Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Tuning underwater adhesion with cation–π interactions

Nature Chemistry volume 9, pages 473–479 (2017)Cite this article

Subjects

An Erratum to this article was published on 23 June 2017

This article has been updated

Abstract

Cation–π interactions drive the self-assembly and cohesion of many biological molecules, including the adhesion proteins of several marine organisms. Although the origin of cation–π bonds in isolated pairs has been extensively studied, the energetics of cation–π-driven self-assembly in molecular films remains uncharted. Here we use nanoscale force measurements in combination with solid-state NMR spectroscopy to show that the cohesive properties of simple aromatic- and lysine-rich peptides rival those of the strong reversible intermolecular cohesion exhibited by adhesion proteins of marine mussel. In particular, we show that peptides incorporating the amino acid phenylalanine, a functional group that is conspicuously sparing in the sequences of mussel proteins, exhibit reversible adhesion interactions significantly exceeding that of analogous mussel-mimetic peptides. More broadly, we demonstrate that interfacial confinement fundamentally alters the energetics of cation–π-mediated assembly: an insight that should prove relevant for diverse areas, which range from rationalizing biological assembly to engineering peptide-based biomaterials.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Sequences and molecular structures of the peptides studied.
Figure 2: Schematic of the SFA set-up and illustration of the surface–peptide–surface interface studied.
Figure 3: Representative force–distance data measured for peptides between mica surfaces.
Figure 4: Solid-state 2D 13C{1H} HETCOR MAS NMR spectrum acquired from bulk Tyr peptide with a 1D 13C{1H} CP MAS NMR spectrum along the top horizontal axis and a single-pulse 1H MAS NMR spectrum along the left vertical axis.
Figure 5: Schematic that depicts the proposed mechanism of cation–π binding in aromatic- and Lys-rich peptide films, with many cation–aromatic binding pairs forming in close proximity.

Similar content being viewed by others

Change history

  • 08 June 2017

    In the version of this Article originally published, the accept date was incorrect and should have read ‘9 December 2016’. This has now been corrected in the online versions of the Article.

References

  1. Ma, J. C. & Dougherty, D. A. The cation–π interaction. Chem. Rev. 97, 1303–1324 (1997).

    Article  CAS  PubMed  Google Scholar 

  2. Gallivan, J. P. & Dougherty, D. A. Cation–π interactions in structural biology. Proc. Natl Acad. Sci. USA 96, 9459–9464 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Crowley, P. B. & Golovin, A. Cation–π interactions in protein–protein interfaces. Proteins. 59, 231–239 (2005).

    Article  CAS  PubMed  Google Scholar 

  4. Madahevi, A. S. & Sastry, G. N. Cation–π interaction: its role and relevance in chemistry, biology, and material science. Chem. Rev. 113, 2100–2138 (2013).

    Article  CAS  Google Scholar 

  5. Zhong, W. et al. From ab initio quantum mechanics to molecular neurobiology: a cation–π binding site in the nicotinic receptor. Proc. Natl Acad. Sci. USA 95, 12088–12093 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Khademi, S. et al. Mechanism of ammonia transport by Amt/MEP/Rh: structure of AmtB at 1.35 Å. Science. 305, 1587–1594 (2004).

    Article  CAS  PubMed  Google Scholar 

  7. Meyer, E. A., Castellano, R. K. & Diederich, F. Interactions with aromatic rings in chemical and biological recognition. Angew. Chem. Int. Ed. 42, 1211–1250 (2003).

    Google Scholar 

  8. Hwang, D. S., Zeng, H., Lu, Q., Israelachvili, J. N. & Waite, J. H. Adhesion mechanism in a DOPA-deficient foot protein from green mussels. Soft Matter 8, 5640–5648 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Lu, Q. et al. Nanomechanics of cation–π interactions in aqueous solutions. Angew. Chem. 125, 4036–4040 (2013).

    Article  Google Scholar 

  10. Kim, S. et al. Cation–π interaction in DOPA-deficient mussel adhesive protein mfp-1. J. Mater. Chem. B 3, 738–743 (2015).

