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SCIENCE CHINA Technological Sciences, Volume 63 , Issue 9 : 1675-1698(2020) https://doi.org/10.1007/s11431-019-1541-8

Inter- and intramolecular adhesion mechanisms of mussel foot proteins

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  • ReceivedNov 9, 2019
  • AcceptedFeb 18, 2020
  • PublishedMay 21, 2020

Abstract

Mussel foot proteins (Mfps) secreted in the byssal plaque of marine mussels are widely researched for their relevance to mussel adhesion in water. As the abundant residue in the amino acid sequences of major adhesive proteins, 3,4-dihydroxyphenylalanine (Dopa) or its catecholic moiety plays a key role in both Mfp binding to surface and cohesive cross-linking of Mfps in byssal plaques. The binding performance of an Mfp significantly depends on the content and redox state of Dopa, whereas the types of interaction vary in line with different surface chemistries and pH conditions. Thorough understanding of mussel adhesion from a molecular perspective is crucial to promote the application of synthetic mussel-bionic adhesives. This article presents a brief review of the research progress on the adhesion mechanisms of Mfps, which further emphasizes the contributions of Dopa-mediated interactions and considers other amino acids and factors. The involved inter- and intramolecular interactions are responsible for not only the diverse adhesion capacities of an adhesive byssal plaque as mussel’s adhesion precursor but also the formation and properties of the plaque structure.


Funded by

the National Natural Science Foundation of China(Grant,No.,51605090)

the Natural Science Foundation of Jiangsu Province(Grant,Nos.,BK20160670,BK20160776)

and the Fundamental Research Funds for the Central Universities(Grant,No.,2242019k1G011)


Acknowledgment

This work was supported by the National Natural Science Foundation of China (Grant No. 51605090), the Natural Science Foundation of Jiangsu Province (Grant Nos. BK20160670 and BK20160776), and the Fundamental Research Funds for the Central Universities (Grant No. 2242019k1G011).


References

[1] Israelachvili J N. Intermolecular and Surface Forces. San Diego: Academic Press, 2011. Google Scholar

[2] Bell E, Gosline J. Mechanical design of mussel byssus: Material yield enhances attachment strength. J Exp Biol, 1996, 199: 1005–1017. Google Scholar

[3] Ackerman J D, Cottrell C M, Ethier C R, et al. Attachment strength of zebra mussels on natural, polymeric, and metallic materials. J Environ Eng, 1996, 122: 141-148 CrossRef Google Scholar

[4] Wilker J J. Marine bioinorganic materials: Mussels pumping iron. Curr Opin Chem Biol, 2010, 14: 276-283 CrossRef PubMed Google Scholar

[5] Waite J H, Tanzer M L. Polyphenolic substance of mytilus edulis: Novel adhesive containing l-dopa and hydroxyproline. Science, 1981, 212: 1038-1040 CrossRef PubMed ADS Google Scholar

[6] Waite J H. Evidence for a repeating 3,4-dihydroxyphenylalanine- and hydroxyproline-containing decapeptide in the adhesive protein of the mussel, mytilus edulis L. J Biol Chem, 1983, 258: 2911–2915. Google Scholar

[7] DeMartini D G, Errico J M, Sjoestroem S, et al. A cohort of new adhesive proteins identified from transcriptomic analysis of mussel foot glands. J R Soc Interface, 2017, 14: 20170151 CrossRef PubMed Google Scholar

[8] Rees D J, Hanifi A, Obille A, et al. Fingerprinting of proteins that mediate quagga mussel adhesion using a de novo assembled foot transcriptome. Sci Rep, 2019, 9: 6305 CrossRef PubMed ADS Google Scholar

[9] Waite J H. Mussel adhesion—essential footwork. J Exp Biol, 2017, 220: 517-530 CrossRef PubMed Google Scholar

[10] Yu M, Hwang J, Deming T J. Role of l-3,4-dihydroxyphenylalanine in mussel adhesive proteins. J Am Chem Soc, 1999, 121: 5825-5826 CrossRef Google Scholar

[11] Li Y, Qin M, Li Y, et al. Single molecule evidence for the adaptive binding of dopa to different wet surfaces. Langmuir, 2014, 30: 4358-4366 CrossRef PubMed Google Scholar

[12] Zhang W, Yang H, Liu F, et al. Molecular interactions between dopa and surfaces with different functional groups: A chemical force microscopy study. RSC Adv, 2017, 7: 32518-32527 CrossRef Google Scholar

[13] Yu J, Kan Y, Rapp M, et al. Adaptive hydrophobic and hydrophilic interactions of mussel foot proteins with organic thin films. Proc Natl Acad Sci USA, 2013, 110: 15680-15685 CrossRef PubMed ADS Google Scholar

[14] Wei W, Petrone L, Tan Y P, et al. An underwater surface-drying peptide inspired by a mussel adhesive protein. Adv Funct Mater, 2016, 26: 3496-3507 CrossRef PubMed Google Scholar

[15] Utzig T, Stock P, Valtiner M. Resolving non-specific and specific adhesive interactions of catechols at solid/liquid interfaces at the molecular scale. Angew Chem Int Ed, 2016, 55: 9524-9528 CrossRef PubMed Google Scholar

[16] Lee H, Scherer N F, Messersmith P B. Single-molecule mechanics of mussel adhesion. Proc Natl Acad Sci USA, 2006, 103: 12999-13003 CrossRef PubMed ADS Google Scholar

[17] Wang J, Tahir M N, Kappl M, et al. Influence of binding-site density in wet bioadhesion. Adv Mater, 2008, 20: 3872-3876 CrossRef Google Scholar

[18] Anderson T H, Yu J, Estrada A, et al. The contribution of DOPA to substrate-peptide adhesion and internal cohesion of mussel-inspired synthetic peptide films. Adv Funct Mater, 2010, 20: 4196-4205 CrossRef PubMed Google Scholar

[19] Zhang W, Yang F K, Pan Z, et al. Bio-inspired dopamine functionalization of polypyrrole for improved adhesion and conductivity. Macromol Rapid Commun, 2014, 35: 350-354 CrossRef PubMed Google Scholar

[20] Das P, Reches M. Revealing the role of catechol moieties in the interactions between peptides and inorganic surfaces. Nanoscale, 2016, 8: 15309-15316 CrossRef PubMed Google Scholar

[21] Zhong C, Gurry T, Cheng A A, et al. Strong underwater adhesives made by self-assembling multi-protein nanofibres. Nat Nanotech, 2014, 9: 858-866 CrossRef PubMed ADS Google Scholar

