Use of atomic force microscopy to study the multi-modular interaction of bacterial adhesins to mucins

International Journal of Molecular Sciences

Volumn 17, Issue 11, 2016, Pages

  Gunning, A Patrick ^a   Kavanaugh, Devon ^a   Thursby, Elizabeth ^a   Etzold, Sabrina ^a,b   Mackenzie, Donald A ^a   Juge, Nathalie ^a  

^a NORWICH RESEARCH PARK   (United Kingdom)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

Atomic force microscopy; Bacterial adhesins; Gut microbiota; Intestinal mucin; Lactobacillus reuteri; Mucus binding protein; Single molecule force spectroscopy

Indexed keywords

3 [(3 CHOLAMIDOPROPYL)DIMETHYLAMMONIO] 1 PROPANESULFONIC ACID; ADHESIN; CARBOHYDRATE BINDING PROTEIN; GALECTIN 3; LACTOSE; MUCIN 1; MUCIN 2; STOMACH MUCIN; CONDITIONED MEDIUM; MUCIN 3; PROTEIN BINDING; RECOMBINANT PROTEIN;

ARTICLE; ATOMIC FORCE MICROSCOPE; ATOMIC FORCE MICROSCOPY; BACTERIUM ADHERENCE; BINDING SITE; CELL ADHESION; ECHOGRAPHY; GASTROINTESTINAL TRACT; HETEROLOGOUS EXPRESSION; HISTOGRAM; LACTOBACILLUS; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRECIPITATION; PROTEIN CARBOHYDRATE INTERACTION; PROTEIN UNFOLDING; SIZE EXCLUSION CHROMATOGRAPHY; ANIMAL; CHEMISTRY; CONDITIONED MEDIUM; GENE EXPRESSION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; INTESTINE MUCOSA; ISOLATION AND PURIFICATION; LACTOBACILLUS REUTERI; METABOLISM; MOLECULAR MODEL; PIG;

ADHESINS, BACTERIAL; ANIMALS; BACTERIAL ADHESION; CULTURE MEDIA, CONDITIONED; GALECTIN 3; GENE EXPRESSION; HUMANS; INTESTINAL MUCOSA; LACTOBACILLUS REUTERI; MICROSCOPY, ATOMIC FORCE; MODELS, MOLECULAR; MUCIN-3; PROTEIN BINDING; RECOMBINANT PROTEINS; SWINE;

EID: 84994691962     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms17111854     Document Type: Article

References (66)

