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Characterization of a Novel Rhamnose-Containing Acidic Journal of Oleo Science Copyright ©2017 by Japan Oil Chemists’ Society doi : 10.5650/jos.ess16150 J. Oleo Sci. 66, (3) 285-295 (2017) Characterization of a Novel Rhamnose-containing Acidic Glycosphingolipid from the Ascidian Halocynthia aurantium Hisao Kojima1,† , Ryota Shinohara1, 2,† , Saki Itonori3 and Masahiro Ito1,＊ 1 Department of Bioinformatics, College of Life Sciences, Ritsumeikan University, 1-1-1 Nojihigashi, Kusatsu, Shiga 525-8577, JAPAN 2 Division of Pharmacology, Graduate School of Medicine, Kobe University, 7-5-1 Kusunoki-cho, Chuo-ku, Kobe 650-0017, JAPAN 3 Department of Chemistry, Faculty of Liberal Arts and Education, Shiga University, 2-5-1 Hiratsu, Otsu, Shiga 520-0862, JAPAN † These authors contributed equally to this work Abstract: Halocynthia aurantium, an edible ascidian species belonging to Urochordata, was subjected to structural characterization of acidic glycosphingolipids to investigate these molecules in ascidians: sulfatide from Ciona intestinalis and the glucuronic acid-containing acidic glycosphingolipid from H. roretzi. Acidic glycosphingolipids containing three or five sugars were isolated from soft parts of the ascidian H. aurantium by chloroform–methanol extraction, mild-alkaline hydrolysis, precipitation with cold acetone, and subsequent column chromatography using a DEAE-Sephadex A-25 column, a Florisil column, and an Iatrobead column. The structures of these glycosphingolipids were determined by methylation studies, sugar analysis, fatty acid analysis, sphingoid analysis, mass spectrometry, and proton nuclear magnetic resonance spectroscopy. A novel glucuronic acid-containing glycosphingolipid having a rhamnose residue was identified as Rhaα1-3GlcNAcβ1-3Galβ1-4(Fucα1-3)GlcAβ1-Cer (UGL-2). This novel structure is particularly unusual given that it contains both a rhamnose residue and a reducing terminal glucuronic acid residue within a single molecule. Rhamnose is a characteristic sugar, which is a component of cell wall pectin in plants and exopolysaccharides in bacteria. Ascidians acquired the cellulose synthase gene via lateral gene transfer, and therefore, it can be speculated that they also acquired the rhamnosyltransferase gene in the same manner. We also detected Galβ1-4(Fucα1-3)GlcAβ1-Cer (UGL-1), which was already identified in another ascidian, H. roretzi. Key words: acidic glycosphingolipid, glucuronic acid, rhamnose, structural characterization, ascidian 1 INTRODUCTION fact, dominant acidic GSLs in flies（Arthropoda）belong to Glycosphingolipids（GSLs）are expressed on the outer the glucuronic acid-containing type; the ones in Nematoda surface of the plasma membrane, forming a microdomain （genus Ascaris）belong to both the inositol phosphate and and playing a role in several types of signal transduction1）. sulfatide types; the ones in a brackish water lugworm in GSLs comprise a sugar chain and an aliphatic portion com- Annelida belong to the inositol phosphate types4）; and the posed of an amide-bonded fatty acid and a sphingoid. They are largely divided into two groups: neutral and acidic Abbreviations: GSL, glycosphingolipid; GC, gas–liquid types. Acidic GSLs are grouped into four types: sialic acid- chromatography; MALDI-TOF MS, matrix-assisted laser containing GSLs（gangliosides）, sulfuric-substituted GSLs desorption/ionization time-of-flight mass spectrometry; 1 （sulfatides）, inositol phosphate-containing GSLs, and H-NMR, proton nuclear magnetic resonance; UGL, uronic acid-containing glycosphingolipid; TLC, thin-layer uronic acid-containing GSLs（UGLs）. chromatography; HPTLC, high-performance thin-layer In phylogenetic analyses of acidic GSLs, gangliosides chromatography; LPS, lipopolysaccharide; Rha, rhamnose; have been found to be the dominant type in vertebrates Man, mannose; Glc, glucose; GlcA, glucuronic acid; GlcN, and echinodermata, but only a few reports on the existence glucosamine; GlcNAc, N-acetylglucosamine; Fuc, fucose; Gal, of gangliosides in protostomes have been published2, 3）. In galactose; Xyl, xylose; Cer, ceramide ＊Correspondence to: Masahiro Ito, Department of Bioinformatics, College of Life Sciences, Ritsumeikan University, 1-1-1 Nojihigashi, Kusatsu, Shiga 525-8577, JAPAN E-mail: [email protected] Accepted September 29, 2016 (received for review July 28, 2016) Journal of Oleo Science ISSN 1345-8957 print / ISSN 1347-3352 online http://www.jstage.jst.go.jp/browse/jos/ http://mc.manusriptcentral.com/jjocs 285 H. Kojima, R. Shinohara and S. Itonori et al. ones in the bivalves Hyriopsis schlegelii5） and Meretrix Therefore, sulfated GSLs in C. intestinalis are rare in lusoria6） belong to the methylated glucuronic acid type. In terms of sulfate group-substituted galactose at the C6 posi- the bivalve H. schlegelii, a