Multistep Fractionation and Mass Spectrometry Reveal Zwitterionic and Anionic Modifications of the N- and O-glycans of a Marine Snail

Ponder, 2008 Volety, 2014, Ecological condition and value of oyster reefs of the Southwest Florida shelf ecosystem, Ecological Indicators, 44, 108, 10.1016/j.ecolind.2014.03.012 Salanki, 2003, Molluscs in biological monitoring of water quality, Toxicol. Lett, 140–141, 403, 10.1016/S0378-4274(03)00036-5 Zuykov, 2013, Bivalve mollusks in metal pollution studies: From bioaccumulation to biomonitoring, Chemosphere, 93, 201, 10.1016/j.chemosphere.2013.05.001 Tian, 2008, Seasonal tracking of histo-blood group antigen expression and norovirus binding in oyster gastrointestinal cells, J. Food Prot, 71, 1696, 10.4315/0362-028X-71.8.1696 Bayne, 2009, Successful parasitism of vector snail Biomphalaria glabrata by the human blood fluke (trematode) Schistosoma mansoni: A 2009 assessment, Mol. Biochem. Parasitol, 165, 8, 10.1016/j.molbiopara.2009.01.005 Geyer, 2005, Identification and characterization of keyhole limpet hemocyanin N-glycans mediating cross-reactivity with Schistosoma mansoni, J. Biol. Chem, 280, 40731, 10.1074/jbc.M505985200 Van Kuik, 1987, Eur. J. Biochem, 169, 399, 10.1111/j.1432-1033.1987.tb13626.x Lommerse, 1997, Primary structure of 21 novel monoantennary and diantennary N- linked carbohydrate chains from aD-hemocyanin of Helix pomatia, Eur. J. Biochem, 249, 195, 10.1111/j.1432-1033.1997.00195.x Siddiqui, 2007, Involvement of glycan chains in the antigenicity of Rapana thomasiana hemocyanin, Biochem. Biophys. Res. Commun, 361, 705, 10.1016/j.bbrc.2007.07.098 Zhang, 1997, A novel monoantennary complex-type sugar chain found in octopus rhodopsin: Occurrence of the Galβ1→4Fuc group linked to the proximal N-acetylglucosamine residue of the trimannosyl core, Glycobiology, 7, 1153, 10.1093/glycob/7.8.1153 Kurz, 2013, Haemocytes and plasma of the eastern oyster (Crassostrea virginica) display a diverse repertoire of sulphated and blood group A-modified N-glycans, J. Biol. Chem, 288, 24410, 10.1074/jbc.M113.478933 Gutternigg, 2007, Neutral N-glycan patterns of the gastropods Limax maximus, Cepaea hortensis, Planorbarius corneus, Arianta arbustorum and Achatina fulica, Glycoconj J, 24, 475, 10.1007/s10719-007-9040-5 Lehr, 2007, Structural characterization of N-glycans from the freshwater snail Biomphalaria glabrata cross-reacting with Schistosoma mansoni glycoconjugates, Glycobiology, 17, 82, 10.1093/glycob/cwl048 Zhou, 2013, Anomalous N-glycan structures with an internal fucose branched to GlcA and GlcN residues isolated from a mollusk shell-forming fluid, J. Proteome. Res, 12, 4547, 10.1021/pr4006734 van Tetering, 1999, Characterization of a core α1→3-fucosyltransferase from the snail Lymnaea stagnalis that is involved in the synthesis of complex-type N-glycans, FEBS Lett, 461, 311, 10.1016/S0014-5793(99)01489-1 Mulder, 1995, In the biosynthesis of N-glycans in connective tissue of the snail Lymnaea stagnalis of incorporation GlcNAc by β2GlcNAc-transferase I is an essential prerequisite for the action of β2GlcNAc-transferase II and β2Xyl-transferase, Eur. J. Biochem, 232, 272, 10.1111/j.1432-1033.1995.tb20809.x Neeleman, 1996, α-Lactalbumin affects the acceptor specificity of Lymnaea stagnalis albumen gland UDP-GalNAc:GlcNAc β-R β1→4-N-acetylgalactosaminyltransferase: Synthesis of GalNAc β1→4Glc, Proc. Natl. Acad. Sci. U.S.A, 93, 10111, 10.1073/pnas.93.19.10111 Bakker, 1994, A Lymnaea stagnalis gene, with sequence