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A Lectin from the Mussel Mytilus galloprovincialis Has a Highly Novel Primary Structure and Induces Glycan-mediated Cytotoxicity of Globotriaosylceramide-expressing Lymphoma Cells*

  • Yuki Fujii
    Footnotes
    Affiliations
    Laboratory of Glycobiology and Marine Biochemistry, Department of Life and Environmental System Science, Graduate School of NanoBio Sciences, Yokohama City University, 22-2 Seto, Kanazawa-ku, Yokohama 236-0027, Japan

    Divisions of Functional Morphology and Microbiology, Department of Pharmacy, Faculty of Pharmaceutical Science, Nagasaki International University, 2825-7 Huis Ten Bosch, Sasebo, Nagasaki 859-3298, Japan
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  • Naoshi Dohmae
    Footnotes
    Affiliations
    Biomolecular Characterization Team, RIKEN Advanced Science Institute, Saitama 351-0198, Japan
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  • Koji Takio
    Affiliations
    Biomolecular Characterization Team, RIKEN Advanced Science Institute, Saitama 351-0198, Japan
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  • Sarkar M.A. Kawsar
    Affiliations
    Laboratory of Glycobiology and Marine Biochemistry, Department of Life and Environmental System Science, Graduate School of NanoBio Sciences, Yokohama City University, 22-2 Seto, Kanazawa-ku, Yokohama 236-0027, Japan

    Laboratory of Carbohydrate and Protein Chemistry, Department of Chemistry, Faculty of Science, University of Chittagong, Chittagong-4331, Bangladesh
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  • Ryo Matsumoto
    Affiliations
    Laboratory of Glycobiology and Marine Biochemistry, Department of Life and Environmental System Science, Graduate School of NanoBio Sciences, Yokohama City University, 22-2 Seto, Kanazawa-ku, Yokohama 236-0027, Japan
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  • Imtiaj Hasan
    Affiliations
    Laboratory of Glycobiology and Marine Biochemistry, Department of Life and Environmental System Science, Graduate School of NanoBio Sciences, Yokohama City University, 22-2 Seto, Kanazawa-ku, Yokohama 236-0027, Japan

    Department of Biochemistry and Molecular Biology, Faculty of Science, Rajshahi University, Rajshahi-6205, Bangladesh
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  • Yasuhiro Koide
    Affiliations
    Laboratory of Glycobiology and Marine Biochemistry, Department of Life and Environmental System Science, Graduate School of NanoBio Sciences, Yokohama City University, 22-2 Seto, Kanazawa-ku, Yokohama 236-0027, Japan
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  • Robert A. Kanaly
    Affiliations
    Laboratory of Glycobiology and Marine Biochemistry, Department of Life and Environmental System Science, Graduate School of NanoBio Sciences, Yokohama City University, 22-2 Seto, Kanazawa-ku, Yokohama 236-0027, Japan
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  • Hidetaro Yasumitsu
    Affiliations
    Laboratory of Glycobiology and Marine Biochemistry, Department of Life and Environmental System Science, Graduate School of NanoBio Sciences, Yokohama City University, 22-2 Seto, Kanazawa-ku, Yokohama 236-0027, Japan
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  • Yukiko Ogawa
    Affiliations
    Divisions of Functional Morphology and Microbiology, Department of Pharmacy, Faculty of Pharmaceutical Science, Nagasaki International University, 2825-7 Huis Ten Bosch, Sasebo, Nagasaki 859-3298, Japan
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  • Shigeki Sugawara
    Affiliations
    Division of Cell Recognition Study, Institute of Molecular Biomembrane and Glycobiology, Tohoku Pharmaceutical University, 4-4-1 Komatsushima, Aoba-ku, Sendai 981-8558, Japan
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  • Masahiro Hosono
    Affiliations
    Division of Cell Recognition Study, Institute of Molecular Biomembrane and Glycobiology, Tohoku Pharmaceutical University, 4-4-1 Komatsushima, Aoba-ku, Sendai 981-8558, Japan
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  • Kazuo Nitta
    Affiliations
    Division of Cell Recognition Study, Institute of Molecular Biomembrane and Glycobiology, Tohoku Pharmaceutical University, 4-4-1 Komatsushima, Aoba-ku, Sendai 981-8558, Japan
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  • Jiharu Hamako
    Affiliations
    Department of Biology, Fujita Health University, Toyoake, Aichi 470-1192, Japan
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  • Taei Matsui
    Affiliations
    Department of Biology, Fujita Health University, Toyoake, Aichi 470-1192, Japan
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  • Yasuhiro Ozeki
    Correspondence
    To whom correspondence should be addressed. Tel.: 81-45-787-2221; Fax: 81-45-787-2413
    Affiliations
    Laboratory of Glycobiology and Marine Biochemistry, Department of Life and Environmental System Science, Graduate School of NanoBio Sciences, Yokohama City University, 22-2 Seto, Kanazawa-ku, Yokohama 236-0027, Japan
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  • Author Footnotes
    * This work was supported in part by grants-in-aid for scientific research from the Japan Society for the Promotion of Science and Japanese Association for Marine Biology from the Ministry of Education, Culture, Sports, Science, and Technology Japan.The protein sequence data reported in this paper will appear in the UniProt Knowledgebase under the accession number B3EWR1 for MytiLec.