    Article  CAS  PubMed  Google Scholar 

  11. Israelachvili, J. N. Intermolecular and Surface Forces Revised 3rd edn (Academic, 2011).

    Google Scholar 

  12. de Gennes, P. G. Soft adhesives. Langmuir 12, 4497–4500 (1996).

    Article  CAS  Google Scholar 

  13. Rose, S. et al. Nanoparticle solutions as adhesives for gels and biological tissues. Nature 505, 382–385 (2014).

    Article  CAS  PubMed  Google Scholar 

  14. Sunner, J., Nishizawa, K. & Kebarle, P. Ion–solvent molecule interactions in the gas phase. The potassium ion and benzene. J. Phys. Chem. 85, 1814–1820 (1981).

    Article  CAS  Google Scholar 

  15. Burley, S. K. & Petsko, G. A. Amino–aromatic interactions in proteins. FEBS Lett. 203, 139–143 (1986).

    Article  CAS  PubMed  Google Scholar 

  16. Deakyne, C. A. & Meot-Ner, M. Unconventional hydrogen bonds. 2. NH+–π complexes of onium ions with olefins and benzene derivatives. J. Am. Chem. Soc. 107, 474–479 (1985).

    Article  Google Scholar 

  17. Lee, B. P., Messersmith, P. B., Israelachvili, J. N. & Waite, J. H. Mussel-inspired adhesives and coatings. Annu. Rev. Mater. Res. 41, 99–132 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Wong Po Foo, C. T. S., Lee, J. S., Mulyasasmita, W., Parisi-Amon, A. & Heilshorn, S. C. Two-component protein-engineered physical hydrogels for cell encapsulation. Proc. Natl Acad. Sci. USA 106, 22067–22072 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  19. Norrby, P. & Liljefors, T. Strong decrease of the benzene–ammonium ion interaction upon complexation with a carboxylate anion. J. Am. Chem. Soc. 121, 2303–2306 (1999).

    Article  CAS  Google Scholar 

  20. Bartoli, S. & Roelens, S. Binding of acetylcholine and tetramethylammonium to a cyclophane receptor: anion's contribution to the cation–π interaction. J. Am. Chem. Soc. 124, 8307–8315 (2002).

    Article  CAS  PubMed  Google Scholar 

  21. Hunter, C. A., Low, C. M. R., Rotger, C., Vinter, J. G. & Cristiano, Z. The role of the counterion in the cation–π interaction. Chem. Commun. 834–835 (2003).

  22. Carrazana-García, J. A., Rodríguez-Otero, J. & Cabaleiro-Lago, E. M. A computational study of anion-modulated cation–π interactions. J. Phys. Chem. B 116, 5860–5871 (2012).

    Article  CAS  PubMed  Google Scholar 

  23. Carrazana-García, J. A., Cabaleiro-Lago, E. M., Campo-Caharrón, A. & Rodríguez-Otero, J. A theoretical study of ternary indole-cation-anion complexes. Org. Biomol. Chem. 12, 9145–9156 (2014).

    Article  CAS  PubMed  Google Scholar 

  24. Shao, H. & Stewart, R. J. Biomimetic underwater adhesives with environmentally triggered setting mechanisms. Adv. Mater. 22, 729–733 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Kamino, K., Nakano, M. & Kanai, S. Significance of the conformation of building blocks in curing of barnacle underwater adhesive. FEBS J. 279, 1750–1760 (2012).

    Article  CAS  PubMed  Google Scholar 

  26. Yamamoto, H. Synthesis and adhesive studies of marine polypeptides. J. Chem. Soc. Perkin Trans. 1 613–618 (1987).

  27. Yu, M. & Deming, T. J. Synthetic polypeptide mimics of marine adhesives. Macromolecules 31, 4739–4745 (1998).

    Article  CAS  PubMed  Google Scholar 

  28. Mattson, K. M. et al. A facile synthesis of catechol-functionalized poly(ethylene oxide) block and random copolymers. J. Polymer Sci. A 53, 2685–2692 (2015).