1. Bäckhed, F.; Ley, R.E.; Sonnenburg, J.L.; Peterson, D.A.; Gordon, J.I. Host-bacterial mutualism in the human intestine. Science 2005, 307, 1915-1920.
2. Chang, C.; Lin, H. Dysbiosis in gastrointestinal disorders. Best Pract. Res. Clin. Gastroenterol. 2016, 30, 3-15.
3. Johansson, M.E.; Ambort, D.; Pelaseyed, T.; Schütte, A.; Gustafsson, J.K.; Ermund, A.; Subramani, D.B.; Holmén-Larsson, J.M.; Thomsson, K.A.; Bergström, J.H.; et al. Composition and functional role of the mucus layers in the intestine. Cell. Mol. Life Sci. 2011, 68, 3635-3641.
4. Brockhausen, I.; Schachter, H.; Stanley, P. O-GalNAc glycans. Essentials of Glycobiology; Varki, A., Cummings, R.D., Esko, J.D., Eds.; Cold Spring Harbor Laboratory Press: New York, NY, USA, 2009; pp. 115-128.
5. Juge, N. Microbial adhesins to gastrointestinal mucus. Trends Microbiol. 2012, 20, 30-39.
6. Tailford, L.E.; Crost, E.H.; Kavanaugh, D.; Juge, N. Mucin glycan foraging in the human gut microbiome. Front. Genet. 2015, 6, 81.
7. Gerbino, E.; Carasi, P.; Mobili, P.; Serradell, M.A.; Gómez-Zavaglia, A. Role of S-layer proteins in bacteria. World J. Microbiol. Biotechnol. 2015, 31, 1877-1887.
8. Hymes, J.P.; Johnson, B.R.; Barrangou, R.; Klaenhammer, T.R. Functional analysis of an S-Layer-associated fibronectin-binding protein in Lactobacillus acidophilus NCFM. Appl. Environ. Microbiol. 2016, 82, 2676-2685.
9. Granato, D.; Perotti, F.; Masserey, I.; Rouvet, M.; Golliard, M.; Servin, A.; Brassart, D. Cell Surface-Associated Lipoteichoic Acid Acts as an Adhesion Factor for Attachment of Lactobacillus johnsonii La1 to Human Enterocyte-Like Caco-2 Cells. Appl. Environ. Microbiol. 1999, 65, 1071-1077.
10. Walter, J.; Loach, D.M.; Alqumber, M.; Rockel, C.; Hermann, C.; Pfitzenmaier, M.; Tannock, G.W. D-alanyl ester depletion of teichoic acids in Lactobacillus reuteri 100-23 results in impaired colonization of the mouse gastrointestinal tract. Environ. Microbiol. 2007, 9, 1750-1760.
11. Kankainen, M.; Paulin, L.; Tynkkynen, S.; von Ossowski, I.; Reunanen, J.; Partanen, P.; Satokari, R.; Vesterlund, S.; Hendrickx, A.P.; Lebeer, S.; et al. Comparative genomic analysis of Lactobacillus rhamnosus GG reveals pili containing a human-mucus binding protein. Proc. Natl. Acad. Sci. USA 2009, 106, 17193-17198.
12. Von Ossowski, I.; Reunanen, J.; Satokari, R.; Vesterlund, S.; Kankainen, M.; Huhtinen, H.; Tynkkynen, S.; Salminen, S.; de Vos, W.M.; Palva, A. Mucosal adhesion properties of the probiotic Lactobacillus rhamnosus GG SpaCBA and SpaFED pilin subunits. Appl. Environ. Microbiol. 2010, 76, 2049-2057.
13. Castelain, M.; Duviau, M.P.; Oxaran, V.; Schmitz, P.; Cocaign-Bousquet, M.; Loubière, P.; Piard, J.C.; Mercier-Bonin, M. Oligomerized backbone pilin helps piliated Lactococcus lactis to withstand shear flow. Biofouling 2016, 32, 911-923.
14. Nishiyama, K.; Ueno, S.; Sugiyama, M.; Yamamoto, Y.; Mukai, T. Lactobacillus rhamnosus GG SpaC pilin subunit binds to the carbohydrate moieties of intestinal glycoconjugates. Anim. Sci. J. 2016, 87, 809-815.
15. Suzuki, K.; Nishiyama, K.; Miyajima, H.; Osawa, R.; Yamamoto, Y.; Mukai, T. Adhesion properties of a putative polymorphic fimbrial subunit protein from Bifidobacterium longum subsp. longum. Biosci. Microbiota Food Health 2016, 35, 19-27.
16. Granato, D.; Bergonzelli, G.E.; Pridmore, R.D.; Marvin, L.; Rouvet, M.; Corthésy-Theulaz, I.E. Cell surface-associated elongation factor Tu mediates the attachment of Lactobacillus johnsonii NCC533 (La1) to human intestinal cells and mucins. Infect. Immun. 2004, 72, 2160-2169.
