CoChat
Sign Up
Cited by 1,597Polymer Surface Interaction StudiesHydrogels: synthesis, properties, applicationsSupramolecular Self-Assembly in Materials

Ph-induced metal-ligand cross-links inspired by mussel yield self-healing polymer networks with near-covalent elastic moduli

Open access
Holten-Andersen, Niels, Harrington, Matthew J., Birkedal, Henrik, Lee, Bruce P., Messersmith, Phillip B., Lee, Ka Yee C., Waite, J. Herbert·2011·Proceedings of the National Academy of Sciences
DOI 10.1073/pnas.1015862108PMC PMC3041094
Open this paper in CoChat — free account

Abstract

Growing evidence supports a critical role of metal-ligand coordination in many attributes of biological materials including adhesion, self-assembly, toughness, and hardness without mineralization [Rubin DJ, Miserez A, Waite JH (2010) Advances in Insect Physiology: Insect Integument and Color , eds Jérôme C, Stephen JS (Academic Press, London), pp 75–133]. Coordination between Fe and catechol ligands has recently been correlated to the hardness and high extensibility of the cuticle of mussel byssal threads and proposed to endow self-healing properties [Harrington MJ, Masic A, Holten-Andersen N, Waite JH, Fratzl P (2010) Science 328:216–220]. Inspired by the pH jump experienced by proteins during maturation of a mussel byssus secretion, we have developed a simple method to control catechol-Fe 3+ interpolymer cross-linking via pH. The resonance Raman signature of catechol-Fe 3+ cross-linked polymer gels at high pH was similar to that from native mussel thread cuticle and the gels displayed elastic moduli (G′) that approach covalently cross-linked gels as well as self-healing properties.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1073/pnas.1015862108

