title: Negligible elongation of mucin glycans with Gal β1-3 units distinguishes the laminated layer of Echinococcus multilocularis from that of Echinococcus granulosus.
abstract: The larval stages of the cestodes Echinococcus multilocularis and Echinococcus granulosus cause the important zoonoses known as larval echinococcoses. These larvae are protected by a unique, massive, mucin-based structure known as the laminated layer. The mucin glycans of the E. granulosus laminated layer are core 1- or core 2-based O-glycans in which the core Galpβ1-3 residue can initiate a chain comprising one to three additional Galpβ1-3 residues, a motif not known in mammalian carbohydrates. This chain can be capped with a Galpα1-4 residue, and can be ramified with GlcNAcpβ1-6 residues. These, as well as the GlcNAcpβ1-6 residue in core 2, can be decorated with the Galpα1-4Galpβ1-4 disaccharide. Here we extend our analysis to the laminated layer of E. multilocularis, showing that the non-decorated cores, together with Galpβ1-3(Galpα1-4Galpβ1-4GlcNAcpβ1-6)GalNAc, comprise over 96% of the glycans in molar terms. This simple laminated layer glycome is exhibited by E. multilocularis grown either in vitro or in vivo. Interestingly, all the differences with the complex laminated layer glycome found in E. granulosus may be explained in terms of strongly reduced activity in E. multilocularis of a putative glycosyltransferase catalysing the elongation with Galpβ1-3. Comparative inter-species analysis of available genomic and transcriptomic data suggested a candidate for this enzyme, amongst more than 20 putative (non-core 1) Gal/GlcNAc β1-3 transferases present in each species as a result of a taeniid-specific gene expansion. The candidate gene was experimentally verified to be transcribed at much higher levels in the larva of E. granulosus than that of E. multilocularis.
authors.affiliation: Cátedra de Inmunología, Departamento de Biociencias (Facultad de Química) and Instituto de Química Biológica (Facultad de Ciencias), Universidad de la República, Montevideo, Uruguay.
authors.forename: Lucía
authors.initials: L
authors.lastname: Del Puerto
authors.affiliation: Cátedra de Inmunología, Departamento de Biociencias (Facultad de Química) and Instituto de Química Biológica (Facultad de Ciencias), Universidad de la República, Montevideo, Uruguay.
authors.forename: Romina
authors.initials: R
authors.lastname: Rovetta
authors.affiliation: Cátedra de Inmunología, Departamento de Biociencias (Facultad de Química) and Instituto de Química Biológica (Facultad de Ciencias), Universidad de la República, Montevideo, Uruguay.
authors.forename: Marco
authors.initials: M
authors.lastname: Navatta
authors.affiliation: Departamento de Química del Litoral, CENUR Litoral Norte, Universidad de la República, Paysandú, Uruguay.
authors.forename: Carolina
authors.initials: C
authors.lastname: Fontana
authors.affiliation: Cátedra de Inmunología, Departamento de Biociencias (Facultad de Química) and Instituto de Química Biológica (Facultad de Ciencias), Universidad de la República, Montevideo, Uruguay.
authors.forename: Gerardo
authors.initials: G
authors.lastname: Lin
authors.affiliation: Departamento de Química del Litoral, CENUR Litoral Norte, Universidad de la República, Paysandú, Uruguay.
authors.forename: Guillermo
authors.initials: G
authors.lastname: Moyna
authors.affiliation: Cátedra de Inmunología, Departamento de Biociencias (Facultad de Química) and Instituto de Química Biológica (Facultad de Ciencias), Universidad de la República, Montevideo, Uruguay.
authors.forename: Sylvia
authors.initials: S
authors.lastname: Dematteis
authors.affiliation: University of Würzburg, Institute of Hygiene and Microbiology, Würzburg, Germany.
authors.forename: Klaus
authors.initials: K
authors.lastname: Brehm
authors.affiliation: University of Würzburg, Institute of Hygiene and Microbiology, Würzburg, Germany; Sección Bioquímica, Facultad de Ciencias, Universidad de la República, Montevideo, Uruguay. Electronic address: ukoziol@gmail.com.
authors.forename: Uriel
authors.initials: U
authors.lastname: Koziol
authors.affiliation: Laboratorio de Carbohidratos y Glicoconjugados, DQO de Facultad de Química and DPDB del Instituto de Higiene de la Facultad de Medicina, Universidad de la República, Montevideo, Uruguay.
authors.forename: Fernando
authors.initials: F
authors.lastname: Ferreira
authors.affiliation: Cátedra de Inmunología, Departamento de Biociencias (Facultad de Química) and Instituto de Química Biológica (Facultad de Ciencias), Universidad de la República, Montevideo, Uruguay. Electronic address: adiaz@fq.edu.uy.
authors.forename: Alvaro
authors.initials: A
authors.lastname: Díaz
mesh_terms: D000818:Animals; D002850:Chromatography, Gel; D057225:Data Mining; D048209:Echinococcus granulosus / Q000737:chemistry* / Q000145:classification / Q000235:genetics; D048210:Echinococcus multilocularis / Q000737:chemistry* / Q000145:classification / Q000235:genetics; D015971:Gene Expression Regulation, Enzymologic; D016678:Genome; D005849:Gerbillinae; D016695:Glycosyltransferases / Q000235:genetics / Q000378:metabolism; D007814:Larva / Q000737:chemistry / Q000145:classification; D009682:Magnetic Resonance Spectroscopy; D051379:Mice; D008807:Mice, Inbred BALB C; D009077:Mucins / Q000737:chemistry* / Q000378:metabolism; D010529:Peritoneal Cavity / Q000469:parasitology; D011134:Polysaccharides / Q000096:biosynthesis / Q000737:chemistry* / Q000302:isolation & purification; D020133:Reverse Transcriptase Polymerase Chain Reaction; D019032:Spectrometry, Mass, Matrix-Assisted Laser Desorption-Ionization; D053719:Tandem Mass Spectrometry; D059467:Transcriptome
chemical_list: D009077:Mucins; D011134:Polysaccharides; D016695:Glycosyltransferases
keywords: Carbohydrate; Galactose; Glycosyltransferase; Helminth; Hydatid; Laminated layer; Mucin; O-Glycan