Use of Atomic Force Microscopy to Study the Multi-Modular Interaction of Bacterial Adhesins to Mucins

The mucus layer covering the gastrointestinal (GI) epithelium is critical in selecting and maintaining homeostatic interactions with our gut bacteria. However, the molecular details of these interactions are not well understood. Here, we provide mechanistic insights into the adhesion properties of t...

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Published in:	International journal of molecular sciences Vol. 17; no. 11; p. 1854
Main Authors:	Gunning, A., Kavanaugh, Devon, Thursby, Elizabeth, Etzold, Sabrina, MacKenzie, Donald, Juge, Nathalie
Format:	Journal Article
Language:	English
Published:	Switzerland MDPI AG 08.11.2016 MDPI
Subjects:	Adhesins, Bacterial - chemistry Adhesins, Bacterial - isolation & purification Adhesins, Bacterial - metabolism Animals Bacteria Bacterial Adhesion Binding sites Cell adhesion & migration Culture Media, Conditioned - chemistry Galectin 3 - chemistry Galectin 3 - genetics Galectin 3 - metabolism Gene Expression Humans Intestinal Mucosa - chemistry Lactobacillus Limosilactobacillus reuteri - growth & development Limosilactobacillus reuteri - metabolism Microscopy Microscopy, Atomic Force Models, Molecular Mucin-3 - chemistry Mucin-3 - isolation & purification Mucin-3 - metabolism Protein Binding Proteins Recombinant Proteins - chemistry Recombinant Proteins - genetics Recombinant Proteins - metabolism Swine intestinal mucin Lactobacillus reuteri single molecule force spectroscopy bacterial adhesins mucus binding protein atomic force microscopy gut microbiota
ISSN:	1422-0067, 1661-6596, 1422-0067
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Abstract	The mucus layer covering the gastrointestinal (GI) epithelium is critical in selecting and maintaining homeostatic interactions with our gut bacteria. However, the molecular details of these interactions are not well understood. Here, we provide mechanistic insights into the adhesion properties of the canonical mucus-binding protein (MUB), a large multi-repeat cell–surface adhesin found in Lactobacillus inhabiting the GI tract. We used atomic force microscopy to unravel the mechanism driving MUB-mediated adhesion to mucins. Using single-molecule force spectroscopy we showed that MUB displayed remarkable adhesive properties favouring a nanospring-like adhesion model between MUB and mucin mediated by unfolding of the multiple repeats constituting the adhesin. We obtained direct evidence for MUB self-interaction; MUB–MUB followed a similar binding pattern, confirming that MUB modular structure mediated such mechanism. This was in marked contrast with the mucin adhesion behaviour presented by Galectin-3 (Gal-3), a mammalian lectin characterised by a single carbohydrate binding domain (CRD). The binding mechanisms reported here perfectly match the particular structural organization of MUB, which maximizes interactions with the mucin glycan receptors through its long and linear multi-repeat structure, potentiating the retention of bacteria within the outer mucus layer.
AbstractList	The mucus layer covering the gastrointestinal (GI) epithelium is critical in selecting and maintaining homeostatic interactions with our gut bacteria. However, the molecular details of these interactions are not well understood. Here, we provide mechanistic insights into the adhesion properties of the canonical mucus-binding protein (MUB), a large multi-repeat cell–surface adhesin found in Lactobacillus inhabiting the GI tract. We used atomic force microscopy to unravel the mechanism driving MUB-mediated adhesion to mucins. Using single-molecule force spectroscopy we showed that MUB displayed remarkable adhesive properties favouring a nanospring-like adhesion model between MUB and mucin mediated by unfolding of the multiple repeats constituting the adhesin. We obtained direct evidence for MUB self-interaction; MUB–MUB followed a similar binding pattern, confirming that MUB modular structure mediated such mechanism. This was in marked contrast with the mucin adhesion behaviour presented by Galectin-3 (Gal-3), a mammalian lectin characterised by a single carbohydrate binding domain (CRD). The binding mechanisms reported here perfectly match the particular structural organization of MUB, which maximizes interactions with the mucin glycan receptors through its long and linear multi-repeat structure, potentiating the retention of bacteria within the outer mucus layer. The mucus layer covering the gastrointestinal (GI) epithelium is critical in selecting and maintaining homeostatic interactions with our gut bacteria. However, the molecular details of these interactions are not well understood. Here, we provide mechanistic insights into the adhesion properties of the canonical mucus-binding protein (MUB), a large multi-repeat cell-surface adhesin found in inhabiting the GI tract. We used atomic force microscopy to unravel the mechanism driving MUB-mediated adhesion to mucins. Using single-molecule force spectroscopy we showed that MUB displayed remarkable adhesive properties favouring a nanospring-like adhesion model between MUB and mucin mediated by unfolding of the multiple repeats constituting the adhesin. We obtained direct evidence for MUB self-interaction; MUB-MUB followed a similar binding pattern, confirming that MUB modular structure mediated such mechanism. This was in marked contrast with the mucin adhesion behaviour presented by Galectin-3 (Gal-3), a mammalian lectin characterised by a single carbohydrate binding domain (CRD). The binding mechanisms reported here perfectly match the particular structural organization of MUB, which maximizes interactions with the mucin glycan receptors through its long and linear multi-repeat structure, potentiating the retention of bacteria within the