    1 Both authors contributed equally to this work and should be considered first authors.
      A novel lectin structure was found for a 17-kDa α- d-galactose-binding lectin (termed “MytiLec”) isolated from the Mediterranean mussel, Mytilus galloprovincialis. The complete primary structure of the lectin was determined by Edman degradation and mass spectrometric analysis. MytiLec was found to consist of 149 amino acids with a total molecular mass of 16,812.59 Da by Fourier transform-ion cyclotron resonance mass spectrometry, in good agreement with the calculated value of 16,823.22 Da. MytiLec had an N terminus of acetylthreonine and a primary structure that was highly novel in comparison with those of all known lectins in the structure database. The polypeptide structure consisted of three tandem-repeat domains of ∼50 amino acids each having 45–52% homology with each other. Frontal affinity chromatography technology indicated that MytiLec bound specifically to globotriose (Gb3; Galα1–4Galβ1–4Glc), the epitope of globotriaosylceramide. MytiLec showed a dose-dependent cytotoxic effect on human Burkitt lymphoma Raji cells (which have high surface expression of Gb3) but had no such effect on erythroleukemia K562 cells (which do not express Gb3). The cytotoxic effect of MytiLec was specifically blocked by the co-presence of an α-galactoside. MytiLec treatment of Raji cells caused increased binding of anti-annexin V antibody and incorporation of propidium iodide, which are indicators of cell membrane inversion and perforation. MytiLec is the first reported lectin having a primary structure with the highly novel triple tandem-repeat domain and showing transduction of apoptotic signaling against Burkitt lymphoma cells by interaction with a glycosphingolipid-enriched microdomain containing Gb3.

      References

        • Kinoshita S.
        • Wang N.
        • Inoue H.
        • Maeyama K.
        • Okamoto K.
        • Nagai K.
        • Kondo H.
        • Hirono I.
        • Asakawa S.
        • Watabe S.
        Deep sequencing of ESTs from nacreous and prismatic layer producing tissues and a screen for novel shell formation-related genes in the pearl oyster.
        PLoS ONE. 2011; 6: e21238
        • Venier P.
        • De Pittà C.
        • Bernante F.
        • Varotto L.
        • De Nardi B.
        • Bovo G.
        • Roch P.
        • Novoa B.
        • Figueras A.
        • Pallavicini A.
        • Lanfranchi G.
        MytiBase. A knowledge base of mussel (M. galloprovincialis) transcribed sequences.
        BMC Genomics. 2009; 10: 72
        • Venier P.
        • Varotto L.
        • Rosani U.
        • Millino C.
        • Celegato B.
        • Bernante F.
        • Lanfranchi G.
        • Novoa B.
        • Roch P.
        • Figueras A.
        • Pallavicini A.
        Insights into the innate immunity of the Mediterranean mussel Mytilus galloprovincialis.
        BMC Genomics. 2011; 12: 69
        • Kim Y.M.
        • Park K.I.
        • Choi K.S.
        • Alvarez R.A.
        • Cummings R.D.
        • Cho M.
        Lectin from the Manila clam Ruditapes philippinarum is induced upon infection with the protozoan parasite Perkinsus olseni.