[22] Saiz-Poseu J, Mancebo-Aracil J, Nador F, et al. The chemistry behind catechol-based adhesion. Angew Chem Int Ed, 2019, 58: 696-714 CrossRef PubMed Google Scholar

[23] Lee H, Dellatore S M, Miller W M, et al. Mussel-inspired surface chemistry for multifunctional coatings. Science, 2007, 318: 426-430 CrossRef PubMed ADS Google Scholar

[24] Fant C, Sott K, Elwing H, et al. Adsorption behavior and enzymatically or chemically induced cross‐linking of a mussel adhesive protein. Biofouling, 2000, 16: 119-132 CrossRef Google Scholar

[25] Höök F, Kasemo B, Nylander T, et al. Variations in coupled water,viscoelastic properties,and film thickness of a mefp-1 protein film during adsorption and cross-linking: A quartz crystal microbalance with dissipation monitoring,ellipsometry,and surface plasmon resonance study. Anal Chem, 2001, 73: 5796-5804 CrossRef PubMed Google Scholar

[26] Baty A M, Leavitt P K, Siedlecki C A, et al. Adsorption of adhesive proteins from the marine mussel, Mytilus edulis, on polymer films in the hydrated state using angle dependent X-ray photoelectron spectroscopy and atomic force microscopy. Langmuir, 1997, 13: 5702-5710 CrossRef Google Scholar

[27] Baty A M, Suci P A, Tyler B J, et al. Investigation of mussel adhesive protein adsorption on polystyrene and poly(octadecyl methacrylate) using angle dependent XPS, ATR-FTIR, and AFM. J Colloid Interface Sci, 1996, 177: 307-315 CrossRef ADS Google Scholar

[28] Suci P A, Geesey G G. Influence of sodium periodate and tyrosinase on binding of alginate to adlayers of mytilus edulis foot protein 1. J Colloid Interface Sci, 2000, 230: 340-348 CrossRef PubMed ADS Google Scholar

[29] Fant C, Hedlund J, Höök F, et al. Investigation of adsorption and cross-linking of a mussel adhesive protein using attenuated total internal reflection fourier transform infrared spectroscopy (atr-ftir). J Adhes, 2010, 86: 25-38 CrossRef Google Scholar

[30] Wei W, Yu J, Broomell C, et al. Hydrophobic enhancement of dopa-mediated adhesion in a mussel foot protein. J Am Chem Soc, 2013, 135: 377-383 CrossRef PubMed Google Scholar

[31] Mudunkotuwa I A, Minshid A A, Grassian V H. ATR-FTIR spectroscopy as a tool to probe surface adsorption on nanoparticles at the liquid-solid interface in environmentally and biologically relevant media. Analyst, 2014, 139: 870-881 CrossRef PubMed ADS Google Scholar

[32] Onyido I, Norris A R, Buncel E. Biomolecule-mercury interactions:  Modalities of DNA base-mercury binding mechanisms. Remediation strategies. Chem Rev, 2004, 104: 5911-5930 CrossRef PubMed Google Scholar

[33] Hong S, Chen T, Zhu Y, et al. Live-cell stimulated raman scattering imaging of alkyne-tagged biomolecules. Angew Chem Int Ed, 2014, 53: 5827-5831 CrossRef PubMed Google Scholar

[34] Hwang D S, Harrington M J, Lu Q, et al. Mussel foot protein-1 (mcfp-1) interaction with titania surfaces. J Mater Chem, 2012, 22: 15530-15533 CrossRef PubMed Google Scholar

[35] Yu J, Wei W, Menyo M S, et al. Adhesion of mussel foot protein-3 to TiO2 surfaces: The effect of pH. Biomacromolecules, 2013, 14: 1072-1077 CrossRef PubMed Google Scholar

[36] Harrington M J, Masic A, Holten-Andersen N, et al. Iron-clad fibers: A metal-based biological strategy for hard flexible coatings. Science, 2010, 328: 216-220 CrossRef PubMed ADS Google Scholar

[37] Willets K A, van Duyne R P. Localized surface plasmon resonance spectroscopy and sensing. Annu Rev Phys Chem, 2007, 58: 267-297 CrossRef ADS Google Scholar

[38] Nie S. Probing single molecules and single nanoparticles by surface-enhanced raman scattering. Science, 1997, 275: 1102-1106 CrossRef Google Scholar

[39] Akemi Ooka A, Garrell R L. Surface-enhanced Raman spectroscopy of DOPA-containing peptides related to adhesive protein of marine mussel, Mytilus edulis. Biopolymers, 2000, 57: 92-102 CrossRef Google Scholar

[40] Lee N, Hummer D R, Sverjensky D A, et al. Speciation of l-DOPA on nanorutile as a function of pH and surface coverage using surface-enhanced Raman spectroscopy (SERS). Langmuir, 2012, 28: 17322-17330 CrossRef PubMed Google Scholar

[41] Waite J H. Adhesion à la moule. Integrative Comp Biol, 2002, 42: 1172-1180 CrossRef PubMed Google Scholar

[42] Hansen D C, Corcoran S G, Waite J H. Enzymatic tempering of a mussel adhesive protein film. Langmuir, 1998, 14: 1139-1147 CrossRef Google Scholar

[43] Engel A, Müller D J. Observing single biomolecules at work with the atomic force microscope. Nat Struct Biol, 2000, 7: 715-718 CrossRef PubMed Google Scholar

[44] Neuman K C, Nagy A. Single-molecule force spectroscopy: Optical tweezers, magnetic tweezers and atomic force microscopy. Nat Methods, 2008, 5: 491-505 CrossRef PubMed Google Scholar

[45] Frank B P, Belfort G. Adhesion of mytilus edulis foot protein 1 on silica: Ionic effects on biofouling. Biotechnol Prog, 2002, 18: 580-586 CrossRef PubMed Google Scholar

[46] Hwang D S, Yoo H J, Jun J H, et al. Expression of functional recombinant mussel adhesive protein mgfp-5 in escherichia coli. Appl Environ MicroBiol, 2004, 70: 3352-3359 CrossRef PubMed Google Scholar

[47] Li Y, Cao Y. The molecular mechanisms underlying mussel adhesion. Nanoscale Adv, 2019, 1: 4246-4257 CrossRef ADS Google Scholar

[48] Butt H J, Cappella B, Kappl M. Force measurements with the atomic force microscope: Technique, interpretation and applications. Surf Sci Rep, 2005, 59: 1-152 CrossRef ADS Google Scholar