outer mucus layer. The mucus layer covering the gastrointestinal (GI) epithelium is critical in selecting and maintaining homeostatic interactions with our gut bacteria. However, the molecular details of these interactions are not well understood. Here, we provide mechanistic insights into the adhesion properties of the canonical mucus-binding protein (MUB), a large multi-repeat cell-surface adhesin found in Lactobacillus inhabiting the GI tract. We used atomic force microscopy to unravel the mechanism driving MUB-mediated adhesion to mucins. Using single-molecule force spectroscopy we showed that MUB displayed remarkable adhesive properties favouring a nanospring-like adhesion model between MUB and mucin mediated by unfolding of the multiple repeats constituting the adhesin. We obtained direct evidence for MUB self-interaction; MUB-MUB followed a similar binding pattern, confirming that MUB modular structure mediated such mechanism. This was in marked contrast with the mucin adhesion behaviour presented by Galectin-3 (Gal-3), a mammalian lectin characterised by a single carbohydrate binding domain (CRD). The binding mechanisms reported here perfectly match the particular structural organization of MUB, which maximizes interactions with the mucin glycan receptors through its long and linear multi-repeat structure, potentiating the retention of bacteria within the outer mucus layer.The mucus layer covering the gastrointestinal (GI) epithelium is critical in selecting and maintaining homeostatic interactions with our gut bacteria. However, the molecular details of these interactions are not well understood. Here, we provide mechanistic insights into the adhesion properties of the canonical mucus-binding protein (MUB), a large multi-repeat cell-surface adhesin found in Lactobacillus inhabiting the GI tract. We used atomic force microscopy to unravel the mechanism driving MUB-mediated adhesion to mucins. Using single-molecule force spectroscopy we showed that MUB displayed remarkable adhesive properties favouring a nanospring-like adhesion model between MUB and mucin mediated by unfolding of the multiple repeats constituting the adhesin. We obtained direct evidence for MUB self-interaction; MUB-MUB followed a similar binding pattern, confirming that MUB modular structure mediated such mechanism. This was in marked contrast with the mucin adhesion behaviour presented by Galectin-3 (Gal-3), a mammalian lectin characterised by a single carbohydrate binding domain (CRD). The binding mechanisms reported here perfectly match the particular structural organization of MUB, which maximizes interactions with the mucin glycan receptors through its long and linear multi-repeat structure, potentiating the retention of bacteria within the outer mucus layer.
Author	Thursby, Elizabeth Etzold, Sabrina Juge, Nathalie MacKenzie, Donald Kavanaugh, Devon Gunning, A.
AuthorAffiliation	2 Division of Neonatology and Division of Gastroenterology, Hepatology and Nutrition, Department of Pediatrics, School of Medicine, University of California San Diego, 9500 Gilman Drive, San Diego, CA 92093-0715, USA 1 The Gut Health and Food Safety Institute Strategic Programme, Institute of Food Research, Norwich Research Park, Norwich NR4 7UA, UK; Devon.Kavanaugh@ifr.ac.uk (D.K.); Elizabeth.Thursby@ifr.ac.uk (E.T.); sabrinaetzold1@gmail.com (S.E.); d.mackenzie91@btinternet.com (D.A.M.)
AuthorAffiliation_xml	– name: 1 The Gut Health and Food Safety Institute Strategic Programme, Institute of Food Research, Norwich Research Park, Norwich NR4 7UA, UK; Devon.Kavanaugh@ifr.ac.uk (D.K.); Elizabeth.Thursby@ifr.ac.uk (E.T.); sabrinaetzold1@gmail.com (S.E.); d.mackenzie91@btinternet.com (D.A.M.) – name: 2 Division of Neonatology and Division of Gastroenterology, Hepatology and Nutrition, Department of Pediatrics, School of Medicine, University of California San Diego, 9500 Gilman Drive, San Diego, CA 92093-0715, USA
Author_xml	– sequence: 1 givenname: A. surname: Gunning fullname: Gunning, A. – sequence: 2 givenname: Devon surname: Kavanaugh fullname: Kavanaugh, Devon – sequence: 3 givenname: Elizabeth surname: Thursby fullname: Thursby, Elizabeth – sequence: 4 givenname: Sabrina surname: Etzold fullname: Etzold, Sabrina – sequence: 5 givenname: Donald surname: MacKenzie fullname: MacKenzie, Donald – sequence: 6 givenname: Nathalie surname: Juge fullname: Juge, Nathalie
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Keywords	intestinal mucin Lactobacillus reuteri single molecule force spectroscopy bacterial adhesins mucus binding protein atomic force microscopy gut microbiota
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Commun. doi: 10.1038/ncomms9292
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Snippet	The mucus layer covering the gastrointestinal (GI) epithelium is critical in selecting and maintaining homeostatic interactions with our gut bacteria. However,...
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SubjectTerms	Adhesins, Bacterial - chemistry Adhesins, Bacterial - isolation & purification Adhesins, Bacterial - metabolism Animals Bacteria Bacterial Adhesion Binding sites Cell adhesion & migration Culture Media, Conditioned - chemistry Galectin 3 - chemistry Galectin 3 - genetics Galectin 3 - metabolism Gene Expression Humans Intestinal Mucosa - chemistry Lactobacillus Limosilactobacillus reuteri - growth & development Limosilactobacillus reuteri - metabolism Microscopy Microscopy, Atomic Force Models, Molecular Mucin-3 - chemistry Mucin-3 - isolation & purification Mucin-3 - metabolism Protein Binding Proteins Recombinant Proteins - chemistry Recombinant Proteins - genetics Recombinant Proteins - metabolism Swine
Title	Use of Atomic Force Microscopy to Study the Multi-Modular Interaction of Bacterial Adhesins to Mucins
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