    CAS  Google Scholar 

  29. Lee, H., Dellatore, S. M., Miller, W. M. & Messersmith, P. B. Mussel-inspired surface chemistry for multifunctional coatings. Science 318, 426–430 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Wang, J. et al. Influence of binding-site density in wet bioadhesion. Adv. Mater. 20, 3872–3876 (2008).

    Article  CAS  Google Scholar 

  31. Wei, W. et al. Bridging adhesion of mussel-inspired peptides: role of charge, chain length, and surface type. Langmuir 31, 1105–1112 (2015).

    Article  CAS  PubMed  Google Scholar 

  32. Maier, G. P., Rapp, M. V., Waite, J. H., Israelachvili, J. N. & Butler, A. Adaptive synergy between catechol and lysine promotes wet adhesion by surface salt displacement. Science. 349, 628–632 (2015).

    Article  CAS  PubMed  Google Scholar 

  33. Danner, E. W., Kan, Y., Hammer, M. U., Israelachvili, J. N. & Waite, J. H. Adhesion of mussel foot protein mefp-5 to mica: an underwater superglue. Biochemistry 51, 6511–6518 (2012).

    Article  CAS  PubMed  Google Scholar 

  34. Luckham, P. F. & Klein, J. Forces between mica surfaces bearing adsorbed polyelectrolyte, poly-L-lysine, in aqueous media. J. Chem. Soc. Faraday Trans. 1 80, 865–878 (1984).

    Article  CAS  Google Scholar 

  35. Israelachvili, J. N. et al. Recent advances in the surface forces apparatus (SFA) technique. Rep. Prog. Phys. 73, 036601 (2010).

    Article  Google Scholar 

  36. Guo, C. & Holland, G. Investigating lysine adsorption on fumed silica nanoparticles. J. Phys. Chem. C 118, 25792–25801 (2014).

    Article  CAS  Google Scholar 

  37. De Vita, E. & Frydman, L. Spectral editing in 13C MAS NMR under moderately fast spinning conditions. J. Magn. Reson. 148, 327–337 (2001).

    Article  CAS  PubMed  Google Scholar 

  38. Ando, S. et al. Conformational characterization of glycine residues incorporated into some homopolypeptides by solid-state 13C NMR spectroscopy. J. Am. Chem. Soc. 107, 7648–7652 (1985).

    Article  CAS  Google Scholar 

  39. Selection of non-protonated carbon resonances in solid-state nuclear magnetic-resonance. J. Am. Chem. Soc. 101, 5854–5856 (1979).

  40. Gomes, J. & Mallion, R. Aromaticity and ring currents. Chem. Rev. 101, 1349–1383 (2001).

    Article  CAS  PubMed  Google Scholar 

  41. Sever, M. J., Weisser, J. T., Monahan, J., Srinivasan, S. & Wilker, J. J. Metal-mediated cross-linking in the generation of a marine mussel adhesive. Angew. Chem. Int. Ed. 43, 448–450 (2004).

    Article  Google Scholar 

  42. Holten-Andersen, N. et al. pH-induced metal–ligand cross-links inspired by mussel yield self-healing polymer networks with near-covalent elastic moduli. Proc. Natl Acad. Sci. USA 108, 2651–2655 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  43. Yu, M., Hwang, J. & Deming, T. J. Role of L-3-4-dihydroxyphenylalanine in mussel adhesive proteins. J. Am. Chem. Soc. 121, 5825–5826 (1999).

    Article  CAS  Google Scholar 

  44. Lee, H., Scherer, N. F. & Messersmith, P. B. Single-molecule mechanics of mussel adhesion. Proc. Natl Acad. Sci. USA 103, 12999–13003 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Martinez Rodriguez, N. R., Das, S., Kaufman, Y., Israelachvili, J. N. & Waite, J. H. Interfacial pH during mussel adhesive plaque formation. Biofouling 31, 221–227 (2015).