Cites

1 of 1 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 32

  1. [1]Holten-Andersen N, Fantner GE, Hohlbauch S, Waite JH, Zok FW. Protective coatings on extensible biofibres. Nat Mater. 2007;6:669–672. doi: 10.1038/nmat1956. [DOI] [PubMed] [Google Scholar] · DOI
  2. [2]Rubin DJ, Miserez A, Waite JH. In: Advances in insect physiology: insect integument and color. Jérôme C, Stephen JS, editors. London: Academic Press; 2010. pp. 75–133. [Google Scholar]
  3. [3]Holten-Andersen N, Zhao H, Waite JH. Stiff coatings on compliant biofibers: the cuticle of Mytilus californianus byssal threads. Biochemistry. 2009;48:2752–2759. doi: 10.1021/bi900018m. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  4. [4]Harrington MJ, Masic A, Holten-Andersen N, Waite JH, Fratzl P. Iron-clad fibers: a metal-based biological strategy for hard flexible coatings. Science. 2010;328:216–220. doi: 10.1126/science.1181044. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI · Paper page
  5. [5]Zeng H, Hwang DS, Israelachvili JN, Waite JH. Strong reversible Fe3+-mediated bridging between dopa-containing protein films in water. Proc Natl Acad Sci USA. 2010;107:12850–12853. doi: 10.1073/pnas.1007416107. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI · Paper page
  6. [7]Taylor SW, Chase DB, Emptage MH, Nelson MJ, Waite JH. Ferric ion complexes of a dopa-containing adhesive protein from Mytilus edulis. Inorg Chem. 1996;35:7572–7577. [Google Scholar]
  7. [8]Taylor SW, Luther GW, Waite JH. Polarographic and spectrophotometric investigation of iron(iii) complexation to 3,4-Dihydroxyphenylalanine-containing peptides and proteins from Mytilus-Edulis. Inorg Chem. 1994;33:5819–5824. [Google Scholar]
  8. [9]Sever MJ, Weisser JT, Monahan J, Srinivasan S, Wilker JJ. Metal-mediated cross-linking in the generation of a marine-mussel adhesive. Angewandte Chemie International Edition. 2004;43:448–450. doi: 10.1002/anie.200352759. [DOI] [PubMed] [Google Scholar] · DOI · Paper page
  9. [10]Avdeef A, Sofen SR, Bregante TL, Raymond KN. Coordination chemistry of microbial iron transport compounds. 9. Stability constants for catechol models of enterobactin. J Am Chem Soc. 1978;100:5362–5370. [Google Scholar]
  10. [11]Lee H, Scherer NF, Messersmith PB. Single-molecule mechanics of mussel adhesion. Proc Natl Acad Sci USA. 2006;103:12999–13003. doi: 10.1073/pnas.0605552103. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI · Paper page
  11. [12]Butler A. Acquisition and utilization of transition metal ions by marine organisms. Science. 1998;281:207–209. doi: 10.1126/science.281.5374.207. [DOI] [PubMed] [Google Scholar] · DOI
  12. [13]Loizou E, et al. Structural effects of cross-linking a biopolymer hydrogel derived from marine mussel adhesive protein. Macromol Biosci. 2006;6:711–718. doi: 10.1002/mabi.200600097. [DOI] [PubMed] [Google Scholar] · DOI
  13. [14]Hwang DS, et al. Protein- and metal-dependent interactions of a prominent protein in mussel adhesive plaques. J Biol Chem. 2010;285:25850–25858. doi: 10.1074/jbc.M110.133157. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  14. [15]Zuccarello LV. Ultrastructural and cytochemical study on the enzyme gland of the foot of a mollusc. Tissue Cell. 1981;13:701–713. doi: 10.1016/s0040-8166(81)80007-9. [DOI] [PubMed] [Google Scholar] · DOI
  15. [16]Zhao H, Waite JH. Linking adhesive and structural proteins in the attachment plaque of Mytilus californianus. J Biol Chem. 2006;281:26150–26158. doi: 10.1074/jbc.M604357200. [DOI] [PubMed] [Google Scholar] · DOI
  16. [17]Sever MJ, Wilker JJ. Absorption spectroscopy and binding constants for first-row transition metal complexes of a dopa-containing peptide. Dalton Transactions. 2006;6:813–822. doi: 10.1039/b509586g. [DOI] [PubMed] [Google Scholar] · DOI
  17. [18]Michaud-Soret I, et al. Resonance Raman studies of catecholate and phenolate complexes of recombinant human tyrosine hydroxylase. Biochemistry. 1995;34:5504–5510. doi: 10.1021/bi00016a022. [DOI] [PubMed] [Google Scholar] · DOI
  18. [19]Lee BP, Dalsin JL, Messersmith PB. Synthesis and gelation of dopa-modified poly(ethylene glycol) hydrogels. Biomacromolecules. 2002;3:1038–1047. doi: 10.1021/bm025546n. [DOI] [PubMed] [Google Scholar] · DOI
  19. [20]Roberts MC, Hanson MC, Massey AP, Karren EA, Kiser PF. Dynamically restructuring hydrogel networks formed with reversible covalent crosslinks. Adv Mater. 2007;19:2503–2507. [Google Scholar]
  20. [21]Lieleg O, Claessens MMAE, Luan Y, Bausch AR. Transient binding and dissipation in cross-linked actin networks. Phys Rev Lett. 2008;101:108101. doi: 10.1103/PhysRevLett.101.108101. [DOI] [PubMed] [Google Scholar] · DOI
  21. [22]Ewoldt RH, Clasen C, Hosoi AE, McKinley GH. Rheological fingerprinting of gastropod pedal mucus and synthetic complex fluids for biomimicking adhesive locomotion. Soft Matter. 2007;3:634–643. doi: 10.1039/b615546d. [DOI] [PubMed] [Google Scholar] · DOI
  22. [23]Skrzeszewska PJ, et al. Fracture and self-healing in a well-defined self-assembled polymer network. Macromolecules. 2010;43:3542–3548. [Google Scholar]
  23. [24]Shao H, Stewart RJ. Biomimetic underwater adhesives with environmentally triggered setting mechanisms. Adv Mater. 2010;22:729–733. doi: 10.1002/adma.200902380. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  24. [25]Pezron E, et al. Reversible gel formation induced by ion complexation. 1. Borax-galactomannan interactions. Macromolecules. 1988;21:1121–1125. [Google Scholar]
  25. [26]Kushner AM, et al. A biomimetic modular polymer with tough and adaptive properties. J Am Chem Soc. 2009;131:8766–8768. doi: 10.1021/ja9009666. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  26. [27]Serero Y, et al. Associating polymers: from “flowers” to transient networks. Phys Rev Lett. 1998;81:5584–5587. [Google Scholar]
  27. [28]Kersey FR, Loveless DM, Craig SL. A hybrid polymer gel with controlled rates of cross-link rupture and self-repair. J R Soc Interface. 2007;4:373–380. doi: 10.1098/rsif.2006.0187. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  28. [29]Lee H, Lee BP, Messersmith PB. A reversible wet/dry adhesive inspired by mussels and geckos. Nature. 2007;448:338–341. doi: 10.1038/nature05968. [DOI] [PubMed] [Google Scholar] · DOI · Paper page
  29. [30]Lee H, Dellatore SM, Miller WM, Messersmith PB. Mussel-inspired surface chemistry for multifunctional coatings. Science. 2007;318:426–430. doi: 10.1126/science.1147241. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI · Paper page
  30. [31]Crisponi G, Nurchi VM, Pivetta T. Potentiometric and spectrophotometric equilibrium study on Fe(III) and new catechol-bisphosphonate conjugates. J Inorg Biochem. 2008;102:209–215. doi: 10.1016/j.jinorgbio.2007.07.038. [DOI] [PubMed] [Google Scholar] · DOI
  31. [32]Andersson KK, Cox DD, Que L, Flatmark T, Haavik J. Resonance Raman studies on the blue-green-colored bovine adrenal tyrosine 3-monooxygenase (tyrosine hydroxylase). Evidence that the feedback inhibitors adrenaline and noradrenaline are coordinated to iron. J Biol Chem. 1988;263:18621–18626. [PubMed] [Google Scholar]
  32. [33]Andersson KK, et al. Purification and characterization of the blue green rat pheochromocytoma-(PC12) tyrosine-hydroxylase with a dopamine-Fe(III) complex—reversal of the endogenous feedback inhibition by phosphorylation of serine-40. Biochem J. 1992;284:687–695. doi: 10.1042/bj2840687. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI

