Abstract
In sea stars, adhesion takes place at the level of a multitude of small appendages, the tube feet. It involves the secretion of an adhesive material which, after tube foot detachment, remains on the substratum as a footprint. It was previously reported that the two main organic components of this material are proteins and carbohydrates. The carbohydrate moiety of the adhesive secretion of Asterias rubens was investigated using a set of 16 lectins which were used on sections through tube feet, on footprints, and on the proteins extracted from these footprints. After gel electrophoresis, these proteins separate into eight protein bands which were named sea star footprint proteins (Sfps). Eleven lectins label the tube foot epidermis at the level of the adhesive cells, four react with footprints, and eight with two of the extracted footprint proteins, which are therefore classified as glycoproteins. Sfp-290 appears to bear mostly N-linked oligosaccharides and Sfp-210 principally O-linked oligosaccharides. The outer chains of both glycoproteins enclose galactose, N-acetylgalactosamine, fucose, and sialic acid residues. Another part of the carbohydrate fraction of the footprints would be in the form of larger molecules, such as sialylated proteoglycans. These two types of glycoconjugates are presumably key components of the sea star temporary adhesive providing both cohesive and adhesive contributions through electrostatic interactions by the polar and hydrogen-bonding functional groups of their glycan chains.
Similar content being viewed by others
References
Ameye L, De Becker G, Killian C, Wilt F, Kemps R, Kuypers S, Dubois P (2001) Proteins and saccharides of the sea urchin organic matrix of mineralization: characterization and localization in the spine skeleton. J Struct Biol 134:56–66
Bhaskar PV, Bhosle NV (2005) Microbial extrapolymeric substances in marine biogeochemical processes. Curr Sci India 88:45–53
Caldwell GS, Pagett HE (2010) Marine glycobiology: current status and future perspectives. Mar Biotechnol 12:241–252
Carlsson SR (1993) Isolation and characterization of glycoproteins. In: Fukuda M, Kobata A (eds) Glycobiology: a practical approach. Oxford University Press, New York, pp 1–26
Chiovitti A, Heraud P, Dugdale TM, Hodson OM, Curtain RCA, Dagastine RR, Wood BR, Wetherbee R (2008) Divalent cations stabilize the aggregation of sulphated glycoproteins in the adhesive nanofibers of the biofouling diatom Toxarium undulatum. Soft Matter 4:811–820
Cummings RD (1993) Structural characterization of N-glycans obtained from metabolically-radiolabelled glycoproteins. In: Fukuda M, Kobata A (eds) Glycobiology: a practical approach. Oxford University Press, New York, pp 243–289
Cummings RD, Kornfeld S (1982) Characterization of the structural determinants required for the high affinity interaction of asparagines-linked oligosaccharides with immobilized Phaseolus vulgaris leukoagglutinating and erythroagglutinating lectins. J Biol Chem 257:11230–11234
Debray H, Decout D, Strecker G, Spik G, Montreuil J (1981) Specificity of twelve lectins toward oligosaccharides and glycopeptides related to N-glycosylproteins. Eur J Biochem 117:41–55
De Moor S, Waite JH, Jangoux M, Flammang P (2003) Characterization of the adhesive from Cuvierian tubules of the sea cucumber Holothuria forskali (Echinodermata, Holothuroidea). Mar Biotechnol 5:45–57
Epstein L, Nicholson RL (2006) Adhesion and adhesives of fungi and oomycetes. In: Smith AM, Callow JA (eds) Biological adhesives. Springer, Berlin, pp 41–62
Flammang P (2006) Adhesive secretions in echinoderms: an overview. In: Smith AM, Callow JA (eds) Biological adhesives. Springer, Berlin, pp 183–206
Flammang P, Demeulenaere S, Jangoux M (1994) The role of podial secretions in adhesion in two species of sea stars (Echinodermata). Biol Bull 187:35–47