[49] Tabor D, Winterton R H S. The direct measurement of normal and retarded van der Waals forces. Proc R Soc Lond A, 1969, 312: 435-450 CrossRef ADS Google Scholar

[50] Oh D X, Shin S, Yoo H Y, et al. Surface forces apparatus and its applications for nanomechanics of underwater adhesives. Korean J Chem Eng, 2014, 31: 1306-1315 CrossRef Google Scholar

[51] Chough S K, Lee H J, Yoon S H. Marine Geology of Korean Seas. Elsevier, 2000. Google Scholar

[52] Si W, Zhang Y, Wu G, et al. DNA sequencing technology based on nanopore sensors by theoretical calculations and simulations. Chin Sci Bull, 2014, 59: 4929-4941 CrossRef ADS Google Scholar

[53] Petrone L, Kumar A, Sutanto C N, et al. Mussel adhesion is dictated by time-regulated secretion and molecular conformation of mussel adhesive proteins. Nat Commun, 2015, 6: 8737 CrossRef PubMed ADS Google Scholar

[54] Levine Z A, Rapp M V, Wei W, et al. Surface force measurements and simulations of mussel-derived peptide adhesives on wet organic surfaces. Proc Natl Acad Sci USA, 2016, 113: 4332-4337 CrossRef PubMed ADS Google Scholar

[55] He C, Zhang H, Lin C, et al. A molecular dynamics study on the adsorption of a mussel protein on two different films: Polymer film and a sam. Chem Phys Lett, 2017, 676: 144-149 CrossRef ADS Google Scholar

[56] Mian S A, Yang L M, Saha L C, et al. A fundamental understanding of catechol and water adsorption on a hydrophilic silica surface: Exploring the underwater adhesion mechanism of mussels on an atomic scale. Langmuir, 2014, 30: 6906-6914 CrossRef PubMed Google Scholar

[57] Li Y, Liao M, Zhou J. Catechol-cation adhesion on silica surfaces: Molecular dynamics simulations. Phys Chem Chem Phys, 2017, 19: 29222-29231 CrossRef PubMed ADS Google Scholar

[58] Li Y, Liao M, Zhou J. Catechol and its derivatives adhesion on graphene: Insights from molecular dynamics simulations. J Phys Chem C, 2018, 122: 22965-22974 CrossRef Google Scholar

[59] Li S C, Chu L N, Gong X Q, et al. Hydrogen bonding controls the dynamics of catechol adsorbed on a TiO2(110) surface. Science, 2010, 328: 882-884 CrossRef PubMed ADS Google Scholar

[60] Leng C, Liu Y, Jenkins C, et al. Interfacial structure of a dopa-inspired adhesive polymer studied by sum frequency generation vibrational spectroscopy. Langmuir, 2013, 29: 6659-6664 CrossRef PubMed Google Scholar

[61] Mian S A, Saha L C, Jang J, et al. Density functional theory study of catechol adhesion on silica surfaces. J Phys Chem C, 2010, 114: 20793-20800 CrossRef Google Scholar

[62] Mian S A, Gao X, Nagase S, et al. Adsorption of catechol on a wet silica surface: Density functional theory study. Theor Chem Acc, 2011, 130: 333-339 CrossRef Google Scholar

[63] Mian S A, Khan Y. The adhesion mechanism of marine mussel foot protein: Adsorption of L-Dopa on α- and β-cristobalite silica using density functional theory. J Chem, 2017, 2017: 1-6 CrossRef Google Scholar

[64] Qin Z, Buehler M. Molecular mechanics of dihydroxyphenylalanine at a silica interface. Appl Phys Lett, 2012, 101: 083702 CrossRef ADS Google Scholar

[65] Lee B P, Messersmith P B, Israelachvili J N, et al. Mussel-inspired adhesives and coatings. Annu Rev Mater Res, 2011, 41: 99-132 CrossRef PubMed ADS Google Scholar

[66] Lin Q, Gourdon D, Sun C, et al. Adhesion mechanisms of the mussel foot proteins mfp-1 and mfp-3. Proc Natl Acad Sci USA, 2007, 104: 3782-3786 CrossRef PubMed ADS Google Scholar

[67] Yu J, Wei W, Danner E, et al. Effects of interfacial redox in mussel adhesive protein films on mica. Adv Mater, 2011, 23: 2362-2366 CrossRef PubMed Google Scholar

[68] Danner E W, Kan Y, Hammer M U, et al. Adhesion of mussel foot protein mefp-5 to mica: An underwater superglue. Biochemistry, 2012, 51: 6511-6518 CrossRef PubMed Google Scholar

[69] Lu Q, Danner E, Waite J H, et al. Adhesion of mussel foot proteins to different substrate surfaces. J R Soc Interface, 2013, 10: 20120759 CrossRef PubMed Google Scholar

[70] Papov V V, Diamond T V, Biemann K, et al. Hydroxyarginine-containing polyphenolic proteins in the adhesive plaques of the marine mussel Mytilus edulis. J Biol Chem, 1995, 270: 20183-20192 CrossRef PubMed Google Scholar

[71] Ahn B K, Lee D W, Israelachvili J N, et al. Surface-initiated self-healing of polymers in aqueous media. Nat Mater, 2014, 13: 867-872 CrossRef PubMed ADS Google Scholar

[72] Maier G P, Rapp M V, Waite J H, et al. Adaptive synergy between catechol and lysine promotes wet adhesion by surface salt displacement. Science, 2015, 349: 628-632 CrossRef PubMed ADS Google Scholar

[73] Rapp M V, Maier G P, Dobbs H A, et al. Defining the catechol-cation synergy for enhanced wet adhesion to mineral surfaces. J Am Chem Soc, 2016, 138: 9013-9016 CrossRef PubMed Google Scholar

[74] Li Y, Wang T, Xia L, et al. Single-molecule study of the synergistic effects of positive charges and dopa for wet adhesion. J Mater Chem B, 2017, 5: 4416-4420 CrossRef Google Scholar

[75] Sever M J, Weisser J T, Monahan J, et al. Metal-mediated cross-linking in the generation of a marine-mussel adhesive. Angew Chem Int Ed, 2004, 43: 448-450 CrossRef PubMed Google Scholar

[76] Holten-Andersen N, Mates T E, Toprak M S, et al. Metals and the integrity of a biological coating: The cuticle of mussel byssus. Langmuir, 2009, 25: 3323-3326 CrossRef PubMed Google Scholar

[77] Li S, Xia Z, Chen Y, et al. Byssus structure and protein composition in the highly invasive fouling mussel limnoperna fortunei. Front Physiol, 2018, 9: 418 CrossRef Google Scholar