Cited by

Sorted by citations

Authors
Holten-Andersen, N., Harrington, M. J., Birkedal, H., Lee, B. P., Messersmith, P. B., Lee, K. Y. C., & Waite, J. H.
Affiliations
  • Department of Chemistry, Institute for Biophysical Dynamics, and the James Franck Institute, University of Chicago, Chicago, IL 60637;
  • Max Planck Society (DE)
  • Aarhus University (DK)
  • Northwestern University (US)
  • University of Chicago (US)
  • University of California, Santa Barbara (US)
ORCID
Venue
Proceedings of the National Academy of Sciences
Publisher
National Academy of Sciences
Published
2011-01-28
Volume
108
Issue
7
Pages
2651-2655
ISSN
  • 0027-8424 (ISSN-L)
  • 1091-6490
DOI
10.1073/pnas.1015862108
PMC
PMC3041094
OpenAlex
W2037432389
Cited by
1,597
References
1
Citations by year
2026: 86 · 2025: 96 · 2024: 98 · 2023: 107 · 2022: 115 · 2021: 157 · 2020: 135 · 2019: 141 · 2018: 132 · 2017: 111 · 2016: 108 · 2015: 109 · 2014: 91 · 2013: 56 · 2012: 47
FWCI
29.86
Type
journal article
Language
en
Open access
Locations
  • Proceedings of the National Academy of Sciences (publishedVersion)
  • Europe PMC (PubMed Central) (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
  • Max Planck Institute for Plasma Physics (submittedVersion)
  • Max Planck Digital Library (submittedVersion)
  • MPG.PuRe (Max Planck Society) (submittedVersion)
Funders
National Institute of Dental and Craniofacial Research (R01DE018468, RC1DE020702, R37DE014193)
Topics
  • Physical Sciences › Materials Science › Surfaces, Coatings and Films › Polymer Surface Interaction Studies
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Medicine › Hydrogels: synthesis, properties, applications
  • Physical Sciences › Materials Science › Biomaterials › Supramolecular Self-Assembly in Materials
Keywords
self-healing polymers, elastic modulus, polymer gels, biomimetic materials, resonance Raman spectroscopy, biomineralization
MeSH terms
Animals, Catechols, Chromatography, Gel, Cross-Linking Reagents, Gels, Hydrogen-Ion Concentration, Iron, Polymers, Rheology, Spectrum Analysis, Raman, Bivalvia, Elastic Modulus

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review