similarity to that of mammalian β1→4-galactosyltransferases, encodes a novel UDP-GlcNAc:GlcNAc β-R β1→4-N-acetylglucosaminyltransferase, J. Biol. Chem, 269, 30326, 10.1016/S0021-9258(18)43816-1 Taus, 2013, Expression and characterization of the first snail-derived UDP-N-acetyl-α-D-galactosamine:polypeptide N-acetylgalactosaminyltransferase, Glycoconj J, 30, 825, 10.1007/s10719-013-9486-6 Tretter, 1991, Peptide-N4-(N-acetyl-β-glucosaminyl)asparagine amidase F cannot release glycans with fucose attached α1→3 to the asparagine-linked N-acetylglucosamine residue, Eur. J. Biochem, 199, 647, 10.1111/j.1432-1033.1991.tb16166.x Hykollari, 2013, Mass spectrometric analysis of neutral and anionic N-glycans from a Dictyostelium discoideum model for human congenital disorder of glycosylation CDG IL, J. Proteome. Res, 12, 1173, 10.1021/pr300806b Ali, 2012, Recent trends in ultra-fast HPLC: new generation superficially porous silica columns, J. Sep. Sci, 35, 3235, 10.1002/jssc.201200454 Adams, 1845, Specierum novarum conchyliorum, in Jamaica repertorum, synopsis, Proc. Boston Soc. Natural History, 2, 1 Cossignani, 2006 Rosenberg, 2015 Paschinger, 2012, The N-glycans of Trichomonas vaginalis contain variable core and antennal modifications, Glycobiology, 22, 300, 10.1093/glycob/cwr149 Schulz, 2002, Small-scale analysis of O-linked oligosaccharides from glycoproteins and mucins separated by gel electrophoresis, Anal. Chem, 74, 6088, 10.1021/ac025890a Tomiya, 1987, Structural analysis of N-linked oligosaccharides by a combination of glycopeptidase, exoglycosidases, and high-performance liquid chromatography, Anal. Biochem, 163, 489, 10.1016/0003-2697(87)90253-3 Domon, 1988, A systematic nomenclature for carbohydrate fragmentations in Fab-MS MS spectra of glycoconjugates, Glycoconjugate J, 5, 397, 10.1007/BF01049915 Dragosits, 2014, Recombinant Aspergillus β-galactosidases as a robust glycomic and biotechnological tool, Appl. Microbiol. Biotechnol, 98, 3553, 10.1007/s00253-013-5192-3 Dragosits, 2015, Enzymatic properties and subtle differences in the substrate specificity of phylogenetically distinct invertebrate N-glycan processing hexosaminidases, Glycobiology, 25, 448, 10.1093/glycob/cwu132 Yan, 2015, Comparison of RP-HPLC modes to analyse the N-glycome of the free-living nematode Pristionchus pacificus, Electrophoresis, 36, 1314, 10.1002/elps.201400528 Tomiya, 1991, Calculated two-dimensional sugar map of pyridylaminated oligosaccharides: Elucidation of the jack bean α-mannosidase digestion pathway of Man9GlcNAc2, Anal. Biochem, 193, 90, 10.1016/0003-2697(91)90047-W Tomiya, 1998, Contribution of component monosaccharides to the coordinates of neutral and sialyl pyridylaminated N-glycans on a two- dimensional sugar map, Anal. Biochem, 264, 204, 10.1006/abio.1998.2849 Hykollari, 2014, N-glycomic profiling of a glucosidase II mutant of Dictyostelium discoideum by ‘‘off-line“ liquid chromatography and mass spectrometry, Electrophoresis, 35, 2116 Kurz, 2015, Targetted release and fractionation reveal glucuronylated and sulphated N- and O-glycans in larvae of dipteran insects, J. Proteomics, 126, 172, 10.1016/j.jprot.2015.05.030 Kubelka, 1993, Primary structures of the N-linked carbohydrate chains from honeybee venom phospholipase A2, Eur. J. Biochem, 213, 1193, 10.1111/j.1432-1033.1993.tb17870.x Yan, 2012, Galactosylated fucose epitopes in nematodes: increased expression in a Caenorhabditis mutant associated with altered lectin sensitivity and occurrence in