methylated glucuronic acid- tion. We also investigated acidic GSLs in the ascidian H. type acidic GSL was shown to be present on the surface of roretzi and characterized a novel UGL［Galβ1-4（Fucα1-3） the sperm, indicating its involvement in fertilization7）. GlcAβ1-1Cer; UGL-1］within this species20）. USLs were Rhamnose is a type of methyl-pentose corresponding to characterized from bivalves as GlcA4Meβ1-4（GalNAc- deoxy-mannose. It is widely distributed as a component of 3Meα1-3）Fucα1-4GlcNAcβ1-2Manα1-3（Xylβ1-2）Manβ1- bacterial exopolysaccharides8）. Plants exhibit rhamnose- 4Glcβ1-Cer）, from the fly Calliphora vicina as GlcAβ1- containing pectins composed of a repeated galacturonic 3Galβ1-3GalNAcβ1-4GlcNAcβ1-3Manβ1-4Glcβ1-Cer, and acid-rhamnose（Rha）backbone or a poly-galactose back- from the fly Lucilia caesar as GlcAβ1-3Galβ1-3GalNAcα1- bone attached to Rha, forming a matrix surrounding cellu- 4GalNAcβ1-4GlcNAcβ1-3Manβ1-4Glcβ1-Cer4）. UGLs other lose microfibrils with hemicellulose and proteins on the than H. roretzi contain a glucuronic acid residue at the primary cell wall9）. An inositol phosphate-containing rham- non-reducing terminus, whereas the H. roretzi UGL con- nolipid was identified in the protozoan Leptomonas tains one at the reducing terminus with an attached samueli: Xylβ1-4Xylβ1-4（Rhaα1-3）Manα1-2Manα1-3 branching fucose. Hence, the H. roretzi UGL is also （aminoethylphosphate-6）Manα1-3Manα1-4（aminoeth- unusual in terms of position on the sugar chain and pres- 10） ylphosphate-6）GlcNα1-6Ins（1/2）-PO4-Cer ; moreover, a ence of a branching fucose. In both ascidians, we could not neutral rhamno-GSL was identified in the marine sponge detect any ganglioside despite our expectations. We further Agelas clathrodes: Rhaα1-3GalNAcβ1-6Galα1-2Galα1- conducted genome-wide analyses by phylogenetic profiling Cer11）. These are the only published reports on rhamno- of glycosyltransferases to confirm that ascidians had actu- GSLs. ally lost sialyltransferases21）. Given that genome sequences Ascidians are largely divided into three orders on the were analyzed only for the Ciona species（C. intestinalis basis of their branchial sac in adults: Aplousobranchia, and C. savignyi）, we could not investigate other species. Phlebobranchia, and Stolidobranchia. Their habitats are We confirmed that these ascidians belonging to the genus widely distributed in the sea from the equator to the Arctic Ciona had lost majority sialyltransferases. Based on these and Antarctic12）. Over 3000 ascidian species have been results, we investigated acidic GSLs in the ascidian H. au- identified. Ascidians commonly possess a notochord in rantium for the presence of gangliosides. their larval stage13）, and are therefore classified as chor- In the present study, we extracted and characterized dates, close to vertebrates. Ascidians belong to Urochorda- acidic GSLs from H. aurantium; we found UGL-1 and a ta; therefore, they are closer to mammals than lancelets novel rhamnose-containing UGL, which were speculated to （Cephalochordata）, as determined by comparative genome be elongated via UGL-1. The presence of a rhamnose-con- analyses14）. Notably, in animals, urochordates, including taining GSL in H. aurantium is interesting, given that few Ascidians, have been proven to produce cellulose15）. The examples of such GSLs have been reported10, 11）. gene that enables cellulose production was identified in as- cidians16） and shown to have been acquired from bacteria via lateral gene transfer17）. We conducted a structural characterization of acidic 2 EXPERIMENTAL PROCEDURES GSLs with the expectation of discovering gangliosides con- 2.1 Isolation of acidic GSLs sidering that deuterostomes such as echinoderms and ver- Fifty individuals（wet weight 4.5 kg）of the ascidian H. tebrates contain gangliosides. Among acidic GSLs in Uro- aurantium, purchased from the company Nishikiya Saito chordata, we reported a sulfated GSL（HSO3-6GlcCer）in （2-19-5 Akaiwa, Otaru, Japan）, were boiled and the encyst- the ascidian Ciona intestinalis18）. The most well-known ment was removed. The remaining materials were dehy- sulfated GSL is sulfatide, a sulfate group-substituted galac- drated using acetone, dried, and pulverized in a blender. tose at the C3 position（HSO3-3Galβ1-Cer）. Other sulfated Acidic GSLs were isolated and purified as described previ- GSLs are common in sulfate group-substituted sugar resi- ously20）. In brief, they were extracted twice with chloro- dues at the C3 position, except for types of sulfate group- form/methanol（C/M）2:1（v/v）, extracted once with C/M 1:1, substituted N-acetyl/glycolyl neuramic acid at the C8 posi- and evaporated to dryness. To remove glycerolipids, the tion19）. In protostomes, sulfated GSLs have been residues were treated with mild-alkaline hydrolysis and characterized as
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