Phylogenetic-Derived Insights Into the Evolution of Sialylation in Eukaryotes

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Phylogenetic-Derived Insights Into the Evolution of Sialylation in Eukaryotes Phylogenetic-Derived Insights into the Evolution of Sialylation in Eukaryotes: Comprehensive Analysis of Vertebrate β-Galactoside α2,3/6-Sialyltransferases (ST3Gal and ST6Gal). Roxana E Teppa, Daniel Petit, Olga Plechakova, Virginie Cogez, Anne Harduin-Lepers To cite this version: Roxana E Teppa, Daniel Petit, Olga Plechakova, Virginie Cogez, Anne Harduin-Lepers. Phylogenetic- Derived Insights into the Evolution of Sialylation in Eukaryotes: Comprehensive Analysis of Vertebrate β-Galactoside α2,3/6-Sialyltransferases (ST3Gal and ST6Gal).. International Journal of Molecular Sciences, MDPI, 2015, 17 (8), 10.3390/ijms17081286. hal-01358174 HAL Id: hal-01358174 https://hal.archives-ouvertes.fr/hal-01358174 Submitted on 28 May 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Distributed under a Creative Commons Attribution| 4.0 International License International Journal of Molecular Sciences Review Phylogenetic-Derived Insights into the Evolution of Sialylation in Eukaryotes: Comprehensive Analysis of Vertebrate β-Galactoside α2,3/6-Sialyltransferases (ST3Gal and ST6Gal) Roxana E. Teppa 1, Daniel Petit 2, Olga Plechakova 3, Virginie Cogez 4 and Anne Harduin-Lepers 4,5,* 1 Bioinformatics Unit, Fundación Instituto Leloir, Av. Patricias Argentinas 435, C1405BWE Buenos Aires, Argentina; [email protected] 2 Laboratoire de Génétique Moléculaire Animale, UMR 1061 INRA, Université de Limoges Faculté des Sciences et Techniques, 123 avenue Albert Thomas, 87060 Limoges, France; [email protected] 3 FRABio-FR3688 CNRS, Univ. Lille, bât. C9, 59655 Villeneuve d’Ascq cedex, France; [email protected] 4 Univ. Lille, CNRS, UMR 8576-UGSF-Unité de Glycobiologie Structurale et Fonctionnelle, 59000 Lille, France; [email protected] 5 UGSF, Bât. C9, Université de Lille-Sciences et Technologies, 59655 Villeneuve d’Ascq, France * Correspondence: [email protected]; Tel.: +33-320-336-246; Fax: +33-320-436-555 Academic Editor: Cheorl-Ho Kim Received: 28 June 2016; Accepted: 28 July 2016; Published: 9 August 2016 Abstract: Cell surface of eukaryotic cells is covered with a wide variety of sialylated molecules involved in diverse biological processes and taking part in cell–cell interactions. Although the physiological relevance of these sialylated glycoconjugates in vertebrates begins to be deciphered, the origin and evolution of the genetic machinery implicated in their biosynthetic pathway are poorly understood. Among the variety of actors involved in the sialylation machinery, sialyltransferases are key enzymes for the biosynthesis of sialylated molecules. This review focus on β-galactoside α2,3/6-sialyltransferases belonging to the ST3Gal and ST6Gal families. We propose here an outline of the evolutionary history of these two major ST families. Comparative genomics, molecular phylogeny and structural bioinformatics provided insights into the functional innovations in sialic acid metabolism and enabled to explore how ST-gene function evolved in vertebrates. Keywords: evolution; sialyltransferases; sialic acid; molecular phylogeny; functional genomics 1. Introduction Sialic acids (SA) represent a broad family of nine-carbon electro-negatively charged monosaccharides commonly described in the deuterostomes and some microorganisms [1–5]. Interestingly, SA show a discontinuous distribution across evolutionary metazoan lineages. Outside the deuterostome lineage (vertebrates, urochordates, echinoderms), SA are rarely described in some ecdysozoa and lophotrochozoa protostomes like in the Drosophila melanogaster nervous system during embryogenesis [6–9] or in larvae of the cicada Philaenus spumarius [10], or on glycolipids of the common squid and pacific octopus [11]. They are notably absent from plants, archaebacteria or the ecdysozoan Caenorhabditis elegans [12]. SA exhibit a huge structural diversity and species specific modifications. This family of compounds encompasses N-acetylneuraminic acid (Neu5Ac) and over 50 derivatives showing various substituents on carbon 4, 5, 7, 8 or 9, like Neu5Gc and Kdn, with Neu5Ac being the most prominent SA found in higher vertebrates (Figure1A). In vertebrates, the SA hydroxyl group at position 2 is most frequently glycosidically-linked to either the 3- or 6-hydroxyl group of galactose (Gal) residues (Figure1B) or the 6-hydroxyl group of N-acetylgalactosamine (GalNAc) residues and Int. J. Mol. Sci. 2016, 17, 1286; doi:10.3390/ijms17081286 www.mdpi.com/journal/ijms Int. J. Mol.Int. J. Sci. Mol.2016 Sci. ,201617,, 1286 17, 1286 2 of 202 of 20 hydroxyl group at position 2 is most frequently glycosidically-linked to either the 3- or 6-hydroxyl can formgroup to of a lessergalactose extent (Gal) di-, residues oligo- or(Fig poly-SAure 1B) or chains the 6-hydroxyl via their 8-hydroxyl group of N group.