018). Calcium stabilizes the strongest protein fold. Nature Communications, 9, 1-10.
Nievergelt, A. P., Banterle, N., Andany, S. H., Gönczy, P., & Fantner, G. E. (2018). High-speed photothermal off-resonance atomic force microscopy reveals assembly routes of centriolar scaffold protein SAS-6. Nature Nanotechnology, 13, 696-701.
Nievergelt, A. P., Brillard, C., Eskandarian, H. A., McKinney, J. D., & Fantner, G. E. (2018). Photothermal off-resonance tapping for rapid and gentle atomic force imaging of live cells. International Journal of Molecular Sciences, 19, E2984.
Odermatt, P. D., Hannebelle, M. T. M., Eskandarian, H. A., Nievergelt, A. P., McKinney, J. D., & Fantner, G. E. (2020). Overlapping and essential roles for molecular and mechanical mechanisms in mycobacterial cell division. Nature Physics, 16, 57-62.
Otto, M. (2009). Staphylococcus epidermidis-The “accidental” pathogen. Nature Reviews. Microbiology, 7, 555-567.
Overton, K., Greer, H. M., Ferguson, M. A., Spain, E. M., Elmore, D. E., Núñez, M. E., & Volle, C. B. (2020). Qualitative and quantitative changes to Escherichia coli during treatment with Magainin 2 observed in native conditions by atomic force microscopy. Langmuir, 36, 650-659.
Pasquina-Lemonche, L., Burns, J., Turner, R. D., Kumar, S., Tank, R., Mullin, N., … Hobbs, J. K. (2020). The architecture of the Gram-positive bacterial cell wall. Nature, 582, 294-297.
Phan, G., Remaut, H., Wang, T., Allen, W. J., Pirker, K. F., Lebedev, A., … Waksman, G. (2011). Crystal structure of the FimD usher bound to its cognate FimC-FimH substrate. Nature, 474, 49-53.
Pizarro-Cerdá, J., & Cossart, P. (2006). Bacterial adhesion and entry into host cells. Cell, 124, 715-727.
Pogoda, K., Piktel, E., Deptuła, P., Savage, P. B., Lekka, M., & Bucki, R. (2017). Stiffening of bacteria cells as a first manifestation of bactericidal attack. Micron, 101, 95-102.
Ponnuraj, K., Bowden, M. G., Davis, S., Gurusiddappa, S., Moore, D., Choe, D., … Narayana, S. V. L. (2003). A “dock, lock, and latch” structural model for a Staphylococcal adhesin binding to fibrinogen. Cell, 115, 217-228.
Prystopiuk, V., Feuillie, C., Herman-Bausier, P., Viela, F., Alsteens, D., Pietrocola, G., … Dufrêne, Y. F. (2018). Mechanical forces guiding Staphylococcus aureus cellular invasion. ACS Nano, 12, 3609-3622.
Quilès, F., Barth, D., Peric, O., Fantner, G. E., & Francius, G. (2020). Parietal structures of Escherichia coli can impact the d-cateslytin antibacterial activity. ACS Chemical Biology, 15, 2801-2814.
Rabbani, S., Fiege, B., Eris, D., Silbermann, M., Jakob, R. P., Navarra, G., … Ernst, B. (2018). Conformational switch of the bacterial adhesin FimH in the absence of the regulatory domain: Engineering a minimalistic allosteric system. The Journal of Biological Chemistry, 293, 1835-1849.
Rojas, E. R., Billings, G., Odermatt, P. D., Auer, G. K., Zhu, L., Miguel, A., … Huang, K. C. (2018). The outer membrane is an essential load-bearing element in Gram-negative bacteria. Nature, 559, 617-621.
Saar Dover, R., Bitler, A., Shimoni, E., Trieu-Cuot, P., & Shai, Y. (2015). Multiparametric AFM reveals turgor-responsive net-like peptidoglycan architecture in live streptococci. Nature Communications, 6, 7193.
Sauer, F. G., Pinkner, J. S., Waksman, G., & Hultgren, S. J. (2002). Chaperone priming of pilus subunits facilitates a topological transition that drives fiber formation. Cell, 111, 543-551.
Sauer, M. M., Jakob, R. P., Eras, J., Baday, S., Eriş, D., Navarra, G., … Glockshuber, R. (2016). Catch-bond mechanism of the bacterial adhesin FimH. Nature Communications, 7, 1-13.
Schwarz-Linek, U., Gurusiddappa, S., Kim, J. H., Pilka, E. S., Briggs, J. A. G., Gough, T. S., … Potts, J. R. (2003). Pathogenic bacteria attach to human fibronectin through a tandem b-zipper, 423, 5.
Silhavy, T. J., Kahne, D., & Walker, S. (2010). The bacterial cell envelope. Cold Spring Harbor Perspectives in Biology, 2, a000414.
Sullan, R. M. A., Beaussart, A., Tripathi, P., Derclaye, S., El-Kirat-Chatel, S., Li, J. K., … Dufrêne, Y. F. (2014). Single-cell force spectroscopy of pili-mediated adhesion. Nanoscale, 6, 1134-1143.