17. Bergonzelli, G.E.; Granato, D.; Pridmore, R.D.; Marvin-Guy, L.F.; Donnicola, D.; Corthésy-Theulaz, I.E. GroEL of Lactobacillus johnsonii La1 (NCC 533) is cell surface associated: potential role in interactions with the host and the gastric pathogen Helicobacter pylori. Infect. Immun. 2006, 74, 425-434.
18. Kinoshita, H.; Uchida, H.; Kawai, Y.; Kawasaki, T.; Wakahara, N.; Matsuo, H.; Watanabe, M.; Kitazawa, H.; Ohnuma, S.; Miura, K.; et al. Cell surface Lactobacillus plantarum LA 318 glyceraldehyde-3-phosphate dehydrogenase (GAPDH) adheres to human colonic mucin. J. Appl. Microbiol. 2008, 104, 1667-1674.
19. Nishiyama, K.; Ochiai, A.; Tsubokawa, D.; Ishihara, K.; Yamamoto, Y.; Mukai, T. Identification and characterization of sulfated carbohydrate-binding protein from Lactobacillus reuteri. PLoS ONE 2013, 8, e83703.
20. Patel, D.K.; Shah, K.R.; Pappachan, A.; Gupta, S.; Singh, D.D. Cloning, expression and characterization of a mucin-binding GAPDH from Lactobacillus acidophilus. Int. J. Biol. Macromol. 2016, 91, 338-346.
21. Petrova, M.I.; Imholz, N.C.; Verhoeven, T.L.; Balzarini, J.; van Damme, E.J.; Schols, D.; Vanderleyden, J.; Lebeer, S. Lectin-Like molecules of Lactobacillus rhamnosus GG inhibit pathogenic Escherichia coli and Salmonella biofilm formation. PLoS ONE 2016, 11, e0161337.
22. Valeriano, V.D.; Bagon, B.B.; Balolong, M.P.; Kang, D.K. Carbohydrate-binding specificities of potential probiotic Lactobacillus strains in porcine jejunal (IPEC-J2) cells and porcine mucin. J. Microbiol. 2016, 54, 510-519.
23. Etzold, S.; Juge, N. Structural insights into bacterial recognition of intestinal mucins. Curr. Opin. Struct. Biol. 2014, 28, 23-31.
24. Roos, S.; Jonsson, H. A high-molecular-mass cell-surface protein from Lactobacillus reuteri 1063 adheres to mucus components. Microbiology 2002, 148, 433-442.
25. MacKenzie, D.A.; Jeffers, F.; Parker, M.L.; Vibert-Vallet, A.; Bongaerts, R.J.; Roos, S.; Walter, J.; Juge, N. Strain-specific diversity of mucus-binding proteins in the adhesion and aggregation properties of Lactobacillus reuteri. Microbiology 2010, 156, 3368-3378.
26. Etzold, S.; Kober, O.I.; MacKenzie, D.A.; Tailford, L.E.; Gunning, P.; Walshaw, J.; Hemmings, A.M.; Juge, N. Structural basis for adaptation of lactobacilli to gastrointestinal mucus. Environ. Microbiol. 2014, 16, 888-903.
27. Lukić, J.; Strahinić, I.; Jovčić, B.; Filipić, B.; Topisirović, L.; Kojić, M.; Begović, J. Different roles for lactococcal aggregation factor and mucin binding protein in adhesion to gastrointestinal mucosa. Appl. Environ. Microbiol. 2012, 78, 7993-8000.
28. Kinoshita, H.; Uchida, H.; Kawai, Y.; Kitazawa, H.; Miura, K.; Shiiba, K.; Horii, A.; Saito, T. Quantitative evaluation of adhesion of lactobacilli isolated from human intestinal tissues to human colonic mucin using surface plasmon resonance (BIACORE assay). J. Appl. Microbiol. 2007, 102, 116-123.
29. Huang, I.N.; Okawara, T.; Watanabe, M.; Kawai, Y.; Kitazawa, H.; Ohnuma, S.; Shibata, C.; Horii, A.; Kimura, K.; Taketomo, N.; et al. New screening methods for probiotics with adhesion properties to sialic acid and sulphate residues in human colonic mucin using the Biacore assay. J. Appl. Microbiol. 2013, 114, 854-860.
30. Nishiyama, K.; Kawanabe, A.; Miyauchi, H.; Abe, F.; Tsubokawa, D.; Ishihara, K.; Yamamoto, Y.; Mukai, T. Evaluation of bifidobacterial adhesion to acidic sugar chains of porcine colonic mucins. Biosci. Biotechnol. Biochem. 2014, 78, 1444-1451.