[78] Taylor S W, Luther G W, Waite J H. 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 CrossRef Google Scholar

[79] Dalsin J L, Lin L, Tosatti S, et al. Protein resistance of titanium oxide surfaces modified by biologically inspired mpeg-dopa. Langmuir, 2005, 21: 640-646 CrossRef PubMed Google Scholar

[80] Janković I A, Šaponjić Z V, Čomor M I, et al. Surface modification of colloidal TiO2 nanoparticles with bidentate benzene derivatives. J Phys Chem C, 2009, 113: 12645-12652 CrossRef Google Scholar

[81] Holten-Andersen N, Jaishankar A, Harrington M J, et al. Metal-coordination: Using one of nature’s tricks to control soft material mechanics. J Mater Chem B, 2014, 2: 2467-2472 CrossRef PubMed Google Scholar

[82] Karpishin T B, Gebhard M S, Solomon E I, et al. Spectroscopic studies of the electronic structure of iron(III) tris(catecholates). J Am Chem Soc, 1991, 113: 2977-2984 CrossRef Google Scholar

[83] Lana-Villarreal T, Rodes A, Pérez J M, et al. A spectroscopic and electrochemical approach to the study of the interactions and photoinduced electron transfer between catechol and anatase nanoparticles in aqueous solution. J Am Chem Soc, 2005, 127: 12601-12611 CrossRef PubMed Google Scholar

[84] Keten S, Buehler M J. Geometric confinement governs the rupture strength of h-bond assemblies at a critical length scale. Nano Lett, 2008, 8: 743-748 CrossRef PubMed ADS Google Scholar

[85] Li Y, Liu H, Wang T, et al. Single-molecule force spectroscopy reveals multiple binding modes between dopa and different rutile surfaces. ChemPhysChem, 2017, 18: 1466-1469 CrossRef PubMed Google Scholar

[86] Xu Z. Mechanics of metal-catecholate complexes: The roles of coordination state and metal types. Sci Rep, 2013, 3: 2914 CrossRef PubMed ADS Google Scholar

[87] Yu M, Deming T J. Synthetic polypeptide mimics of marine adhesives. Macromolecules, 1998, 31: 4739-4745 CrossRef PubMed ADS Google Scholar

[88] Zhang F, Pan J. Recent development of corrosion protection strategy based on mussel adhesive protein. Front Mater, 2019, 6: 207 CrossRef ADS Google Scholar

[89] Hansen D C, Luther George W. I, Waite J H. The adsorption of the adhesive protein of the blue mussel mytilus edulis l onto type 304l stainless steel. J Colloid Interface Sci, 1994, 168: 206-216 CrossRef ADS Google Scholar

[90] Yu F, Chen S, Chen Y, et al. Experimental and theoretical analysis of polymerization reaction process on the polydopamine membranes and its corrosion protection properties for 304 stainless steel. J Mol Structure, 2010, 982: 152-161 CrossRef ADS Google Scholar

[91] Sababi M, Zhang F, Krivosheeva O, et al. Thin composite films of mussel adhesive proteins and ceria nanoparticles on carbon steel for corrosion protection. J Electrochem Soc, 2012, 159: C364-C371 CrossRef Google Scholar

[92] Zhao H, Waite J H. Proteins in load-bearing junctions: The histidine-rich metal-binding protein of mussel byssus. Biochemistry, 2006, 45: 14223-14231 CrossRef PubMed Google Scholar

[93] Schmidt S, Reinecke A, Wojcik F, et al. Metal-mediated molecular self-healing in histidine-rich mussel peptides. Biomacromolecules, 2014, 15: 1644-1652 CrossRef PubMed Google Scholar

[94] Hwang D S, Zeng H, Masic A, et al. Protein- and metal-dependent interactions of a prominent protein in mussel adhesive plaques. J Biol Chem, 2010, 285: 25850-25858 CrossRef PubMed Google Scholar

[95] Zeng H, Hwang D S, Israelachvili J N, et al. Strong reversible Fe3+- mediated bridging between dopa-containing protein films in water. Proc Natl Acad Sci USA, 2010, 107: 12850-12853 CrossRef PubMed ADS Google Scholar

[96] Hwang D S, Waite J H. Three intrinsically unstructured mussel adhesive proteins, mfp-1, mfp-2, and mfp-3: Analysis by circular dichroism. Protein Sci, 2012, 21: 1689-1695 CrossRef PubMed Google Scholar

[97] Ninan L, Stroshine R L, Wilker J J, et al. Adhesive strength and curing rate of marine mussel protein extracts on porcine small intestinal submucosa. Acta Biomater, 2007, 3: 687-694 CrossRef PubMed Google Scholar

[98] Park J P, Song I T, Lee J, et al. Vanadyl-catecholamine hydrogels inspired by ascidians and mussels. Chem Mater, 2014, 27: 105-111 CrossRef Google Scholar

[99] Das S, Miller D R, Kaufman Y, et al. Tough coating proteins: Subtle sequence variation modulates cohesion. Biomacromolecules, 2015, 16: 1002-1008 CrossRef PubMed Google Scholar

[100] Priemel T, Degtyar E, Dean M N, et al. Rapid self-assembly of complex biomolecular architectures during mussel byssus biofabrication. Nat Commun, 2017, 8: 14539 CrossRef PubMed ADS Google Scholar

[101] Holten-Andersen N, Fantner G E, Hohlbauch S, et al. Protective coatings on extensible biofibres. Nat Mater, 2007, 6: 669-672 CrossRef PubMed ADS Google Scholar

[102] Holten-Andersen N, Zhao H, Waite J H. Stiff coatings on compliant biofibers: The cuticle of Mytilus californianus byssal threads. Biochemistry, 2009, 48: 2752-2759 CrossRef PubMed Google Scholar

[103] Li Y, Wen J, Qin M, et al. Single-molecule mechanics of catechol-iron coordination bonds. ACS Biomater Sci Eng, 2017, 3: 979-989 CrossRef Google Scholar

[104] Loizou E, Weisser J T, Dundigalla A, et al. Structural effects of crosslinking a biopolymer hydrogel derived from marine mussel adhesive protein. Macromol Biosci, 2006, 6: 711-718 CrossRef PubMed Google Scholar

[105] Holten-Andersen N, Harrington M J, Birkedal H, 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, 2011, 108: 2651-2655 CrossRef PubMed ADS Google Scholar

[106] Xu H, Nishida J, Wu H, et al. Structural effects of catechol-containing polystyrene gels based on a dual cross-linking approach. Soft Matter, 2013, 9: 1967-1974 CrossRef ADS Google Scholar