parasitic species, J. Biol. Chem, 287, 28276, 10.1074/jbc.M112.353128 Paschinger, 2005, Fucosyltransferase substrate specificity and the order of fucosylation in invertebrates, Glycobiology, 15, 463, 10.1093/glycob/cwi028 Tomiya, 1988, Analyses of N-linked oligosaccharides using a two-dimensional mapping technique, Anal. Biochem, 171, 73, 10.1016/0003-2697(88)90126-1 Wong-Madden, 1995, Purification and characterization of novel glycosidases from the bacterial genus Xanthomonas, Glycobiology, 5, 19, 10.1093/glycob/5.1.19 Hykollari, 2015, More than just oligomannose: An N-glycomic comparison of Penicillium species, Mol. Cell Proteomics, 1, 73 Harvey, 2005, Fragmentation of negative ions from carbohydrates: Part 3. Fragmentation of hybrid and complex N-linked glycans, J. Am. Soc. Mass Spectrom, 16, 647, 10.1016/j.jasms.2005.01.006 Hayashi, 1989, A new homolog of phosphonoglycosphingolipid, N-methylaminoethylphosphonyltrigalactosylceramide, Biochim. Biophys. Acta, 1006, 89, 10.1016/0005-2760(89)90327-5 Hård, 1993, Structure of the Asn-linked oligosaccharides of apolipophorin III from the insect Locusta migratoria. Carbohydrate- linked 2-aminoethylphosphonate as a constituent of a glycoprotein, Biochemistry, 32, 766, 10.1021/bi00054a005 Gallego, 2001, Epitope diversity of N-glycans from bovine peripheral myelin glycoprotein P0 revealed by mass spectrometry and nano probe magic angle spinning 1H NMR spectroscopy, J. Biol. Chem, 276, 30834, 10.1074/jbc.M101013200 van Kuik, 1987, Primary structure of the acidic carbohydrate chain of hemocyanin from Panulirus interruptus, FEBS Lett, 221, 150, 10.1016/0014-5793(87)80370-8 Paschinger, 2015, Two types of galactosylated fucose motifs are present on N-glycans of Haemonchus contortus, Glycobiology, 25, 585, 10.1093/glycob/cwv015 Schachter, 1982, Biosynthesis of mucus glycoproteins, Adv. Exp. Med. Biol, 144, 3, 10.1007/978-1-4615-9254-9_1 Shao, 2003, O-fucose modifications of epidermal growth factor-like repeats and thrombospondin type 1 repeats: Unusual modifications in unusual places, Cell Mol. Life Sci, 60, 241, 10.1007/s000180300019 Van Kuik, 1986, A 500-MHz 1H-NMR study on the N-linked carbohydrate chain of bromelain, Glycoconjugate J, 3, 27, 10.1007/BF01108609 Yan, 2015, Comparisons of Caenorhabditis fucosyltransferase mutants reveal a multiplicity of isomeric N-glycan structures, J. Proteome Res, 10.1021/acs.jproteome.5b00746 Hanneman, 2006, Isomer and glycomer complexities of core GlcNAcs in Caenorhabditis elegans, Glycobiology, 16, 874, 10.1093/glycob/cwl011 Wuhrer, 2004, A novel Gal(β1–4)Gal(β1–4)Fuc(α1–6)-core modification attached to the proximal N-acetylglucosamine of keyhole limpet haemocyanin (KLH) N-glycans, Biochem. J, 378, 625, 10.1042/bj20031380 Paschinger, 2011, Presence of galactosylated core fucose on N-glycans in the planaria Dugesia japonica, J. Mass Spectrom, 46, 561, 10.1002/jms.1925 Gielens, 2005, Mass spectral evidence for N-glycans with branching on fucose in a molluscan hemocyanin, Biochem. Biophys. Res. Commun, 331, 562, 10.1016/j.bbrc.2005.03.217 Sandra, 2007, New insights in Rapana venosa hemocyanin N-glycosylation resulting from on-line mass spectrometric analyses, Glycobiology, 17, 141, 10.1093/glycob/cwl063 Dolashka, 2010, Glycan structures and antiviral effect of the structural subunit RvH2 of Rapana hemocyanin, Carbohydr. Res, 345, 2361, 10.1016/j.carres.2010.08.005 Satake, 2012, A group of glycosphingolipids found in an invertebrate: Their structures and biological