Fucose-binding Lectin from Opportunistic Pathogen Burkholderia ambifaria Binds to Both Plant and Human Oligosaccharidic Epitopes

• Type of Material: Article
• Authors: Aymeric Audfray, Université Joseph Fourier and Institut de Chimie Moléculaire de Grenoble; Julie Claudinon, Albert Ludwigs University Freiburg; Saida Abounit, Institut Curie; Nathalie Ruvoen-Clouet, University of Nantes; Goran Larson, Sahlgrenska University Hospital; David Smith, Emory University; Michaela Wimmerova, Masaryk Univ; Jacques Le Pendu, University of Nantes; Winfried Roemer, University of Freiburg; Annabelle Varrot, Université Joseph Fourier and Institut de Chimie Moléculaire de Grenoble; Anne Imberty, Université Joseph Fourier and Institut de Chimie Moléculaire de Grenoble
• Language: English
• Date: 2012-02-03
• Publisher: American Society for Biochemistry and Molecular Biology
• Publication Version: Final Published Version
• Copyright Statement: © 2012 by The American Society for Biochemistry and Molecular Biology, Inc.
• Final Published Version (URL): http://dx.doi.org/10.1074/jbc.M111.314831
• Title of Journal or Parent Work: Journal of Biological Chemistry
• Volume: 287
• Issue: 6
• Start Page: 4335
• End Page: 4347
• Grant/Funding Information: This work was supported by CNRS-INSERM, the German Excellence Initiative of the Deutsche Forschungsgemeinschaft, and the Association Vaincre la Mucoviscidose.; This work was also supported by Agence Nationale de la Recherche Grants NeoLect 11-BSV5-002-01 (to A. I., W. R., and J. L. P.) and GlycanClust (to W. R.) and by grants from the Czech Science Foundation (GA303/09/1168) and the CEITEC-Central European Institute of Technology (CZ.1.05/1.1.00/02.0068) from the European Regional Development Fund (to M. W.)
• Keywords: CEPACIA COMPLEX; SP-NOV.; SPECIFICITY; DIVERSITY; GLYCOSYLATION; MOLECULAR-BASIS; PSEUDOMONAS-AERUGINOSA; Biochemistry & Molecular Biology; INFECTION; RECOGNITION; Science & Technology; Life Sciences & Biomedicine; POLYMORPHISM
• Research Categories: Chemistry, Biochemistry; Biology, Molecular

Abstract

Burkholderia ambifaria is generally associated with the rhizosphere of plants where it has biocontrol effects on other microorganisms. It is also a member of the Burkholderia cepacia complex, a group of closely related bacteria that cause lung infections in immunocompromised patients as well as in patients with granulomatous disease or cystic fibrosis. Our previous work indicated that fucose on human epithelia is a frequent target for lectins and adhesins of lung pathogens (Sulák, O., Cioci, G., Lameignére, E., Balloy, V., Round, A., Gutsche, I., Malinovská, L., Chignard, M., Kosma, P., Aubert, D. F., Marolda, C. L., Valvano, M. A., Wimmerová, M., and Imberty, A. (2011) PLoS Pathog. 7, e1002238). Analysis of the B. ambifaria genome identified BambL as a putative fucose-binding lectin. The 87- amino acid protein was produced recombinantly and demonstrated to bind to fucosylated oligosaccharides with a preference for αFuc1-2Gal epitopes. Crystal structures revealed that it associates as a trimer with two fucose-binding sites per monomer. The overall fold is a six-bladed β-propeller formed by oligomerization as in the Ralstonia solanacearum lectin and not by sequential domains like the fungal fucose lectin from Aleuria aurantia. The affinity of BambL for small fucosylated glycans is very high as demonstrated by microcalorimetry (K D < 1 μM). Plant cell wall oligosaccharides and human histo-blood group oligosaccharides H-type 2 and Lewis Y are bound with equivalent efficiency. Binding to artificial glycosphingolipid-containing vesicles, human saliva, and lung tissues confirmed that BambL could recognize a wide spectrum of fucosylated epitopes, albeit with a lower affinity for biological material from nonsecretor individuals.