Flammang P, Michel A, Van Cauwenberge A, Alexandre H, Jangoux M (1998) A study of the temporary adhesion of the podia in the sea star Asterias rubens (Echinodermata, Asteroidea) through their footprints. J Exp Biol 201:2383–2395
Flammang P, Lambert A, Bailly P, Hennebert E (2009) Polyphosphoprotein-containing marine adhesives. J Adhes 85:447–464
Fukuda M, Kobata A (1993) Glycobiology: a practical approach. Oxford University Press, New York
Gabe M (1968) Techniques histologiques. Masson, Paris
Graham LD, Glattauer V, Peng YY, Vaughan PR, Wermeister JA, Tyler MJ, Ramshaw JAM (2006) An adhesive secreted by Australian frogs of the genus Notaden. In: Smith AM, Callow JA (eds) Biological adhesives. Springer, Berlin, pp 207–223
Gravel P, Golaz O (1996) Identification of glycoproteins on nitrocellulose membranes using lectin blotting. In: Walker JM (ed) The protein protocols handbook. Humana, Totowa, pp 603–617
Haag P (2006) Mechanical properties of bacterial exopolymeric adhesives and their commercial development. In: Smith AM, Callow JA (eds) Biological adhesives. Springer, Berlin, pp 1–19
Hennebert E, Viville P, Lazzaroni R, Flammang P (2008) Micro-and nanostructure of the adhesive material secreted by the tube feet of the sea star Asterias rubens. J Struct Biol 164:108–118
Kamino K (2006) Barnacle underwater attachment. In: Smith AM, Callow JA (eds) Biological adhesives. Springer, Berlin, pp 145–166
Kamino K (2008) Underwater adhesive of marine organisms as the vital link between biological science and material science. Mar Biotechnol 10:111–121
Kobata A, Yamashita K (1993) Fractionation of oligosaccharides by serial affinity chromatography with use of immobilized lectin columns. In: Fukuda M, Kobata A (eds) Glycobiology: a practical approach. Oxford University Press, New York, pp 103–125
Leathem AJC, Atkins J (1983) Lectin binding to paraffin sections. In: Bullock GR, Petrusz P (eds) Techniques in immunocytochemistry (vol II). Academic, London, pp 39–70
Lee BP, Dalsin JL, Messersmith PB (2006) Biomimetic adhesive polymers based on mussel adhesive proteins. In: Smith AM, Callow JA (eds) Biological adhesives. Springer, Berlin, pp 257–278
Li D, Huson GH, Graham LD (2008) Proteinaceous adhesive secretions from insects, and in particular the egg attachment glue of Opodiphthera sp. moths. Arch Insect Biochem 69:85–105
Michael TS (2009) Glycoconjugate organization of Enteromorpha (=Ulva) flexuosa and Ulva fasciata (Chlorophyta) zoospores. J Phycol 45:660–677
Molino PJ, Wetherbee R (2008) The biology of biofouling diatoms and their role in the development of microbial slimes. Biofouling 24:365–379
Monsigny M, Roche A, Sene C, Maget-Dana R, Delmotte F (1980) Sugar–lectin interactions: how does wheat-germ agglutinin bind sialoglycoconjugates? Eur J Biochem 104:147–153
Montreuil J, Bouquelet S, Debray H, Fournet B, Spik G, Strecker G (1986) Glycoproteins. In: Chaplin MS, Kennedy JF (eds) Carbohydrate analysis: a practical approach. Academic, Oxford, pp 143–204
Ohkawa K, Nishida A, Yamamoto H, Waite JH (2004) A glycosylated byssal precursor protein from the green mussel Perna viridis with modified Dopa side-chains. Biofouling 20:101–115
Osawa T, Tsuji T (1987) Fractionation and structural assessment of oligosaccharides and glycopeptides by use of immobilized lectins. Annu Rev Biochem 56:21–42
Piller F, Piller V (1993) Structural characterization of mucin-type O-linked oligosaccharides. In: Fukuda M, Kobata A (eds) Glycobiology: a practical approach. Oxford University Press, New York, pp 491–328
Ravindranath RMH, Basilrose SRM (2005) Localization of sulfated sialic acids in the dentinal tubules during tooth formation in mice. Acta Histochem 107:43–56
Sagert J, Sun C, Waite JH (2006) Chemical subtleties of mussel and polychaete holdfasts. In: Smith AM, Callow JA (eds) Biological adhesives. Springer, Berlin, pp 125–143