    Article  CAS  PubMed  Google Scholar 

  46. Liaqat, F. et al. High-performance TiO2 nanoparticle/DOPA polymer composites. Macromol. Rapid Commun. 36, 1129–1137 (2015).

    Article  CAS  PubMed  Google Scholar 

  47. Guardingo, M. et al. Bioinspired catechol-terminated self-assembled monolayers with enhanced adhesion properties. Small 10, 1594–1602 (2014).

    Article  CAS  PubMed  Google Scholar 

  48. Hediger, S., Meier, B. H., Kurur, N. D., Bodenhausen, G. & Ernst, R. R. NMR cross polarization by adiabatic passage through the Hartmann–Hahn condition (APHH). Chem. Phys. Lett. 223, 283–288 (1994).

    Article  CAS  Google Scholar 

  49. Elena, B., de Paëpe, G. & Emsley, L. Direct spectral optimisation of proton–proton homonuclear dipolar decoupling in solid-state NMR. Chem. Phys. Lett. 398, 532–538 (2004).

    Article  CAS  Google Scholar 

  50. Marion, D. & Wüthrich, K. Application of phase sensitive two-dimensional correlated spectroscopy (COSY) for measurements of 1H–1H spin-spin coupling constants in proteins. Biochem. Biophys. Res. Commun. 113, 967–974 (1983).

    Article  CAS  PubMed  Google Scholar 

  51. Fung, B. M., Khitrin, A. K. & Ermolaev, K. An improved broadband decoupling sequence for liquid crystals and solids. J. Magn. Reson. 142, 97–101 (2000).

    Article  CAS  PubMed  Google Scholar 

  52. Hayashi, S. & Hayamizu, K. Chemical shift standards in high-resolution solid-state NMR (1) 13C, 29Si, and 1H nuclei. Bull. Chem. Soc. Jpn 64, 685–687 (1991).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This research was supported by the Materials Research Science and Engineering Centers Program of the National Science Foundation under Award no. DMR 1121053. The authors acknowledge A. Griffin for assistance in characterizing the peptide adsorption.

Author information

Authors and Affiliations

  1. Materials Department, University of California, Santa Barbara, 93106, California, USA

    Matthew A. Gebbie, Thomas R. Cristiani & Jacob N. Israelachvili

  2. Materials Research Laboratory, University of California, Santa Barbara, 93106, California, USA

    Matthew A. Gebbie, Wei Wei, Alex M. Schrader, J. Herbert Waite & Jacob N. Israelachvili

  3. Department of Molecular, Cell and Developmental Biology, University of California, Santa Barbara, 93106, California, USA

    Alex M. Schrader & J. Herbert Waite

  4. Department of Chemical Engineering, University of California, Santa Barbara, 93106, California, USA

    Howard A. Dobbs, Matthew Idso, Bradley F. Chmelka & Jacob N. Israelachvili

Authors
  1. Matthew A. Gebbie
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Wei Wei
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Alex M. Schrader
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Thomas R. Cristiani
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Howard A. Dobbs
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Matthew Idso
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Bradley F. Chmelka
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. J. Herbert Waite
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Jacob N. Israelachvili
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

M.A.G. and W.W. contributed equally to this work. M.A.G., W.W., J.H.W. and J.N.I. conceived the research. M.A.G., A.M.S. and T.R.C. performed and analysed the force–distance measurements, W.W. synthesized and purified the peptides, M.A.G., H.A.D. and M.I. performed the NMR measurements, H.A.D., M.I. and B.F.C. analysed the NMR results, M.A.G. wrote the paper. All of the authors interpreted the data, discussed the results and commented on the manuscript.

Corresponding authors

Correspondence to J. Herbert Waite or Jacob N. Israelachvili.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary information

Supplementary information (PDF 1224 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gebbie, M., Wei, W., Schrader, A. et al. Tuning underwater adhesion with cation–π interactions. Nature Chem 9, 473–479 (2017). https://doi.org/10.1038/nchem.2720

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nchem.2720

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing