Journal of Biological Physics

, Volume 32, Issue 5, pp 393–401 | Cite as

Nanoscale Mechanical Characterisation of Amyloid Fibrils Discovered in a Natural Adhesive

  • Anika S. Mostaert
  • Michael J. Higgins
  • Takeshi Fukuma
  • Fabio Rindi
  • Suzanne P. Jarvis
Open Access
Research Paper

Abstract

Using the atomic force microscope, we have investigated the nanoscale mechanical response of the attachment adhesive of the terrestrial alga Prasiola linearis (Prasiolales, Chlorophyta). We were able to locate and extend highly ordered mechanical structures directly from the natural adhesive matrix of the living plant. The in vivo mechanical response of the structured biopolymer often displayed the repetitive sawtooth force-extension characteristics of a material exhibiting high mechanical strength at the molecular level. Mechanical and histological evidence leads us to propose a mechanism for mechanical strength in our sample based on amyloid fibrils. These proteinaceous, pleated β-sheet complexes are usually associated with neurodegenerative diseases. However, we now conclude that the amyloid protein quaternary structures detected in our material should be considered as a possible generic mechanism for mechanical strength in natural adhesives.

Key words

amyloid natural adhesive atomic force microscopy adhesion nanoscale mechanics force measurements extracellular polymeric substances algae biopolymer 

References

  1. 1.
    Fletcher, R., Callow, M.E.: Settlement, attachment and establishment of marine algal spores. Br. Phycol. J. 27, 303–329 (1992)CrossRefGoogle Scholar
  2. 2.
    Smith, B.L., Schäffer, T.E., Viani, M., Thompson, J.B., Frederick, N.A., Kindt, J., Belcher, A., Stucky, G.D., Morse, D.E., Hansma, P.K.: Molecular mechanistic origin of the toughness of natural adhesives, fibres and composites. Nature 399, 761–763 (1999)CrossRefADSGoogle Scholar
  3. 3.
    Bustamante, C., Marko, J.F., Siggia, E.D., Smith, S.: Entropic elasticity of λ-phage DNA. Science 265, 1599–1600 (1994)CrossRefADSGoogle Scholar
  4. 4.
    Rief, M., Gautel, M., Oesterhelt, F., Fernandez, J.M., Gaub, H.E.: Reversible unfolding of individual titin immunoglobulin domains by AFM. Science 276, 1109–1112 (1997)CrossRefGoogle Scholar
  5. 5.
    Tskhovrebova, L., Trinick, J., Sleep, J.A., Simmons, R.M.: Elasticity and unfolding of single molecules of the giant muscle protein titin. Nature 387, 308–312 (1997)CrossRefADSGoogle Scholar
  6. 6.
    Oberhauser, A.F., Marszalek, P.E., Erickson, H.P., Fernandez, J.M.: The molecular elasticity of the extracellular matrix protein tenascin. Nature 393, 181–185 (1998)CrossRefADSGoogle Scholar
  7. 7.
    Wetherbee, R., Lind, J.L., Burke, J., Quatrano, R.S.: The first kiss: establishment and control of initial adhesion by raphid diatoms. J. Phycol. 34, 9–15 (1998)CrossRefGoogle Scholar
  8. 8.
    Brockwell, D.J., Beddard, G.S., Paci, E., West, D.K., Olmsted, P.D., Smith, D.A., Radford, S.E.: Mechanically unfolding the small, topologically simple protein L. Biophys. J. 89, 506–519 (2005)CrossRefGoogle Scholar
  9. 9.
    Bemis, J.E., Akhremitchev, B.B., Walker, G.C.: Single polymer chain elongation by atomic force microscopy. Langmuir 15, 2799–2805 (1999)CrossRefGoogle Scholar
  10. 10.
    Waite, J.H., Qin, X.: Polyphosphoprotein from the adhesive pads of Mytilus edulis. Biochemistry 40, 2887–2893 (2001)CrossRefGoogle Scholar
  11. 11.
    Fukuma, T., Mostaert, A.S., Jarvis, S.P.: Explanation for the mechanical strength of amyloid fibrils. Tribol. Lett. (2006), dx.doi.org/10.1007/s11249-006-9086-8.
  12. 12.
    Bateman, A., Lachlan, C., Durbin, R., Finn, R.D., Volker, H., Griffiths-Jones, S., Khanna, A., Marshall, M., Moxon, S., Sonnhammer, E.L.L., Studholme, D.J., Yeats, C., Eddy, S.R.: The Pfam protein families database. Nucleic Acids Res. (Database issue) 32, D138–D141 (2004)CrossRefGoogle Scholar
  13. 13.
    Dobson, C.M.: Protein folding and misfolding. Nature 426, 884–890 (2003)CrossRefADSGoogle Scholar
  14. 14.
    Vowles, G.H., Francis, R.J.: Amyloid. In: Bancroft, J.D., Gamble, M. (eds.) Theory and Practice of Histological Techniques, 5th ed., pp. 303–324. Churchill Livingstone, Harcourt, London, UK (2002)Google Scholar
  15. 15.
    Sipe, J.D.: Amyloid Proteins: The Beta Sheet Conformation and Disease. Wiley, Weinheim, Germany (2005)Google Scholar
  16. 16.
    Baxa, U., Speransky, V., Stevens, A.C., Wickner, R.B.: Mechanism of inactivation on prion conversion of the Saccharomyces cerevisiae Ure2 protein. Proc. Natl Acad. Sci. U.S.A. 99, 5253–5260 (2002)CrossRefADSGoogle Scholar
  17. 17.
    Fowler, D.M., Koulov, A.V., Alory-Jost, C., Marks, M.S., Balch, W.E., Kelly, J.W.: Functional Amyloid formation within mammalian tissue. PLoS Biol. 4, 100–107 (2006)CrossRefGoogle Scholar
  18. 18.
    Guiry, M.D., Cunningham, E.M.: Photoperiodic and temperature responses in the reproduction of north-eastern Atlantic Gigartina acicularis (Rhodophyta: Gigartinales). Phycologia 23, 357–367 (1984)Google Scholar
  19. 19.
    Sader, J.E., Chon, J.W.M., Mulvaney, P.: Calibration of rectangular atomic force microscope cantilevers. Rev. Sci. Instrum. 70, 3967–3969 (1999)CrossRefADSGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2006

Authors and Affiliations

  • Anika S. Mostaert
    • 1
  • Michael J. Higgins
    • 1
  • Takeshi Fukuma
    • 1
  • Fabio Rindi
    • 2
  • Suzanne P. Jarvis
    • 1
  1. 1.Centre for Research on Adaptive Nanostructures and NanodevicesTrinity College DublinDublin 2Ireland
  2. 2.Department of Botany, Martin Ryan InstituteNational University of IrelandGalwayIreland

Personalised recommendations