Santos R, Hennebert E, Varela Coelho A, Flammang P (2009) The echinoderm tube foot and its role in temporary underwater adhesion. In: Gorb S (ed) Functional surfaces in biology. Springer, Nertherlands, pp 9–42
Segrest JP, Jackson RL (1972) Molecular weight determination of glycoproteins by polyacrylamide gel electrophoresis in sodium dodecyl sulphate. In: Ginsburg V (ed) Methods in enzymology vol 28B V. Academic, New York, pp 54–63
Silverman HG, Roberto FF (2007) Understanding marine mussel adhesion. Mar Biotechnol 9:661–681
Smith AM, Callow JA (2006) Biological adhesives. Springer, Berlin
Smith AM, Morin MC (2002) Biochemical differences between trail mucus and adhesive mucus from marsh periwinkle snails. Biol Bull 203:338–346
Smith AM, Quick TJ, St Peter RLS (1999) Differences in the composition of adhesive and non-adhesive mucus from the limpet Lottia limatula. Biol Bull 196:34–44
Stanley MS, Callow ME, Callow JA (1999) Monoclonal antibodies to adhesive cell coat glycoproteins secreted by zoospores of the green alga Enteromorpha. Planta 210:61–71
Stewart RJ, Weaver JC, Morse DE, Waite JH (2004) The tube cement of Phragmatopoma californica: a solid foam. J Exp Biol 207:4727–4734
Sueyoshi S, Tsuji T, Osawa T (1988) Carbohydrate-binding specificities of five lectins that bind to O-glycosyl-linked carbohydrate chains. Quantitative analysis by frontal-affinity chromatography. Carbohydr Res 178:213–224
Sun C, Fantner GE, Adams J, Hansma PK, Waite JH (2007) The role of calcium and magnesium in the concrete tubes of the sandcastle worm. J Exp Biol 210:1481–1488
Sun C, Shrivastava A, Reifert JR, Waite JH (2009) Halogenated DOPA in a marine adhesive protein. J Adhes 85:126–138
Thomas LA, Hermans CO (1985) Adhesive interactions between the tube feet of a starfish, Leptasterias hexactis, and substrata. Biol Bull 169:675–688
Waite JH (1987) Nature’s underwater adhesive specialist. Int J Adhes Adhes 7:9–14
Waite JH, Qin X (2001) Polyphosphoprotein from the adhesive pads of Mytilus edulis. Biochemistry 40:2887–2893
Waite JH, Andersen NH, Jewhurst S, Sun C (2005) Mussel adhesion: finding the tricks worth mimicking. J Adhes 81:297–317
Walker G (1987) Marine organisms and their adhesion. In: Wake WC (ed) Synthetic adhesives and sealants. Wiley, Chichester, pp 112–135
Wiegemann M (2005) Adhesion in blue mussels (Mytilus edulis) and barnacles (genus Balanus): mechanisms and technical applications. Aquat Sci 67:166–176
Wu AM, Song SC, Sugii S, Herp A (1997) Differential binding properties of Gal/GalNAc specific lectins available for characterization of glycoreceptors. Indian J Biochem Biophys 34:61–71
Yamamoto K, Konami Y, Irimura T (1997) Sialic acid-binding motif of Maackia amurensis lectins. J Biochem 121:756–761
Zhao H, Waite JH (2006) Linking adhesive and structural proteins in the attachment plaque of Mytilus californianus. J Biol Chem 281:26150–26158
Zhao H, Sun C, Stewart RJ, Waite JH (2005) Cement proteins of the tube-building polychaete Phragmatopoma californica. J Biol Chem 280:42938–42944
Zhao H, Sagert J, Hwang DS, Waite JH (2009) Glycosylated hydroxytryptophan in a mussel adhesive protein from Perna viridis. J Biol Chem 284:23344–23352
Acknowledgements
Work supported by a FRIA doctoral grant to E.H., by a FRFC Grant no 2.4532.07, by the “Service Public de Wallonie—Programme Winnomat 2” and by the “Communauté française de Belgique—Actions de Recherche Concertées”. P.F. is Senior Research Associate of the Fund for Scientific Research of Belgium (F.R.S.-FNRS). This study is a contribution of the “Centre Interuniversitaire de Biologie Marine” (CIBIM; http://www.ulb.ac.be/sciences/biomar/).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Hennebert, E., Wattiez, R. & Flammang, P. Characterisation of the Carbohydrate Fraction of the Temporary Adhesive Secreted by the Tube Feet of the Sea Star Asterias rubens . Mar Biotechnol 13, 484–495 (2011). https://doi.org/10.1007/s10126-010-9319-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10126-010-9319-6