[107] Holten-Andersen N, Waite J H. Mussel-designed protective coatings for compliant substrates. J Dent Res, 2008, 87: 701-709 CrossRef PubMed Google Scholar

[108] Monahan J, Wilker J J. Specificity of metal ion cross-linking in marine mussel adhesives. Chem Commun, 2003, : 1672 CrossRef PubMed Google Scholar

[109] Monahan J, Wilker J J. Cross-linking the protein precursor of marine mussel adhesives: Bulk measurements and reagents for curing. Langmuir, 2004, 20: 3724-3729 CrossRef PubMed Google Scholar

[110] Liu Q, Lu X, Li L, et al. Probing the reversible Fe3+-DOPA-mediated bridging interaction in mussel foot protein-1. J Phys Chem C, 2016, 120: 21670-21677 CrossRef Google Scholar

[111] Taylor S W, Chase D B, Emptage M H, et al. Ferric ion complexes of a DOPA-containing adhesive protein from Mytilus edulis. Inorg Chem, 1996, 35: 7572-7577 CrossRef Google Scholar

[112] Krogsgaard M, Behrens M A, Pedersen J S, et al. Self-healing mussel-inspired multi-ph-responsive hydrogels. Biomacromolecules, 2013, 14: 297-301 CrossRef PubMed Google Scholar

[113] Avdeef A, Sofen S R, Bregante T L, et al. Coordination chemistry of microbial iron transport compounds. 9. Stability constants for catechol models of enterobactin. J Am Chem Soc, 1978, 100: 5362-5370 CrossRef Google Scholar

[114] Yang B, Lim C, Hwang D S, et al. Switch of surface adhesion to cohesion by DOPA-Fe3+ complexation, in response to microenvironment at the mussel plaque/substrate interface. Chem Mater, 2016, 28: 7982-7989 CrossRef Google Scholar

[115] Aldred N, Ista L K, Callow M E, et al. Mussel (Mytilus edulis) byssus deposition in response to variations in surface wettability. J R Soc Interface, 2006, 3: 37-43 CrossRef PubMed Google Scholar

[116] Huang S, Hou Q, Guo D, et al. Adsorption mechanism of mussel-derived adhesive proteins onto various self-assembled monolayers. RSC Adv, 2017, 7: 39530-39538 CrossRef Google Scholar

[117] Nozaki Y, Tanford C. The solubility of amino acids and two glycine peptides in aqueous ethanol and dioxane solutions: Establishment of a hydrophobicity scale. J Biol Chem, 1971, 246: 2211–2217. Google Scholar

[118] Kaur S, Narayanan A, Dalvi S, et al. Direct observation of the interplay of catechol binding and polymer hydrophobicity in a mussel-inspired elastomeric adhesive. ACS Cent Sci, 2018, 4: 1420-1429 CrossRef Google Scholar

[119] Akdogan Y, Wei W, Huang K Y, et al. Intrinsic surface-drying properties of bioadhesive proteins. Angew Chem Int Ed, 2014, 53: 11253-11256 CrossRef PubMed Google Scholar

[120] Jelesarov I, Dürr E, Thomas R M, et al. Salt effects on hydrophobic interaction and charge screening in the folding of a negatively charged peptide to a coiled coil (leucine zipper). Biochemistry, 1998, 37: 7539-7550 CrossRef PubMed Google Scholar

[121] Stewart R J, Ransom T C, Hlady V. Natural underwater adhesives. J Polym Sci B Polym Phys, 2011, 49: 757-771 CrossRef PubMed ADS Google Scholar

[122] Lu Q, Hwang D S, Liu Y, et al. Molecular interactions of mussel protective coating protein, mcfp-1, from mytilus californianus. Biomaterials, 2012, 33: 1903-1911 CrossRef PubMed Google Scholar

[123] Rzepecki L M, Waite J H. Αβ-dehydro-3,4-dihydroxyphenylalanine derivatives: Rate and mechanism of formation. Archives Biochem Biophys, 1991, 285: 27-36 CrossRef Google Scholar

[124] Mirshafian R, Wei W, Israelachvili J N, et al. α,β-dehydro-DOPA: A hidden participant in mussel adhesion. Biochemistry, 2016, 55: 743-750 CrossRef PubMed Google Scholar

[125] Weidman S W, Kaiser E T. The mechanism of the periodate oxidation of aromatic systems. III. A kinetic study of the periodate oxidation of catechol. J Am Chem Soc, 1966, 88: 5820-5827 CrossRef Google Scholar

[126] Haemers S, Koper G J M, Frens G. Effect of oxidation rate on cross-linking of mussel adhesive proteins. Biomacromolecules, 2003, 4: 632-640 CrossRef PubMed Google Scholar

[127] van der Leeden M C. Are conformational changes, induced by osmotic pressure variations, the underlying mechanism of controlling the adhesive activity of mussel adhesive proteins?. Langmuir, 2005, 21: 11373-11379 CrossRef PubMed Google Scholar

[128] Yu J, Wei W, Danner E, et al. Mussel protein adhesion depends on interprotein thiol-mediated redox modulation. Nat Chem Biol, 2011, 7: 588-590 CrossRef PubMed Google Scholar

[129] Miller D R, Spahn J E, Waite J H. The staying power of adhesion-associated antioxidant activity in Mytilus californianus. J R Soc Interface, 2015, 12: 20150614 CrossRef PubMed Google Scholar

[130] Seo S, Das S, Zalicki P J, et al. Microphase behavior and enhanced wet-cohesion of synthetic copolyampholytes inspired by a mussel foot protein. J Am Chem Soc, 2015, 137: 9214-9217 CrossRef PubMed Google Scholar

[131] Zhao H, Waite J H. Linking adhesive and structural proteins in the attachment plaque of Mytilus californianus. J Biol Chem, 2006, 281: 26150-26158 CrossRef PubMed Google Scholar

[132] Nicklisch S C T, Das S, Martinez Rodriguez N R, et al. Antioxidant efficacy and adhesion rescue by a recombinant mussel foot protein-6. Biotechnol Prog, 2013, 29: 1587-1593 CrossRef PubMed Google Scholar

[133] Wang J, Suhre M H, Scheibel T. A mussel polyphenol oxidase-like protein shows thiol-mediated antioxidant activity. Eur Polym J, 2019, 113: 305-312 CrossRef Google Scholar

[134] Nicklisch S C T, Spahn J E, Zhou H, et al. Redox capacity of an extracellular matrix protein associated with adhesion in Mytilus californianus. Biochemistry, 2016, 55: 2022-2030 CrossRef PubMed Google Scholar