-acetylgalactosamine In deuterostome lineages,(GalNAc) sialoglycans residues and are foundcan form in to cellular a lesser secretionsextent di-, oligo- and onor poly-SA the outer chains cell via surface, their 8-hydroxyl essentially as group. In deuterostome lineages, sialoglycans are found in cellular secretions and on the outer cell terminal residues of the glycan chains of glycoproteins and glycolipids [13,14] constituting the so-called surface, essentially as terminal residues of the glycan chains of glycoproteins and glycolipids [13,14] siaLome [15], which varies according to animal species. constituting the so-called siaLome [15], which varies according to animal species. Figure 1. Sialic acids and sialylated molecules. (A) N-acetylneuraminic acid (Neu5Ac) is the major Figure 1. Sialic acids and sialylated molecules. (A) N-acetylneuraminic acid (Neu5Ac) is the major sialic acid molecule found in human tissues. Other commonly described sialic acids in vertebrates are sialicN acid-glycolylneuraminic molecule found acid in human (Neu5Gc) tissues. and 2-keto-3-deoxy-nonulosonic Other commonly described acid sialic (Kdn); acids (B) In in vertebrates, vertebrates are N-glycolylneuraminicthe sialic acid hydroxyl acid group (Neu5Gc) at position and 2-keto-3-deoxy-nonulosonic 2 is most frequently glycosidically-linked acid (Kdn); to (B either) In vertebrates, the 3- the sialicor 6-hydroxyl acid hydroxyl group group of galactose at position (Gal) 2 isresidues. most frequently These glycosidic glycosidically-linked linkages are formed to either by thethe 3- or 6-hydroxylβ-galactoside group ofα2,3/6-sialyltransferases galactose (Gal) residues. described These in glycosidic this review. linkages are formed by the β-galactoside α2,3/6-sialyltransferases described in this review. Owing to their anionic charge and their peripheral position in glycans, SA play major roles in the various vertebrate biological systems ranging from protecting proteins from proteolysis, Owing to their anionic charge and their peripheral position in glycans, SA play major roles modulating cell functions to regulating intracellular communication [16]. For instance, the in theα2,3-linked various vertebrateSA contribute biological to the high systems viscosity ranging of the mucin-type from protecting O-glycosylproteins proteins fromfound proteolysis, on the modulatingintestine cell endothelia functions orto on regulating the surface intracellular of fish or frog communication eggs [17]. Besides, [16 ].some For instance,endogenous the proteinsα2,3-linked SA contributespecificallyto recognize the high sialylated viscosity molecules of the at mucin-type the cell surfaceO-glycosylproteins that act as receptors. found Examples on the include intestine endotheliaselectin or on on endothelial the surface cells of mediating fish or frog leucocytes eggs [17 and]. Besides, platelets sometrafficking, endogenous and siglecs proteins playing specifically a role recognizein immune sialylated cell regulation molecules [18,19]. at the cellLikewise, surface a number that act of as pathogenic receptors. Examplesagents like includetoxins (cholera selectin on endothelialtoxin), protozoa cells mediating (Plasmodium), leucocytes viruses and (influenza platelets virus), trafficking, bacteria and (Helicobacter siglecs playing pylori) use a rolecell surface in immune cell regulationSA as ligands [18 ,for19]. cell Likewise, adhesion a [20] number and have of pathogenic evolved this agents ability liketo distinguish toxins (cholera a specific toxin), sialylated protozoa (Plasmodium),sugar code viruses[21,22] distinguishing (influenza virus), α2,3- bacteriaor α2,6-linked (Helicobacter SA in vertebrate pylori) use tissues cell surface[23]. One SA of asthe ligands most for notable examples is the flu virus tropism: human strains of influenza A virus bind selectively to cell adhesion [20] and have evolved this ability to distinguish a specific sialylated sugar code [21,22] SAα2,6-Gal epitopes that prevail in the human tracheal mucosal epithelium, whereas chimpanzee α α distinguishingstrains bind 2,3-selectively or 2,6-linked to SAα2,3-Gal SA in vertebrateepitopes primarily tissues [expressed23]. One ofin thetheir most tracheal notable mucosal examples is theepithelium
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