Skip to main content
SpringerLink
Log in

The glue protein of ribbed mussels (Geukensia demissa): a natural adhesive with some features of collagen

  • Published:
Journal of Comparative Physiology B Aims and scope Submit manuscript

Summary

The Atlantic ribbed musselGeukensia (Modiolus)demissa attaches itself to the roots of cord grass and other hard objects in tidal salt marshes by spinning adhesive byssal threads. The precursor of a protein apparently present in the adhesive plaques of the threads was isolated in quantity from the foot of the mussel. The protein has an apparent molecular weight of 130000, a pI of 8.1, and contains a high proportion of Gly, Glu/Gln, Lys and 3,4-dihydroxyphenyl-l-alanine (DOPA). Sequence of tryptic peptides suggests a pattern of repeated motifs, such as: Gly-DOPA-Lys, and X-Gly-DOPA-Y-Z-Gly-DOPA/Tyr-Lys, where X is Thr or Ala in octapeptides and Gln-Thr in nonapeptides. Y is variable, but more often than not hydrophobic; and Z is frequently Pro or 4-trans-hydroxyproline (Hyp). The presence of Pro-Gly and Hyp-Gly sequences of δ-hydroxylysine in the protein is reminiscent of typical collagens; however, the protein is not labile to clostridial collagenase, nor does collagen cross-react with antibodies raised against the mussel protein. Unlike typical collagens, Gly probably occurs only at every 4th or 5th residue in this unusual mussel protein.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

Anti-Gdfp :

anti-G. demissa foot protein

Dopa :

3,4-dihydroxyphenylalanine

CTAB :

cetyltrimethylammonium bromide

HPLC :

high performance liquid chromatography

PAGE :

polyacrylamide gel electrophoresis

References

  • Avdeef A, Sofen SR, Bregante TL, Raymond KN (1978) Coordination chemistry of microbial iron transport compounds J Am Chem Soc 100:5362–5370

    Google Scholar 

  • Bartels H (1964) Stabilitat von Silicium-Komplexen. Helv Chem Acta 47:1605–1609

    Google Scholar 

  • Brahmachari SK, Ananthanarayanan VS (1979) β-Turns in nascent procollagen are sites of post-translational enzymatic hydroxylation of proline. Proc Nat Acad Sci USA 76:5199–5123

    Google Scholar 

  • Brown CH (1952) Some structural proteins ofMytilus edulis. Quart J Microsc Sci 93:487–502

    Google Scholar 

  • Comyn J (1981) In: Kinloch AJ (ed) Developments in adhesives, vol 2, pp 279–313, Applied Science Publishers, Barking, UK

    Google Scholar 

  • Dorsett LC, Hawkins CJ, Grice JA, Lavin MF, Merefield PM, Parry DL, Ross IL (1987) Ferreascidin: A highly aromatic protein containing 3,4-dihydroxyphenylalanine from the blood cells of a stolidobranch ascidian. Biochemistry 26:8078–8082

    Google Scholar 

  • Foster JA (1982) Elastin structure and biosynthesis. Meth Enzymol 82:559–570

    Google Scholar 

  • Gibson LJ, Ashby MF (1982) The mechanics of three-dimensional cellular materials. Proc Roy Soc Lond A 382:43–59

    Google Scholar 

  • Glauert AM (1984) Fixation, dehydration, and embedding of biological specimens. North-Holland Publishing Co, Amsterdam, NETH

    Google Scholar 

  • Hawkins CL, Lavin MF, Parry DL, Ross I (1986) Isolation of 3,4-dihydroxyphenylalanine-containing proteins using boronate affinity chromatography. Anal Biochem 156:187–191

    Google Scholar 

  • Jensen RA, Morse DE (1988) The bioadhesive ofPhragmatopoma californica tubes: a silk-like cement containingl-DOPA. J Comp Physiol B 158:317–324

    Google Scholar 

  • Kivirikko K, Myllylä R (1982) Post-translational enzymes in the biosynthesis of collagen: Intracellular enzymes. Meth Enzymol 82:245–304

    Google Scholar 

  • Kraus ML, Crow JH (1985) Substrate characteristics associated with the distribution of the ribbed musselGeukensia demissa on a tidal creek bank in southern New Jersey. Estuaries 8:237–243

    Google Scholar 

  • Kummert R, Stumm W (1980) The surface complexation of organic acids on hydrous γ-alumina. J Colloid Interf Sci 75:373–385

    Google Scholar 

  • Lent CH (1969) Adaptations of the ribbed musselGeukensis (Modiolus) demissa to the intertidal habitat. Am Zool 9:283–292

    Google Scholar 

  • Marjanen IA, Ryrie IJ (1974) Molecular weight determination of hydrophilic proteins by cationic detergent electrophoresis. Acta Biochim Biophys 371:442–449

    Google Scholar 

  • Mascolo JM, Waite JH (1986) Protein gradients in byssal threads of some marine bivalve molluscs. J Exp Zool 240:1–7