[135] Argust P. Distribution of boron in the environment. Biol Trace Elem Res, 1998, 66: 131-143 CrossRef PubMed Google Scholar

[136] Waite J H, Qin X. Polyphosphoprotein from the adhesive pads of Mytilus edulis. Biochemistry, 2001, 40: 2887-2893 CrossRef PubMed Google Scholar

[137] Taylor S W. Chemoenzymatic synthesis of peptidyl 3,4-dihydroxyphenylalanine for structure-activity relationships in marine invertebrate polypeptides. Anal Biochem, 2002, 302: 70-74 CrossRef PubMed Google Scholar

[138] Lee B P, Huang K, Nunalee F N, et al. Synthesis of 3,4-dihydroxyphenylalanine (dopa) containing monomers and their co-polymerization with peg-diacrylate to form hydrogels. J BioMater Sci Polym Ed, 2004, 15: 449-464 CrossRef PubMed Google Scholar

[139] Kan Y, Danner E W, Israelachvili J N, et al. Boronate complex formation with dopa containing mussel adhesive protein retards ph-induced oxidation and enables adhesion to mica. PLoS ONE, 2014, 9: e108869 CrossRef PubMed ADS Google Scholar

[140] George M N, Carrington E. Environmental post-processing increases the adhesion strength of mussel byssus adhesive. Biofouling, 2018, 34: 388-397 CrossRef PubMed Google Scholar

[141] Guvendiren M, Brass D A, Messersmith P B, et al. Adhesion of dopa-functionalized model membranes to hard and soft surfaces. J Adhes, 2009, 85: 631-645 CrossRef PubMed Google Scholar

[142] Yang B, Kang D G, Seo J H, et al. A comparative study on the bulk adhesive strength of the recombinant mussel adhesive protein fp-3. Biofouling, 2013, 29: 483-490 CrossRef PubMed Google Scholar

[143] Suci P A, Geesey G G. Comparison of adsorption behavior of two mytilus edulis foot proteins on three surfaces. Colloids Surfs B-Biointerfaces, 2001, 22: 159-168 CrossRef Google Scholar

[144] Suci P A, Geesey G G. Use of attenuated total internal reflection fourier transform infrared spectroscopy to investigate interactions between Mytilus edulis foot proteins at a surface. Langmuir, 2001, 17: 2538-2540 CrossRef Google Scholar

[145] Fant C, Elwing H, Höök F. The influence of cross-linking on protein-protein interactions in a marine adhesive: The case of two byssus plaque proteins from the blue mussel. Biomacromolecules, 2002, 3: 732-741 CrossRef PubMed Google Scholar

[146] McDowell L M, Burzio L A, Waite J H, et al. Rotational echo double resonance detection of cross-links formed in mussel byssus under high-flow stress. J Biol Chem, 1999, 274: 20293-20295 CrossRef PubMed Google Scholar

[147] Burzio L A, Waite J H. Cross-linking in adhesive quinoproteins: Studies with model decapeptides. Biochemistry, 2000, 39: 11147-11153 CrossRef PubMed Google Scholar

[148] Hedlund J, Andersson M, Fant C, et al. Change of colloidal and surface properties of mytilus edulis foot protein 1 in the presence of an oxidation (NaIO4) or a complex-binding (Cu2+) agent. Biomacromolecules, 2009, 10: 845-849 CrossRef PubMed Google Scholar

[149] Burdine L, Gillette T G, Lin H J, et al. Periodate-triggered cross-linking of dopa-containing peptide-protein complexes. J Am Chem Soc, 2004, 126: 11442-11443 CrossRef PubMed Google Scholar

[150] Liu B, Burdine L, Kodadek T. Chemistry of periodate-mediated cross-linking of 3,4-dihydroxylphenylalanine-containing molecules to proteins. J Am Chem Soc, 2006, 128: 15228-15235 CrossRef PubMed Google Scholar

[151] Zhao H, Waite J H. Coating proteins: Structure and cross-linking in fp-1 from the green shell mussel Perna canaliculus. Biochemistry, 2005, 44: 15915-15923 CrossRef PubMed Google Scholar

[152] Nicklisch S C T, Waite J H. Mini-review: The role of redox in dopa-mediated marine adhesion. Biofouling, 2012, 28: 865-877 CrossRef PubMed Google Scholar

[153] Jang H G, Cox D D, Que L. A highly reactive functional model for the catechol dioxygenases. Structure and properties of [Fe(TPA)- DBC]BPh4. J Am Chem Soc, 1991, 113: 9200-9204 CrossRef Google Scholar

[154] Matin M A, Chitumalla R K, Lim M, et al. Density functional theory study on the cross-linking of mussel adhesive proteins. J Phys Chem B, 2015, 119: 5496-5504 CrossRef PubMed Google Scholar

[155] Brooksby P A, Schiel D R, Abell A D. Electrochemistry of catechol terminated monolayers with Cu(II), Ni(II) and Fe(III) cations: A model for the marine adhesive interface. Langmuir, 2008, 24: 9074-9081 CrossRef PubMed Google Scholar

[156] Barrett D G, Fullenkamp D E, He L, et al. Ph-based regulation of hydrogel mechanical properties through mussel-inspired chemistry and processing. Adv Funct Mater, 2013, 23: 1111-1119 CrossRef PubMed Google Scholar

[157] Fullenkamp D E, Barrett D G, Miller D R, et al. pH-dependent cross-linking of catechols through oxidation via Fe3+ and potential implications for mussel adhesion. RSC Adv, 2014, 4: 25127-25134 CrossRef PubMed Google Scholar

[158] Li S, Chen Y, Gao Y, et al. Chemical oxidants affect byssus adhesion in the highly invasive fouling mussel limnoperna fortunei. Sci Total Environ, 2019, 646: 1367-1375 CrossRef PubMed ADS Google Scholar

[159] Dougherty D A. Cation-π interactions in chemistry and biology: A new view of benzene,phe,tyr,and trp. Science, 1996, 271: 163-168 CrossRef PubMed ADS Google Scholar

[160] Frank B P, Belfort G. Atomic force microscopy for low-adhesion surfaces: Thermodynamic criteria,critical surface tension,and intermolecular forces. Langmuir, 2001, 17: 1905-1912 CrossRef Google Scholar

[161] Ma J C, Dougherty D A. The cation-π interaction. Chem Rev, 1997, 97: 1303-1324 CrossRef PubMed Google Scholar