        J. Biol. Chem. 2006; 281: 26854-26864
        • Pales Espinosa E.
        • Perrigault M.
        • Allam B.
        Identification and molecular characterization of a mucosal lectin (MeML) from the blue Mytilus edulis and its potential role in particle capture.
        Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2010; 156: 495-501
        • Tasumi S.
        • Vasta G.R.
        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. 2007; 179: 3086-3098
        • Gorbushin A.M.
        • Iakovleva N.V.
        A new gene family of single fibrinogen domain lectins in Mytilus.
        Fish Shellfish Immunol. 2011; 30: 434-438
        • Li C.
        • Yu S.
        • Zhao J.
        • Su X.
        • Li T.
        Cloning and characterization of sialic acid binding lectins (SABL) from Manila clam Venerupis philippinarum.
        Fish Shellfish Immunol. 2011; 30: 1202-1206
        • Chen J.
        • Xiao S.
        • Yu Z.
        F-type lectin involved in defense against bacterial infection in the pearl oyster (Pinctada martensii).
        Fish Shellfish Immunol. 2011; 30: 750-754
        • Belogortseva N.I.
        • Molchanova V.I.
        • Kurika A.V.
        • Skobun A.S.
        • Glazkova V.E.
        Isolation of characterization of new GalNAc/Gal-specific lectin from the sea mussel Crenomytilus grayanus.
        Comp. Biochem. Physiol. C Pharmacol. Toxicol. Endocrinol. 1998; 119: 45-50
        • Ozeki Y.
        • Matsui T.
        • Suzuki M.
        • Titani K.
        Amino acid sequence and molecular characterization of a d-galactoside-specific lectin purified from sea urchin (Anthocidaris crassispina) eggs.
        Biochemistry. 1991; 30: 2391-2394
        • Naganuma T.
        • Ogawa T.
        • Hirabayashi J.
        • Kasai K.
        • Kamiya H.
        • Muramoto K.
        Isolation, characterization, and molecular evolution of a novel pearl shell lectin from a marine bivalve, Pteria penguin.
        Mol. Divers. 2006; 10: 607-618
        • Blixt O.
        • Head S.
        • Mondala T.
        • Scanlan C.
        • Huflejt M.E.
        • Alvarez R.
        • Bryan M.C.
        • Fazio F.
        • Calarese D.
        • Stevens J.
        • Razi N.
        • Stevens D.J.
        • Skehel J.J.
        • van Die I.
        • Burton D.R.
        • Wilson I.A.
        • Cummings R.
        • Bovin N.
        • Wong C.-H.
        • Paulson J.C.
        Printed covalent glycan array for ligand profiling of diverse glycan binding proteins.
        Proc. Natl. Acad. Sci. U.S.A. 2004; 101: 17033-17038
        • Angeloni S.
        • Ridet J.L.
        • Kusy N.
        • Gao H.
        • Crevoisier F.
        • Guinchard S.
        • Kochhar S.
        • Sigrist H.
        • Sprenger N.
        Glycoprofiling with micro-arrays of glycoconjugates and lectins.
        Glycobiology. 2005; 15: 31-41
        • Tateno H.
        • Uchiyama N.
        • Kuno A.
        • Togayachi A.
        • Sato T.
        • Narimatsu H.
        • Hirabayashi J.
        A novel strategy for mammalian cell surface glycome profiling using lectin microarray.
        Glycobiology. 2007; 17: 1138-1146
        • Hirabayashi J.
        Concept, strategy, and realization of lectin-based glycan profiling.
        J. Biochem. 2008; 144: 139-147
        • Kasai K.
        • Ishii S.
        Affinity chromatography of trypsin and related enzymes. V. Basic studies of quantitative affinity chromatography.
        J. Biochem. 1978; 84: 1051-1060
        • Kasai K.
        • Ishii S.
        Studies on the interaction of immobilized trypsin and specific ligands by quantitative affinity chromatography.
        J. Biochem. 1978; 84: 1061-1069
        • Hirabayashi J.
        • Hashidate T.
        • Arata Y.
        • Nishi N.
        • Nakamura T.
        • Hirashima M.
        • Urashima T.
        • Oka T.
        • Futai M.
        • Muller W.E.
