Fish Physiology and Biochemistry

, Volume 39, Issue 6, pp 1619–1630 | Cite as

Domain composition of rhamnose-binding lectin from shishamo smelt eggs and its carbohydrate-binding profiles

  • Masahiro HosonoEmail author
  • Shigeki Sugawara
  • Takeo Tatsuta
  • Toshiyuki Hikita
  • Junko Kominami
  • Sachiko Nakamura-Tsuruta
  • Jun Hirabayashi
  • Sarkar M. A. Kawsar
  • Yasuhiro Ozeki
  • Sen-itiroh Hakomori
  • Kazuo Nitta


Osmerus (Spirinchus) lanceolatus egg lectin (OLL) is a member of the rhamnose-binding lectin (RBL) family which is mainly found in aqueous beings. cDNA of OLL was cloned, and its genomic architecture was revealed. The deduced amino acid (aa) sequence indicated that OLL was composed of 213 aa including 95 aa of domain N and 97 aa of domain C. N and C showed 73 % sequence identity and contained both -ANYGR- and -DPC-KYL-peptide motifs which are conserved in most of the RBL carbohydrate recognition domains. The calculated molecular mass of mature OLL was 20,852, consistent with the result, and 20,677.716, from mass spectrometry. OLL was encoded by eight exons: exons 1 and 2 for a signal peptide; exons 3–5 and 6–8 for N- and C-domains, respectively. Surface plasmon resonance spectrometric analyses revealed that OLL showed comparable affinity for Galα- and β-linkages, whereas Silurus asotus lectin (SAL), a catfish RBL, bound preferentially to α-linkages of neoglycoproteins. The Kd values of OLL and SAL against globotriaosylceramide (Gb3) were 1.69 × 10−5 M for and 2.81 × 10−6 M, respectively. Thus, the carbohydrate recognition property of OLL is slightly different from that of SAL. On the other hand, frontal affinity chromatography revealed that both OLL and SAL interacted with only glycolipid-type oligosaccharides such as Gb3 trisaccharides, not with N-linked oligosaccharides. The domain composition of these RBLs and an analytical environment such as the “cluster effect” of a ligand might influence the binding between RBL and sugar chains.


Lectin Fish eggs Domain structure Carbohydrate-binding Rhamnose 



Rhamnose-binding lectin


Osmerus lanceolatus lectin


Silurus asotus lectin


Surface plasmon resonance


Frontal affinity chromatography


Carbohydrate recognition domain



A part of this work was supported by a Grant-in-Aid for Frontier Research Program from The Ministry of Education, Culture, Sports, Science, and Technology of Japan. We thank Dr. Stephen Anderson for editing of the manuscript.

Supplementary material

10695_2013_9814_MOESM1_ESM.doc (33 kb)
Supplementary material 1 (DOC 33 kb)