[162] Gallivan J P, Dougherty D A. A computational study of cation-π interactions vs salt bridges in aqueous media: Implications for protein engineering. J Am Chem Soc, 2000, 122: 870-874 CrossRef Google Scholar

[163] Kim S, Huang J, Lee Y, et al. Complexation and coacervation of like-charged polyelectrolytes inspired by mussels. Proc Natl Acad Sci USA, 2016, 113: E847-E853 CrossRef PubMed ADS Google Scholar

[164] Kim S, Yoo H Y, Huang J, et al. Salt triggers the simple coacervation of an underwater adhesive when cations meet aromatic π electrons in seawater. ACS Nano, 2017, 11: 6764-6772 CrossRef Google Scholar

[165] Yang B, Jin S, Park Y, et al. Coacervation of interfacial adhesive proteins for initial mussel adhesion to a wet surface. Small, 2018, 14: 1803377 CrossRef PubMed Google Scholar

[166] Zhao H, Sagert J, Hwang D S, et al. Glycosylated hydroxytryptophan in a mussel adhesive protein from Perna viridis. J Biol Chem, 2009, 284: 23344-23352 CrossRef PubMed Google Scholar

[167] Hwang D S, Zeng H, Lu Q, et al. Adhesion mechanism in a dopa-deficient foot protein from green mussels. Soft Matter, 2012, 8: 5640-5648 CrossRef PubMed ADS Google Scholar

[168] Kim S, Faghihnejad A, Lee Y, et al. Cation-π interaction in dopa-deficient mussel adhesive protein mfp-1. J Mater Chem B, 2015, 3: 738-743 CrossRef Google Scholar

[169] Das S, Martinez Rodriguez N R, Wei W, et al. Peptide length and dopa determine iron-mediated cohesion of mussel foot proteins. Adv Funct Mater, 2015, 25: 5840-5847 CrossRef PubMed Google Scholar

[170] Lu Q, Oh D X, Lee Y, et al. Nanomechanics of cation-π interactions in aqueous solution. Angew Chem, 2013, 125: 4036-4040 CrossRef Google Scholar

[171] Gebbie M A, Wei W, Schrader A M, et al. Tuning underwater adhesion with cation-π interactions. Nat Chem, 2017, 9: 473-479 CrossRef PubMed ADS Google Scholar

[172] White J D, Wilker J J. Underwater bonding with charged polymer mimics of marine mussel adhesive proteins. Macromolecules, 2011, 44: 5085-5088 CrossRef ADS Google Scholar

[173] Haemers S, van der Leeden M C, Nijman E J, et al. The degree of aggregation in solution controls the adsorbed amount of mussel adhesive proteins on a hydrophilic surface. Colloids Surfs A-Physicochem Eng Aspects, 2001, 190: 193-203 CrossRef Google Scholar

[174] Krivosheeva O, Dėdinaitė A, Claesson P M. Adsorption of mefp-1: Influence of ph on adsorption kinetics and adsorbed amount. J Colloid Interface Sci, 2012, 379: 107-113 CrossRef PubMed ADS Google Scholar

[175] Wei W, Tan Y, Martinez Rodriguez N R, et al. A mussel-derived one component adhesive coacervate. Acta Biomater, 2014, 10: 1663-1670 CrossRef PubMed Google Scholar

[176] Wang J, Scheibel T. Coacervation of the recombinant Mytilus galloprovincialis foot protein-3b. Biomacromolecules, 2018, 19: 3612-3619 CrossRef PubMed Google Scholar

[177] Haemers S, van der Leeden M C, Frens G. Coil dimensions of the mussel adhesive protein mefp-1. Biomaterials, 2005, 26: 1231-1236 CrossRef PubMed Google Scholar

[178] Even M A, Wang J, Chen Z. Structural information of mussel adhesive protein mefp-3 acquired at various polymer/mefp-3 solution interfaces. Langmuir, 2008, 24: 5795-5801 CrossRef PubMed Google Scholar

[179] Matos-Pérez C R, White J D, Wilker J J. Polymer composition and substrate influences on the adhesive bonding of a biomimetic, cross-linking polymer. J Am Chem Soc, 2012, 134: 9498-9505 CrossRef PubMed Google Scholar

[180] Jenkins C L, Meredith H J, Wilker J J. Molecular weight effects upon the adhesive bonding of a mussel mimetic polymer. ACS Appl Mater Interfaces, 2013, 5: 5091-5096 CrossRef PubMed Google Scholar

[181] Kim E, Dai B, Qiao J B, et al. Microbially synthesized repeats of mussel foot protein display enhanced underwater adhesion. ACS Appl Mater Interfaces, 2018, 10: 43003-43012 CrossRef Google Scholar

[182] Ahn B K, Das S, Linstadt R, et al. High-performance mussel-inspired adhesives of reduced complexity. Nat Commun, 2015, 6: 8663 CrossRef PubMed ADS Google Scholar

[183] Kord Forooshani P, Lee B P. Recent approaches in designing bioadhesive materials inspired by mussel adhesive protein. J Polym Sci Part A-Polym Chem, 2017, 55: 9-33 CrossRef PubMed ADS Google Scholar

[184] Bilic G, Brubaker C, Messersmith P B, et al. Injectable candidate sealants for fetal membrane repair: Bonding and toxicity in vitro. Am J Obstetrics GynEcol, 2010, 202: 85.e1-85.e9 CrossRef PubMed Google Scholar

[185] Kim B J, Oh D X, Kim S, et al. Mussel-mimetic protein-based adhesive hydrogel. Biomacromolecules, 2014, 15: 1579-1585 CrossRef PubMed Google Scholar

[186] Ren Y, Zhao X, Liang X, et al. Injectable hydrogel based on quaternized chitosan, gelatin and dopamine as localized drug delivery system to treat Parkinson’s disease. Int J Biol Macromolecules, 2017, 105: 1079-1087 CrossRef PubMed Google Scholar

[187] Barrett D G, Bushnell G G, Messersmith P B. Mechanically robust, negative-swelling, mussel-inspired tissue adhesives. Adv Healthcare Mater, 2013, 2: 745-755 CrossRef PubMed Google Scholar

[188] Cui J, Yan Y, Such G K, et al. Immobilization and intracellular delivery of an anticancer drug using mussel-inspired polydopamine capsules. Biomacromolecules, 2012, 13: 2225-2228 CrossRef PubMed Google Scholar

[189] Statz A R, Meagher R J, Barron A E, et al. New peptidomimetic polymers for antifouling surfaces. J Am Chem Soc, 2005, 127: 7972-7973 CrossRef PubMed Google Scholar