    Google Scholar 

  • Matsudaira P (1987) Sequence from picomole quantities of proteins onto polyvinylidene difluoride membranes. J Biol Chem 262:10035–10038

    Google Scholar 

  • McBride MB, Wesselink LG (1988) Chemisorption of catechol on gibbsite, boehmite, and noncrystalline alumina surfaces. Environ Sci Technol 22:703–708

    Google Scholar 

  • Mentasti E, Pelizzetti E, Saini F (1973) Reactions between iron (III) and catechol. Equilibria and kinetics of the redox reaction in aqueous acid solution. J Chem Soc A 1973:2609–2614

    Google Scholar 

  • Öhman LO, Sjöberg S (1983) A potentiometric study of aluminum pyrocatecholates and aluminum hydroxo pyrocatecholates in 0.6M NaCl. Polyhedron 2:13429–13435

    Google Scholar 

  • Ozols J (1986) Complete amino acid sequence of cytochrome P-450 isolated from β-naphtho-flavone induced rabbit liver microsomes. J Biol Chem 261:3965–3979

    Google Scholar 

  • Panyim S, Chalkley R (1969) High resolution acrylamide gel electrophoresis of histones. Arch Biochem Biophys 130:337–346

    Google Scholar 

  • Pierpont CG, Buchanan RB (1981) Transition metal complexes of o-benzoquinone, o-semiquinone, and catecholate ligands. Coord Chem Rev 38:45–87

    Google Scholar 

  • Raju K, Anwar RA (1987) Primary structures of bovine elastin a, b, and c deduced from the sequences of cDNA clones. J Biol Chem 262:5755–5762

    Google Scholar 

  • Reynolds GEJ (1969) Polymer design in relation to adhesive properties. Aspects Adhes 6:96–111

    Google Scholar 

  • Rzepecki L, Nagafuchi T, Waite JH (in press) Oxidative formation of peptidy α, β-dehydro DOPA: a potential sclerotization intermediate. J Am Chem Soc

  • Segrest JP, Jackson RL (1972) Molecular weight determination of glycoproteins by polyacrylamide gel electrophoresis in sodium dodecyl sulfate. Methods Enzymol 28:54–62

    Google Scholar 

  • Seifter S, Harper E (1971) The collagenases. Enzymes 3:649–700

    Google Scholar 

  • Stamhuis EJ (1969) In: Cook AG (ed) Enamines: synthesis, structure, and reactions. Marcel Dekker, New York, p 101–113

    Google Scholar 

  • Towbin H, Staehelin T, Gordon J (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Nat Acad Sci USA 76:4350–4354

    Google Scholar 

  • Waite JH (1983) Evidence for a repeating 3,4-dihydroxyphenylalanine- and hydroxyproline-containing decapeptide in the adhesive protein of the musselMytilus edulis. J Biol Chem 258:2911–2915

    Google Scholar 

  • Waite JH (1985) Catecholoxidase in the byssus of the common musselMytilus edulis. J Mar Biol Ass UK 65:359–371

    Google Scholar 

  • Waite JH (1986) Mussel glue fromMytilus californianus: a comparative study. J Comp Physiol 156B:491–496

    Google Scholar 

  • Waite JH (1987) Nature's underwater adhesive specialist. Int J Adhesion Adhesives 7:9–14

    Google Scholar 

  • Waite JH, Housley TJ, Tanzer ML (1985) Peptide repeats in a mussel glue protein: Theme and variations. Biochemistry 24:5010–5014

    Google Scholar 

  • Waite JH, Benedict CV (1984) Assay of dihydroxyphenylalanine in invertebrate structural proteins. Methods Enzymol 107:397–412

    Google Scholar 

  • Waite JH, Rice-Ficht AC (1987) Presclerotized eggshell protein from the liver flukeFasciola hepatica. Biochemistry 26:7819–7825

    Google Scholar 

  • Waite JH, Rice-Ficht AC (1989) A histidine-rich protein from the vitellaria of the liver flukeFasciola hepatica. Biochemistry 28:In press

  • Williams T, Marumo K, Waite JH, Henkens R (1989) Mussel glue protein has an open conformation. Arch Biochem Biophys 269:415–422

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Marine Biology/Biochemistry Program, College of Marine Studies, University of Delaware, 19958, Lewes, Delaware, USA

    J. Herbert Waite, Douglas C. Hansen & Kathleen T. Little

Authors
  1. J. Herbert Waite
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Douglas C. Hansen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kathleen T. Little
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Supported by grants from the National Science Foundation (DMB 8500301) and the Office of Naval Research (N00014-86K-0717)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Waite, J.H., Hansen, D.C. & Little, K.T. The glue protein of ribbed mussels (Geukensia demissa): a natural adhesive with some features of collagen. J Comp Physiol B 159, 517–525 (1989). https://doi.org/10.1007/BF00694376

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00694376

Key words

Search

Navigation