  1. Bah CSF, Fang EF, Ng TB, Mros S, McConnell M, Bekhit AE-DA (2011) Purification and characterization of a rhamnose-binding Chinook salmon roe lectin with antiproliferative activity toward tumor cells and nitric oxide-inducing activity toward murine macrophage. J Agric Food Chem 59:5720–5728PubMedCrossRefGoogle Scholar
  2. Barondes SH, Castronovo V, Cooper DN, Cummings RD, Drickamer K, Feizi T, Gitt MA, Hirabayashi J, Hughes C, Kasai K (1994) Galectins: a family of animal β-galactoside-binding lectins. Cell 76:597–598PubMedCrossRefGoogle Scholar
  3. Beck BH, Framer BD, Straus DL, Li C, Peatman E (2012) Putative roles for a rhamnose binding lectin in Flavobacterium columnare pathogenesis in channel catfish Ictalurus punctatus. Fish Shellfish Immunol 33:1008–1015PubMedGoogle Scholar
  4. Breathnach R, Chambon P (1981) Organization and expression of eucaryotic split genes coding for proteins. Annu Rev Biochem 50:349–383PubMedCrossRefGoogle Scholar
  5. Day AJ (1994) The C-type carbohydrate recognition domain (CRD) superfamily. Biochem Soc Trans 22:83–87PubMedGoogle Scholar
  6. Dodd RB, Drickamer K (2001) Lectin-like protein in model organisms: implications for evolution of carbohydrate-binding activity. Glycobiology 11:71R–79RPubMedCrossRefGoogle Scholar
  7. Drickamer K, Dodd RB (1999) C-type lectin-like domains in Caenorhabditis elegans: predictions from the complete genome sequence. Glycobiology 9:1357–1369PubMedCrossRefGoogle Scholar
  8. Eto T, Ichikawa Y, Nishimura K, Ando S, Yamakawa T (1968) Chemistry of lipid of the posthemolytic residue or stroma of erythrocytes. J Biochem 64:205–213PubMedGoogle Scholar
  9. Franchi N, Schiavon F, Carletto M, Gasparini F, Bertoloni G, Tosatto SCE, Ballarin L (2011) Immune roles of a rhamnose-binding lectin in the colonial ascidian Botryllus schlosseri. Immunology 216:725–736Google Scholar
  10. Gasparini F, Franchi N, Spolaore B, Ballarin L (2008) Novel rhamnose-binding lectins from the colonial ascidian Botryllus schlosseri. Dev Comp Immunol 32:1177–1191PubMedCrossRefGoogle Scholar
  11. Gitt MA, Xia YR, Atchison RE, Lusis AJ, Barondes SH, Leffler H (1998) Sequence, structure, and Chromosomal mapping of the mouse Lgals6 gene, encoding galectin-6. J Biol Chem 273:2961–2970PubMedCrossRefGoogle Scholar
  12. Hanashima T, Miyake M, Yahiro K, Iwamaru Y, Ando A, Morinaga N, Noda M (2008) Effect of Gb3 in lipid rafts in resistance to Shiga-like toxin of mutant Vero cells. Microb Pathog 45:124–133PubMedCrossRefGoogle Scholar
  13. Hirabayashi J, Arata Y, Kasai K (2003) Frontal affinity chromatography as a tool for elucidation of sugar recognition properties of lectins. Methods Enzymol 362:353–368PubMedCrossRefGoogle Scholar
  14. Hosono M, Matsuda K, Kawauchi H, Takayanagi Y, Shiokawa H, Mineki R, Murayama K, Nitta K (1992) Comparison of N-terminal amino acid sequence of fish roe rhamnose-binding lectins. Biomed Res 13:443–449Google Scholar
  15. Hosono M, Kawauchi H, Nitta K, Takayanagi Y, Shiokawa H, Mineki R, Murayama K (1993) Purification and characterization of Silurus asotus (Catfish) roe lectin. Biol Pharm Bull 16:1–5PubMedCrossRefGoogle Scholar
  16. Hosono M, Ishikawa K, Mineki R, Murayama K, Numata C, Ogawa Y, Takayanagi Y, Nitta K (1999) Tandem repeat structure of rhamnose-binding lectin from catfish (Silurus asotus) eggs. Biochim Biophys Acta 1472:668–675PubMedCrossRefGoogle Scholar
  17. Jia WZ, Shang N, Guo QL (2010) Molecular cloning of rhamnose-binding lectin gene and its promoter region from snakehead Channa argus. Fish Physiol Biochem 36:451–459PubMedCrossRefGoogle Scholar