31. Nishiyama, K.; Nakamata, K.; Ueno, S.; Terao, A.; Aryantini, N.P.; Sujaya, I.N.; Fukuda, K.; Urashima, T.; Yamamoto, Y.; Mukai, T. Adhesion properties of Lactobacillus rhamnosus mucus-binding factor to mucin and extracellular matrix proteins. Biosci. Biotechnol. Biochem. 2015, 79, 271-279.
32. Naughton, J.; Duggan, G.; Bourke, B.; Clyne, M. Interaction of microbes with mucus and mucins: Recent developments. Gut Microbes 2014, 5, 48-52.
33. Jeffers, F.; Fuell, C.; Tailford, L.E.; MacKenzie, D.A.; Bongaerts, R.J.; Juge, N. Mucin-lectin interactions assessed by flow cytometry. Carbohydr. Res. 2010, 345, 1486-1491.
34. Naughton, J.A.; Mariño, K.; Dolan, B.; Reid, C.; Gough, R.; Gallagher, M.E.; Kilcoyne, M.; Gerlach, J.Q.; Joshi, L.; Rudd, P.; et al. Divergent mechanisms of interaction of Helicobacter pylori and Campylobacter jejuni with mucus and mucins. Infect. Immun. 2013, 81, 2838-2850.
35. Lukic, J.; Strahinic, I.; Milenkovi, M.; Nikolic, M.; Tolinacki, M.; Kojic, M.; Begovic, J. Aggregation factor as an inhibitor of bacterial binding to gut mucosa. Microb. Ecol. 2014, 68, 633-644.
36. Altamimi, M.; Abdelhay, O.; Rastall, R.A. Effect of oligosaccharides on the adhesion of gut bacteria to human HT-29 cells. Anaerobe 2016, 39, 136-142.
37. Beaussart, A.; El-Kirat-Chatel, S.; Sullan, R.M.; 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.
38. Hinterdorfer, P.; Gruber, H.J.; Kienberger, F.; Kada, G.; Riener, C.; Broken, C.; Schindler, H. Surface attachment of ligands and receptors for molecular recognition force microscopy. Colloids Surf. 2002, 23, 115-123.
39. Dague, E.; Le, D.T.; Zanna, S.; Marcus, P.; Loubière, P.; Mercier-Bonin, M. Probing in vitro interactions between Lactococcus lactis and mucins using AFM. Langmuir 2010, 26, 11010-11017.
40. Le, D.T.; Tran, T.L.; Duviau, M.P.; Meyrand, M.; Guérardel, Y.; Castelain, M.; Loubière, P.; Chapot-Chartier, M.P.; Dague, E.; Mercier-Bonin, M. Unraveling the role of surface mucus-binding protein and pili in muco-adhesion of Lactococcus lactis. PLoS ONE 2013, 8, e79850.
41. Tripathi, P.; Beaussart, A.; Alsteens, D.; Dupres, V.; Claes, I.; von Ossowski, I.; de Vos, W.M.; Palva, A.; Lebeer, S.; Vanderleyden, J.; et al. Adhesion and nanomechanics of pili from the probiotic Lactobacillus rhamnosus GG. ACS Nano 2013, 7, 3685-3697.
42. Gunning, A.P.; Kirby, A.R.; Fuell, C.; Pin, C.; Tailford, L.E.; Juge, N. Mining the “glycocode”—Exploring the spatial distribution of glycans in gastrointestinal mucin using force spectroscopy. FASEB J. 2013, 27, 2342-2354.
43. Bhatia, S.K.; Shriver-Lake, L.C.; Prior, K.J.; Georger, J.H.; Calvert, J.M.; Bredehorst, R.; Ligler, F.S. Use of thiol terminated silanes and heterobifunctional crosslinkers for immobilisation of antibodies on silica surfaces. Anal. Biochem. 1989, 178, 408-413.
44. Kratky, O.; Porod, G. Röntgenuntersuchung gelöster Fadenmoleküle. Recl. Trav. Chim. 1949, 68, 1106-1122.
45. Flory, P.J.; Volkenstein, M. Statistical mechanics of chain molecules. Biopolymers 1969, 8, 699-700.
46. Beuche, F. Physical Properties of Polymers; Interscience: New York, NY, USA, 1962; p. 354.
47. Smith, S.B.; Cui, Y.; Bustamante, C. Overstretching B-DNA: The elastic response of individual double-stranded and single-stranded DNA molecules. Science 1996, 271, 795-799.
48. Rounsevell, R.; Forman, J.R.; Clarke, J. Atomic Force Microscopy: Mechanical unfolding of proteins. Methods 2004, 34, 100-111.
49. Morris, V.J.; Kirby, A.R.; Gunning, A.P. Atomic Force Microscopy for Biologists, 2nd ed.; Imperial College Press: London, UK, 2009; pp. 384-387.