        • Yagi F.
        • Kasai K.
        Oligosaccharide specificity of galectins. A search by frontal affinity chromatography.
        Biochim. Biophys. Acta. 2002; 1572: 232-254
        • Hirabayashi J.
        • Arata Y.
        • Kasai K.
        Frontal affinity chromatography as a tool for elucidation of sugar recognition properties of lectins.
        Methods Enzymol. 2003; 362: 353-368
        • Kawsar S.M.
        • Fujii Y.
        • Matsumoto R.
        • Ichikawa T.
        • Tateno H.
        • Hirabayashi J.
        • Yasumitsu H.
        • Dogasaki C.
        • Hosono M.
        • Nitta K.
        • Hamako J.
        • Matsui T.
        • Ozeki Y.
        Isolation, purification, characterization and glycan-binding profile of a d-galactoside specific lectin from the marine sponge, Halichondria okadai.
        Comp. Biochem. Physiol. B Biochem. Mol. Biol. 2008; 150: 349-357
        • Kawsar S.M.
        • Takeuchi T.
        • Kasai K.
        • Fujii Y.
        • Matsumoto R.
        • Yasumitsu H.
        • Ozeki Y.
        Glycan-binding profile of a d-galactose binding lectin purified from the annelid, Perinereis nuntia ver. vallata.
        Comp. Biochem. Physiol. B Biochem. Mol. Biol. 2009; 152: 382-389
        • Kawsar S.M.
        • Matsumoto R.
        • Fujii Y.
        • Matsuoka H.
        • Masuda N.
        • Chihiro I.
        • Yasumitsu H.
        • Kanaly R.A.
        • Sugawara S.
        • Hosono M.
        • Nitta K.
        • Ishizaki N.
        • Dogasaki C.
        • Hamako J.
        • Matsui T.
        • Ozeki Y.
        Cytotoxicity and glycan-binding profile of a d-galactose-binding lectin from the eggs of a Japanese sea hare (Aplysia kurodai).
        Protein J. 2011; 30: 509-519
        • Matsumoto R.
        • Shibata T.F.
        • Kohtsuka H.
        • Sekifuji M.
        • Sugii N.
        • Nakajima H.
        • Kojima N.
        • Fujii Y.
        • Kawsar S.M.
        • Yasumitsu H.
        • Hamako J.
        • Matsui T.
        • Ozeki Y.
        Glycomics of a novel type-2 N-acetyllactosamine-specific lectin purified from the feather star, Oxycomanthus japonicus Pelmatozoa: Crinoidea).
        Comp. Biochem. Physiol. B Biochem. Mol. Biol. 2011; 158: 266-273
        • Matsumoto R.
        • Fujii Y.
        • Kawsar S.M.
        • Kanaly R.A.
        • Yasumitsu H.
        • Koide Y.
        • Hasan I.
        • Iwahara C.
        • Ogawa Y.
        • Im C.H.
        • Sugawara S.
        • Hosono M.
        • Nitta K.
        • Hamako J.
        • Matsui T.
        • Ozeki Y.
        Cytotoxicity and glycan-binding properties of an 18-kDa lectin isolated from the marine sponge Halichonderia okadai.
        Toxins. 2012; 4: 323-338
        • Gourdine J.P.
        • Cioci G.
        • Miguet L.
        • Unverzagt C.
        • Silva D.V.
        • Varrot A.
        • Gautier C.
        • Smith-Ravin E.J.
        • Imberty A.
        High affinity interaction between a bivalve C-type lectin and a biantennary complex-type N-glycan revealed by crystallography and microcalorimetry.
        J. Biol. Chem. 2008; 283: 30112-30120
        • Smith P.K.
        • Krohn R.I.
        • Hermanson G.T.
        • Mallia A.K.
        • Gartner F.H.
        • Provenzano M.D.
        • Fujimoto E.K.
        • Goeke N.M.
        • Olson B.J.
        • Klenk D.C.
        Measurement of protein using bicinchoninic acid.
        Anal. Biochem. 1985; 150: 76-85
        • Wiechelman K.J.
        • Braun R.D.
        • Fitzpatrick J.D.
        Investigation of the bicinchoninic acid protein assay. Identification of the groups responsible for color formation.