Telford, J. L., Barocchi, M. A., Margarit, I., Rappuoli, R., & Grandi, G. (2006). Pili in Gram-positive pathogens. Nature Reviews. Microbiology, 4, 509-519.
Thomas, W., Forero, M., Yakovenko, O., Nilsson, L., Vicini, P., Sokurenko, E., & Vogel, V. (2006). Catch-bond model derived from allostery explains force-activated bacterial adhesion. Biophysical Journal, 90, 753-764.
Thomas, W. E., Nilsson, L. M., Forero, M., Sokurenko, E. V., & Vogel, V. (2004). Shear-dependent ‘stick-and-roll’ adhesion of type 1 fimbriated Escherichia coli. Molecular Microbiology, 53, 1545-1557.
Thomas, W. E., Trintchina, E., Forero, M., Vogel, V., & Sokurenko, E. V. (2002). Bacterial adhesion to target cells enhanced by shear force. Cell, 109, 913-923.
Thomas, W. E., Vogel, V., & Sokurenko, E. (2008). Biophysics of catch bonds. Annual Review of Biophysics, 37, 399-416.
Touhami, A., Nysten, B., & Dufrêne, Y. F. (2003). Nanoscale mapping of the elasticity of microbial cells by atomic force microscopy. Langmuir, 19, 4539-4543.
Tripathi, P., Beaussart, A., Alsteens, D., Dupres, V., Claes, I., von Ossowski, I., … Dufrêne, Y. F. (2013). Adhesion and nanomechanics of pili from the probiotic Lactobacillus rhamnosus GG. ACS Nano, 7, 3685-3697.
Tripathi, P., Dupres, V., Beaussart, A., Lebeer, S., Claes, I. J. J., Vanderleyden, J., & Dufrêne, Y. F. (2012). Deciphering the nanometer-scale organization and assembly of Lactobacillus rhamnosus GG pili using atomic force microscopy. Langmuir, 28, 2211-2216.
Turner, R. D., Hurd, A. F., Cadby, A., Hobbs, J. K., & Foster, S. J. (2013). Cell wall elongation mode in Gram-negative bacteria is determined by peptidoglycan architecture. Nature Communications, 4, 1496.
Turner, R. D., Mesnage, S., Hobbs, J. K., & Foster, S. J. (2018). Molecular imaging of glycan chains couples cell-wall polysaccharide architecture to bacterial cell morphology. Nature Communications, 9, 1263.
Turner, R. D., Ratcliffe, E. C., Wheeler, R., Golestanian, R., Hobbs, J. K., & Foster, S. J. (2010). Peptidoglycan architecture can specify division planes in Staphylococcus aureus. Nature Communications, 1, 26.
Vassen, V., Valotteau, C., Feuillie, C., Formosa-Dague, C., Dufrêne, Y. F., & De Bolle, X. (2019). Localized incorporation of outer membrane components in the pathogen Brucella abortus. The EMBO Journal, 38, e100323.
Velegol, S. B., & Logan, B. E. (2002). Contributions of bacterial surface polymers, electrostatics, and cell elasticity to the shape of AFM force curves. Langmuir, 18, 5256-5262.
Verbelen, C., Dupres, V., Menozzi, F. D., Raze, D., Baulard, A. R., Hols, P., & Dufrêne, Y. F. (2006). Ethambutol-induced alterations in Mycobacterium bovis BCG imaged by atomic force microscopy. FEMS Microbiology Letters, 264, 192-197.
Viela, F., Mathelié-Guinlet, M., Pietrocola, G., Speziale, P., & Dufrêne, Y. F. (2020). The molecular complex between Staphylococcal adhesin SpsD and fibronectin sustains mechanical forces in the nanonewton range. MBio, 11, e00371-e00320.
Viela, F., Prystopiuk, V., Leprince, A., Mahillon, J., Speziale, P., Pietrocola, G., & Dufrêne, Y. F. (2019). Binding of Staphylococcus aureus Protein A to von Willebrand factor is regulated by mechanical force. MBio, 10, e00555-e00519.
Viljoen, A., Foster, S. J., Fantner, G. E., Hobbs, J. K., & Dufrêne, Y. F. (2020). Scratching the surface: Bacterial cell envelopes at the nanoscale. MBio, 11, e03020-19.
Vitry, P., Valotteau, C., Feuillie, C., Bernard, S., Alsteens, D., Geoghegan, J. A., & Dufrêne, Y. F. (2017). Force-induced strengthening of the interaction between Staphylococcus aureus clumping factor B and loricrin. MBio, 8, e01748-e01717.
Yakovenko, O., Sharma, S., Forero, M., Tchesnokova, V., Aprikian, P., Kidd, B., … Thomas, W. E. (2008). FimH forms catch bonds that are enhanced by mechanical force due to allosteric regulation. The Journal of Biological Chemistry, 283, 11596-11605.