50. Gunning, A.P.; Pin, C.; Morris, V.J. Galectin 3-β-galactobiose interactions. Carbohydr. Polym. 2013, 92, 529-533.
51. Bresalier, R.S.; Byrd, J.C.; Wang, L.; Raz, A. Colon cancer mucin: A new ligand for the β-galactoside-binding protein galectin-3. Cancer Res. 1996, 56, 4354-4357.
52. Shan, M.; Gentile, M.; Yeiser, J.R.; Walland, A.C.; Bornstein, V.U.; Chen, K.; He, B.; Cassis, L.; Bigas, A.; Cols, M.; et al. Mucus enhances gut homeostasis and oral tolerance by delivering immunoregulatory signals. Science 2013, 342, 447-453.
53. Dumic, J.; Dabelic, S.; Flögel, M. Galectin-3: An open-ended story. Biochim. Biophys. Acta 2006, 1760, 616-635.
54. Boekhorst, J.; Helmer, Q.; Kleerebezem, M.; Siezen, R.J. Comparative analysis of proteins with a mucus-binding domain found exclusively in lactic acid bacteria. Microbiology 2006, 152, 273-280.
55. Gruszka, D.T.; Whelan, F.; Farrance, O.E.; Fung, H.K.H.; Paci, E.; Jeffries, C.M.; Svergun, D.I.; Baldock, C.; Baumann, C.G.; Brockwell, D.J.; et al. Cooperative folding of intrinsically disordered domains drives assembly of a strong elongated protein. Nat. Commun. 2015, 6, 7271.
56. MacKenzie, D.A.; Tailford, L.E.; Hemmings, A.M.; Juge, N. Crystal structure of a mucus-binding protein repeat reveals an unexpected functional immunoglobulin binding activity. J. Biol. Chem. 2009, 284, 32444-32453.
57. Sullan, R.M.; Beaussart, A.; Tripathi, P.; Derclaye, S.; El-Kirat-Chatel, S.; Li, J.K.; Schneider, Y.J.; Vanderleyden, J.; Lebeer, S.; Dufrêne, Y.F. Single-cell force spectroscopy of pili-mediated adhesion. Nanoscale 2014, 6, 1134-1143.
58. Strunz, T.; Oroszlan, K.; Schumakovitch, I.; Güntherodt, H.J.; Hegner, M. Model energy landscapes and the force-induced dissociation of ligand-receptor bonds. Biophys. J. 2000, 79, 1206-1212.
59. El-Kirat-Chatel, S.; Beaussart, A.; Boyd, C.D.; O'Toole, G.A.; Dufrêne, Y.F. Single-cell and single-molecule analysis deciphers the localization, adhesion, and mechanics of the biofilm adhesin LapA. ACS Chem. Biol. 2014, 9, 485-494.
60. Touhami, A.; Hoffmann, B.; Vasella, A.; Denis, F.; Dufrene, Y.F. Probing specific lectin-carbohydrate interactions using atomic force microscopy imaging and force measurements. Langmuir 2003, 19, 1745-1751.
61. Li, H.; Limenitakis, J.P.; Fuhrer, T.; Geuking, M.B.; Lawson, M.A.; Wyss, M.; Brugiroux, S.; Keller, I.; Macpherson, J.A.; Rupp, S.; et al. The outer mucus layer hosts a distinct intestinal microbial niche. Nat. Commun. 2015, 6, 8292.
62. Johansson, M.E.; Phillipson, M.; Petersson, J.; Velcich, A.; Holm, L.; Hansson, G.C. The inner of the two Muc2 mucin-dependent mucus layers in colon is devoid of bacteria. Proc. Natl. Acad. Sci. USA 2008, 105, 15064-15069.
63. Larsson, J.M.; Karlsson, H.; Sjövall, H.; Hansson, G.C. A complex, but uniform O-glycosylation of the human MUC2 mucin from colonic biopsies analyzed by nanoLC/MSn. Glycobiology 2009, 19, 756-766.
64. Crost, E.H.; Tailford, L.E.; Le Gall, G.; Fons, M.; Henrissat, B.; Juge, N. Utilisation of mucin glycans by the human gut symbiont Ruminococcus gnavus is strain-dependent. PLoS ONE 2013, 8, e76341.
65. Hutter, J.L.; Bechhoefer, J. Calibration of atomic force microscope tips. Rev. Sci. Instrum. 1993, 64, 1868-1873.
66. Gunning, A.P.; Chambers, S.; Pin, C.; Man, A.L.; Morris, V.J.; Nicoletti, C. Mapping specific adhesive interactions on living human intestinal epithelial cells with atomic force microscopy. FASEB J. 2008, 22, 2331-2339.