        Anal. Biochem. 1988; 175: 231-237
        • Laemmli U.K.
        Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
        Nature. 1970; 227: 680-685
        • Masaki T.
        • Tanabe M.
        • Nakamura K.
        • Soejima M.
        Studies on a new proteolytic enzyme from Achromobacter lyticus M497-1. I. Purification and some enzymatic properties.
        Biochim. Biophys. Acta. 1981; 660: 44-50
        • Gross E.
        Cleavage of peptide chains. The cyanogen bromide reaction.
        Methods Enzymol. 1967; 11: 238-255
        • Tahirov T.H.
        • Oki H.
        • Tsukihara T.
        • Ogasahara K.
        • Yutani K.
        • Ogata K.
        • Izu Y.
        • Tsunasawa S.
        • Kato I.
        Crystal structure of methionine aminopeptidase from hyperthermophile, Pyrococcus furiosus.
        J. Mol. Biol. 1998; 284: 101-124
        • Titani K.
        • Narita K.
        Amino acid sequences of 18 peptides isolated from the tryptic hydrolysate of Baker's yeast cytochrome c.
        J. Biochem. 1964; 56: 241-256
        • Simpson R.J.
        • Neuberger M.R.
        • Liu T.Y.
        Complete amino acid analysis of proteins from a single hydrolysate.
        J. Biol. Chem. 1976; 251: 1936-1940
        • Hewick R.M.
        • Hunkapiller M.W.
        • Hood L.E.
        • Dreyer W.J.
        A gas-liquid solid phase peptide and protein sequenator.
        J. Biol. Chem. 1981; 256: 7990-7997
        • Altschul S.F.
        • Lipman D.J.
        Protein database searches for multiple alignments.
        Proc. Natl. Acad. Sci. U.S.A. 1990; 87: 5509-5513
        • Altschul S.F.
        • Madden T.L.
        • Schäffer A.A.
        • Zhang J.
        • Zhang Z.
        • Miller W.
        • Lipman D.J.
        Gapped BLAST and PSI-BLAST: a new generation of protein database search programs.
        Nucleic Acids Res. 1997; 25: 3389-3402
        • Xu N.
        • Huang Z.-H.
        • Watson J.T.
        • Gage D.A.
        Mercaptobenzothiazoles. A new class of matrices for laser desorption ionization mass spectrometry.
        J. Am. Soc. Mass Spectrom. 1997; 8: 116-124
        • Vukelić Z.
        • Zamfir A.D.
        • Bindila L.
        • Froesch M.
        • Peter-Katalinić J.
        • Usuki S.
        • Yu R.K.
        Screening and sequencing of complex sialylated and sulfated glycosphingolipid mixtures by negative ion electrospray Fourier transform ion cyclotron resonance mass spectrometry.
        J. Am. Soc. Mass Spectrom. 2005; 16: 571-580
        • Shinohara Y.
        • Kim F.
        • Shimizu M.
        • Goto M.
        • Tosu M.
        • Hasegawa Y.
        Kinetic measurement of the interaction between an oligosaccharide and lectins by a biosensor based on surface plasmon resonance.
        Eur. J. Biochem. 1994; 223: 189-194
        • Kawano T.
        • Sugawara S.
        • Hosono M.
        • Tatsuta T.
        • Ogawa Y.
        • Fujimura T.
        • Taka H.
        • Murayama K.
        • Nitta K.
        Globotriaosylceramide-expressing Burkitt lymphoma cells are committed to early apoptotic status by rhamnose-binding lectin from catfish eggs.
        Biol. Pharm. Bull. 2009; 32: 345-353
        • Kawano T.
        • Sugawara S.
        • Hosono M.
        • Tatsuta T.
        • Nitta K.
        Alteration of gene expression induced by Silurus asotus lectin in Burkitt lymphoma cells.
        Biol. Pharm. Bull. 2008; 31: 998-1002
        • Sugawara S.
        • Hosono M.
        • Ogawa Y.
        • Takayanagi M.
        • Nitta K.
        Catfish egg lectin causes rapid activation of multidrug resistance 1 P-glycoprotein as a lipid translocase.
        Biol. Pharm. Bull. 2005; 28: 434-441
        • Sugawara S.
        • Sasaki S.