  18. Jimbo M, Usui R, Sakai R, Muramoto K, Kamiya H (2007) Purification, cloning and characterization of egg lectins from the teleost Tribolodon brandti. Comp Biochem Physiol B147:164–171Google Scholar
  19. Kawano T, Sugawara S, Hosono M, Tatsuta T, Nitta K (2008) Alteration of gene expression induced by Silurus asotus lectin in Burkitt’s lymphoma cells. Biol Pharm Bull 31:998–1002PubMedCrossRefGoogle Scholar
  20. Krajhanzl A (1990) Egg lectins of invertebrates and lower vertebrates: properties and biological function. Adv Lectin Res 3:83–131Google Scholar
  21. Mangeney M, Lingwood CA, Taga S, Caillou B, Tursz T, Wiels J (1993) Apoptosis induced in Burkitt’s lymphoma cells via Gb3/CD77, a glycolipid antigen. Cancer Res 53:5314–5319PubMedGoogle Scholar
  22. Naganuma T, Ogawa T, Hirabayashi J, Kasai K, Kamiya H, Muramoto K (2006) Isolation, characterization and molecular evolution of a novel pearl shell lectin from a marine bivalve, Pteria penguin. Mol Div 10:607–618CrossRefGoogle Scholar
  23. Nakamura S, Yagi F, Totani K, Ito Y, Hirabayashi J (2005) Comparative analysis of carbohydrate-binding properties of two tandem repeat-type Jacalin related lectins, Castanea crenata agglutinin and Cycas revoluta leaf lectin. FEBS J 272:2784–2799PubMedCrossRefGoogle Scholar
  24. Nitta K, Kawano T, Sugawara S, Hosono M (2007) Regulation of Globotriaosylceramide (Gb3)-mediated signal transduction by rhamnose-binding lectin. Yakugaku Zasshi 127:553–561PubMedCrossRefGoogle Scholar
  25. Ogawa T, Watanabe M, Naganuma T, Muramoto K (2011) Diversified carbohydrate-binding lectins from marine resources. J Amino acids. doi: 10.4061/2011/838914 PubMedGoogle Scholar
  26. Okamoto M, Tsutsui S, Tasumi S, Suetake H, Kikuchi K, Suzuki Y (2005) Tandem repeat l-rhamnose-binding lectin from the skin mucus of ponyfish, Leiognathus nuchalis. Biochem Biophys Res Commum 333:463–469CrossRefGoogle Scholar
  27. Ozeki Y, Matsui T, Suzuki M, Titani K (1991) Amino acid sequence and molecular characterization of a D-galactose-specific lectin purified from sea urchin (Anthocidaris crassispina) eggs. Biochemistry 30:2391–2394PubMedCrossRefGoogle Scholar
  28. Shiina N, Tateno H, Ogawa T, Muramoto K, Saneyoshi M, Kamiya H (2002) Isolation and characterization of L-rhamnose-binding lectin from chum salmon (Oncorhynchus keta) eggs. Fisheries Sci 68:1352–1366CrossRefGoogle Scholar
  29. Shirai T, Watanabe Y, Lee M, Ogawa T, Muramoto K (2009) Structure of rhamnose-binding lectin CSL3: unique pseudo-tetrameric architecture of a pattern recognition protein. J Mol Biol 391:390–403PubMedCrossRefGoogle Scholar
  30. Stellner K, Saito H, Hakomori S (1973) Determination of amino sugar linkages in glycolipids by methylation: amino sugar linkages of ceramide pentasaccharides of rabbit erythrocytes and of Forssman antigen. Arch Biochem Biophys 155:464–472PubMedCrossRefGoogle Scholar
  31. Sugawara S, Sasaki S, Ogawa Y, Hosono M, Nitta K (2005a) Catfish (Silurus asotus) lectin enhances the cytotoxic effects of doxorubicin. Yakugaku Zasshi 125:327–334PubMedCrossRefGoogle Scholar
  32. Sugawara S, Hosono M, Ogawa Y, Takayanagi M, Nitta K (2005b) Catfish egg lectin causes rapid activation of multidrug resistance 1 P-glycoprotein as a lipid translocase. Biol Pharm Bull 28:434–441PubMedCrossRefGoogle Scholar
  33. Sun F, Peatman E, Li C, Liu S, Jiang Y, Zhou Z, Liu Z (2012) Transcriptomic signatures of attachment, NF-kB suppression and IFN stimulation in the catfish gill following columnaris bacterial infection. Dev Comp Immunol 38:169–180PubMedCrossRefGoogle Scholar
  34. Tateno H (2010) SUEL-related lectin, a lectin family widely distributed throughout organisms. Biosci Biotechnol Biochem 74:1141–1144PubMedCrossRefGoogle Scholar