significance, Proc. Japan Acad. Ser. B. Phys. Biolog. Sci, 88, 509, 10.2183/pjab.88.509 Urai, 2009, Structural analysis of O-glycans of mucin from jellyfish (Aurelia aurita) containing 2-aminoethylphosphonate, Carbohydr Res, 344, 2182, 10.1016/j.carres.2009.08.001 Serrano, 1995, The lipid structure of the glycosylphosphatidylinositol-anchored mucin-like sialic acid acceptors of Trypanosoma cruzi changes during parasite differentiation from epimastigotes to infective metacyclic trypomastigote forms, J. Biol. Chem, 270, 27244, 10.1074/jbc.270.45.27244 Paschinger, 2008, The N-glycosylation pattern of Caenorhabditis elegans, Carbohydr Res, 343, 2041, 10.1016/j.carres.2007.12.018 Paschinger, 2012, Mass spectrometric analysis of the immunodominant glycan epitope of Echinococcus granulosus antigen Ag5, Int. J. Parasitol, 42, 279, 10.1016/j.ijpara.2012.01.002 Sugita, 1995, Structural elucidation of two novel amphoteric glycosphingolipids from the earthworm, Pheretima hilgendorfi, Biochim. Biophys. Acta, 1259, 220, 10.1016/0005-2760(95)00168-9 Lysenko, 2000, The position of phosphorylcholine on the lipopolysaccharide of Haemophilus influenzae affects binding and sensitivity to C-reactive protein-mediated killing, Mol. Microbiol, 35, 234, 10.1046/j.1365-2958.2000.01707.x Wuhrer, 2006, Gender-specific expression of complex-type N-glycans in schistosomes, Glycobiology, 16, 991, 10.1093/glycob/cwl020 Moloney, 2000, Fringe is a glycosyltransferase that modifies Notch, Nature, 406, 369, 10.1038/35019000 Aoki, 2008, The diversity of O-linked glycans expressed during Drosophila melanogaster development reflects stage- and tissue-specific requirements for cell signaling, J. Biol. Chem, 283, 30385, 10.1074/jbc.M804925200 Hocking, 2013, Structure of the O-glycosylated conopeptide CcTx from Conus consors venom, Chemistry, 19, 870, 10.1002/chem.201202713 Stepan, 2012, O-Glycosylation of snails, Glycoconjugate J, 29, 189, 10.1007/s10719-012-9391-4 Packer, 1998, A general approach to desalting oligosaccharides released from glycoproteins, Glycoconjugate Journal, 15, 737, 10.1023/A:1006983125913 Chu, 2009, Profile of native N-linked glycan structures from human serum using high performance liquid chromatography on a microfluidic chip and time-of-flight mass spectrometry, Proteomics, 9, 1939, 10.1002/pmic.200800249 Lin, 2014, Facile removal of high mannose structures prior to extracting complex type N-glycans from de-N-glycosylated peptides retained by C18 solid phase to allow more efficient glycomic mapping, Proteomics, 14, 87, 10.1002/pmic.201300343 Morelle, 2005, Galactomannoproteins of Aspergillus fumigatus, Eukaryot. Cell, 4, 1308, 10.1128/EC.4.7.1308-1316.2005 Schneider, 1995, Microscale analysis of glycosylphosphatidylinositol structures, Methods Enzymol, 250, 614, 10.1016/0076-6879(95)50100-2 Haslam, 2000, Structural characterisation of the N-glycans of Dictyocaulus viviparus: discovery of the Lewisx structure in a nematode, Glycobiology, 10, 223, 10.1093/glycob/10.2.223 Adema, 2015, Digenean-gastropod host associations inform on aspects of specific immunity in snails, Dev. Comp. Immunol, 48, 275, 10.1016/j.dci.2014.06.014 Tasumi, 2007, A galectin of unique domain organization from hemocytes of the Eastern oyster (Crassostrea virginica) is a receptor for the protistan parasite Perkinsus marinus, J. Immunol, 179, 3086, 10.4049/jimmunol.179.5.3086 Varki, 2006, Nothing in glycobiology makes sense, except in the light of evolution, Cell, 126, 841, 10.1016/j.cell.2006.08.022