        • Ogawa Y.
        • Hosono M.
        • Nitta K.
        Catfish (Silurus asotus) lectin enhances the cytotoxic effects of doxorubicin.
        Yakugaku Zasshi. 2005; 125: 327-334
        • Tennant J.R.
        Evaluation of the trypan blue technique for determination of cell viability.
        Transplantation. 1964; 2: 685-694
        • Ishiyama M.
        • Miyazono Y.
        • Sasamoto K.
        • Ohkura Y.
        • Ueno K.
        A highly water-soluble disulfonated tetrazolium salt as a chromogenic indicator for NADH as well as cell viability.
        Talanta. 1997; 44: 1299-1305
        • Pepper C.
        • Thomas A.
        • Tucker H.
        • Hoy T.
        • Bentley P.
        Flow cytometric assessment of three different methods for the measurement of in vivo apoptosis.
        Leuk. Res. 1998; 22: 439-444
        • Naismith J.H.
        • Field R.A.
        Structural basis of trimannoside recognition by concanavalin A.
        J. Biol. Chem. 1996; 271: 972-976
        • Transue T.R.
        • Smith A.K.
        • Mo H.
        • Goldstein I.J.
        • Saper M.A.
        Structure of benzyl T-antigen disaccharide bound to Amaranthus caudatus agglutinin.
        Nat. Struct. Biol. 1997; 4: 779-783
        • Kasai K.
        • Hirabayashi J.
        Galectins. A family of animal lectins that decipher glycocodes.
        J Biochem. 1996; 119: 1-8
        • Weis W.I.
        • Taylor M.E.
        • Drickamer K.
        The C-type lectin superfamily in the immune system.
        Immunol. Rev. 1998; 163: 19-34
        • Vakonakis I.
        • Langenhan T.
        • Prömel S.
        • Russ A.
        • Campbell I.D.
        Solution structure and sugar-binding mechanism of mouse latrophilin-1 RBL. A 7TM receptor-attached lectin-like domain.
        Structure. 2008; 16: 944-953
        • Ogawa T.
        • Watanabe M.
        • Naganuma T.
        • Muramoto K.
        Diversified carbohydrate-binding lectins from marine resources.
        J. Amino Acids. 2011; 2011: 838914
        • Kotake T.
        • Dina S.
        • Konishi T.
        • Kaneko S.
        • Igarashi K.
        • Samejima M.
        • Watanabe Y.
        • Kimura K.
        • Tsumuraya Y.
        Molecular cloning of a β-galactosidase from radish that specifically hydrolyzes {β}-(1–3)-and {β}-(1–6)-galactosyl residues of Arabidnogalactan protein.
        Plant Physiol. 2005; 138: 1563-1576
        • Stepan H.
        • Pabst M.
        • Altmann F.
        • Geyer H.
        • Geyer R.
        • Staudacher E.
        O-Glycosylation of snails.
        Glycoconj. J. 2012; 29: 189-198
        • Velkova L.
        • Dolashka P.
        • Lieb B.
        • Dolashki A.
        • Voelter W.
        • Van Beeumen J.
        • Devreese B.
        Glycan structures of the structural subunit (HtH1) of Haliotis tuberculata hemocyanin.
        Glycoconj. J. 2011; 28: 385-395
        • Gutternigg M.
        • Bürgmayr S.
        • Pöltl G.
        • Rudolf J.
        • Staudacher E.
        Neutral N-glycan patterns of the gastropods Limax maximus Cepaea hortensis Planorbarius corneus Arianta arbustorum and Achatina fulica.
        Glycoconj. J. 2007; 24: 475-489
        • Fujii Y.
        • Sugawara S.
        • Araki D.
        • Kawano T.
        • Tatsuta T.
        • Takahashi K.
        • Kawsar S.M.
        • Matsumoto R.
        • Kanaly R.A.
        • Yasumitsu H.
        • Ozeki Y.
        • Hosono M.
        • Miyagi T.
        • Hakomori S.-I.
        • Takayanagi M.
        • Nitta K.
        MRP1 expressed on Burkitt lymphoma cells was depleted by catfish egg lectin through Gb3-glycosphinogolipid and enhanced cytotoxic effect of drugs.
        Protein J. 2012; 31: 15-26
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