  35. Tateno H, Saneyoshi A, Ogawa T, Muramoto K, Kamiya H, Saneyoshi M (1998) Isolation and characterization of rhamnose-binding lectins from eggs of steelhead trout (Oncorhynchus mykiss) homologous to low density lipoprotein receptor superfamily. J Biol Chem 273:19190–19197PubMedCrossRefGoogle Scholar
  36. Tateno H, Ogawa T, Muramoto K, Kamiya H, Hirai T, Saneyoshi M (2001) A novel rhamnose-binding lectin family from eggs of steelhead trout (Oncorhynchus mykiss) with different structures and tissue distribution. Biosci Biotechnol Biochem 65:1328–1338PubMedCrossRefGoogle Scholar
  37. Tateno H, Ogawa T, Muramoto K, Kamiya H, Saneyoshi M (2002a) Distribution and molecular evolution of rhamnose-binding lectins in Salmonidae: isolation and characterization of two lectins from white-spotted charr (Salvelinus leucomaenis) eggs. Biosci Biotechnol Biochem 66:1356–1365PubMedCrossRefGoogle Scholar
  38. Tateno H, Ogawa T, Muramoto K, Kamiya H, Saneyoshi M (2002b) Rhamnose-binding lectins from steelhead trout (Oncorhynchus mykiss) eggs recognize bacterial lipopolysaccharides and lipoteichoic acid. Biosci Biotechnol Biochem 66:604–612PubMedCrossRefGoogle Scholar
  39. Tateno H, Shibata Y, Nagahama Y, Hirai T, Saneyoshi M, Ogawa T, Muramoto K, Kamiya H (2002c) Tissue-specific expression of rhamnose-binding lectins in the steelhead trout(Oncorhynchus mykiss). Biosci Biotechnol Biochem 66:1427–1430PubMedCrossRefGoogle Scholar
  40. Tateno H, Yamaguchi T, Ogawa T, Muramoto K, Watanabe T, Kamiya H, Saneyoshi M (2002d) Immunohistochemical localization of rhamnose-binding lectins in the steelhead trout (Oncorhynchus mykiss). Dev Comp Immun 26:543–550CrossRefGoogle Scholar
  41. Terada T, Watanabe Y, Tateno H, Naganuma T, Ogawa T, Muramoto K, Kamiya H (2007) Structural characterization of a rhamnose-binding glycoprotein (lectin) from Spanish mackerel (Scomberomorous niphonius) eggs. Biochim Biophys Acta 1770:617–629PubMedCrossRefGoogle Scholar
  42. Watanabe Y, Tateno H, Nakamura-Tsuruta S, Kominami J, Hirabayashi J, Nakamura O, Watanabe T, Kamiya H, Naganuma T, Ogawa T, Naude RJ, Muramoto K (2009) The function of rhamnose-binding lectin in innate immunity by restricted binding to Gb3. Dev Comp Immunol 33:187–197PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Masahiro Hosono
    • 1
    Email author
  • Shigeki Sugawara
    • 1
  • Takeo Tatsuta
    • 1
  • Toshiyuki Hikita
    • 2
  • Junko Kominami
    • 3
  • Sachiko Nakamura-Tsuruta
    • 3
  • Jun Hirabayashi
    • 4
  • Sarkar M. A. Kawsar
    • 5
  • Yasuhiro Ozeki
    • 6
  • Sen-itiroh Hakomori
    • 7
    • 8
  • Kazuo Nitta
    • 1
  1. 1.Division of Cell Recognition Study, Institute of Molecular Biomembrane and GlycobiologyTohoku Pharmaceutical UniversitySendaiJapan
  2. 2.Department of PediatricsTeikyo University School of MedicineTokyoJapan
  3. 3.Research Center for Medical GlycosciencesNational Institute of Advanced Industrial Science and TechnologyTsukubaJapan
  4. 4.Research Center for Stem Cell EngineeringNational Institute of Advanced Industrial Science and TechnologyTsukubaJapan
  5. 5.Laboratory of Carbohydrate and Protein Chemistry, Department of Chemistry, Faculty of ScienceUniversity of ChittagongChittagongBangladesh
  6. 6.Laboratory of Glycobiology and Marine Biochemistry, Department of Life and Environmental System Science, Graduate School of NanoBio SciencesYokohama City UniversityYokohamaJapan
  7. 7.Division of Biomembrane ResearchPacific Northwest Research InstituteSeattleUSA
  8. 8.Departments of Pathobiology and MicrobiologyUniversity of WashingtonSeattleUSA

Personalised recommendations