[190] Lee H, Lee B P, Messersmith P B. A reversible wet/dry adhesive inspired by mussels and geckos. Nature, 2007, 448: 338-341 CrossRef PubMed ADS Google Scholar

[191] Zhang L, Wu J, Wang Y, et al. Combination of bioinspiration: A general route to superhydrophobic particles. J Am Chem Soc, 2012, 134: 9879-9881 CrossRef PubMed Google Scholar

[192] Zhong D, Yang Q, Guo L, et al. Fusion of nacre, mussel, and lotus leaf: Bio-inspired graphene composite paper with multifunctional integration. Nanoscale, 2013, 5: 5758-5764 CrossRef PubMed ADS Google Scholar

[193] Rzepecki L M, Hansen K M, Waite J H. Characterization of a cystine-rich polyphenolic protein family from the blue mussel Mytilus edulis L. Biol Bull, 1992, 183: 123-137 CrossRef PubMed Google Scholar

[194] Zhao H, Robertson N B, Jewhurst S A, et al. Probing the adhesive footprints of Mytilus californianus byssus. J Biol Chem, 2006, 281: 11090-11096 CrossRef PubMed Google Scholar

[195] Krogsgaard M, Nue V, Birkedal H. Mussel-inspired materials: Self-healing through coordination chemistry. Chem Eur J, 2016, 22: 844-857 CrossRef PubMed Google Scholar

[196] Hellio C, Thomas‐Guyon H, Culioli G, et al. Marine antifoulants from bifurcaria bifurcata (phaeophyceae, cystoseiraceae) and other brown macroalgae. Biofouling, 2001, 17: 189-201 CrossRef Google Scholar

[197] Amini S, Kolle S, Petrone L, et al. Preventing mussel adhesion using lubricant-infused materials. Science, 2017, 357: 668-673 CrossRef PubMed ADS Google Scholar

[198] Venkatareddy N L, Wilke P, Ernst N, et al. Mussel-glue inspired adhesives: A study on the relevance ofl -Dopa and the function of the sequence at nanomaterial-peptide interfaces. Adv Mater Interfaces, 2019, 6: 1900501 CrossRef Google Scholar

[199] Meyer E A, Castellano R K, Diederich F. Interactions with aromatic rings in chemical and biological recognition. Angew Chem Int Ed, 2003, 42: 1210-1250 CrossRef PubMed Google Scholar

[200] Zhang J, Xiang L, Yan B, et al. Nanomechanics of anion-π interaction in aqueous solution. J Am Chem Soc, 2020, 142: 1710-1714 CrossRef PubMed Google Scholar

[201] Ren H Y, Mizukami M, Kurihara K. Preparation of stable silica surfaces for surface forces measurement. Rev Sci Instrum, 2017, 88: 095108 CrossRef PubMed ADS Google Scholar

[202] Dobbs H A, Kaufman Y, Scott J, et al. Ultra-smooth, chemically functional silica surfaces for surface interaction measurements and optical/interferometry-based techniques. Adv Eng Mater, 2018, 20: 1700630 CrossRef Google Scholar

[203] Kristiansen K, Donaldson Jr. S H, Berkson Z J, et al. Multimodal miniature surface forces apparatus (μSFA) for interfacial science measurements. Langmuir, 2019, 35: 15500-15514 CrossRef PubMed Google Scholar

[204] de Aguiar H B, McGraw J D, Donaldson Jr. S H. Interface-sensitive raman microspectroscopy of water via confinement with a multimodal miniature surface forces apparatus. Langmuir, 2019, 35: 15543-15551 CrossRef PubMed Google Scholar

[205] Desmond K W, Zacchia N A, Waite J H, et al. Dynamics of mussel plaque detachment. Soft Matter, 2015, 11: 6832-6839 CrossRef PubMed ADS Google Scholar

[206] Wilhelm M H, Filippidi E, Waite J H, et al. Influence of multi-cycle loading on the structure and mechanics of marine mussel plaques. Soft Matter, 2017, 13: 7381-7388 CrossRef PubMed ADS Google Scholar

[207] Cohen N, Waite J H, McMeeking R M, et al. Force distribution and multiscale mechanics in the mussel byssus. Phil Trans R Soc B, 2019, 374: 20190202 CrossRef PubMed Google Scholar

  • Figure 1

    (Color online) Distribution of known mussel foot proteins in the plaque and distal thread of a Mytilus. When a Mytilus attaches to a surface through hundreds of threads (upper-left corner), one adhesive plaque marked in the circle (insert) is enlarged as the main schematic. Mfp is the mussel foot protein; PreCOL and TMP are the collagen gland proteins of prepolymerized collagens and thread matrix proteins, respectively.

  • Figure 2

    (Color online) Surface forces apparatus (SFA) system.

  • Figure 3

    (Color online) (a) Principle of the force measurement in the SFA, and (b) force-distance profile measured in the SFA, where “in” denotes the surface approaching, and “out” denotes the surface separation.

  • Figure 4

    (Color online) Adhesion of Mefp-5 with mica surface measured through SFA. (a) Interaction between a Mefp-5-coated mica surface and a bare mica in pH 2.6 buffer. Mefp-5 showed the strongest adhesive energy of −13.7 mJ/m2 with a contact time of ~1 h. Reprinted with permission from ref. [68]. Copyright © 2012, American Chemical Society. (b) Proposed hydrogen bonding as the adhesion mechanism of Mfp with mica, of which the bidentate bonds depend on the surface geometry. The adhesion of Mfp to mica can be abolished by the oxidation of Dopa into dopaquinone.

  • Figure 5

    (Color online) Fe3+-mediated cross-linking of the Mefp-1 measured in the SFA. Interaction between two symmetrical Mefp-1 layers measured in buffers (a) without Fe3+, (b) with 10 μM Fe3+, and (c) with 100 μM Fe3+. Reprinted and modified with permission from ref. [95]. Copyright © 2010 National Academy of Sciences of the United States.

  • Figure 6

    (Color online) Hydrophobic effects of Mfps in the bridging between a CH3-SAM surface and a bare mica. (a) SFA force curves were measured after Mfp-1, Mfp-3 or Mfp-5 was injected into the gap solution between two surfaces, all of which exhibited strong adhesion. (b) Illustration of the hydrophobic attraction dominating in the Mfp adhesion between hydrophobic SAM and a mica surface. All three Dopa-rich Mfps can bind tightly with the CH3 headgroups on SAM surface mainly through Dopa, whereas Mfp-3 has three additional tryptophan residues at its C-terminus. Reprinted and modified with permission from ref. [13]. Copyright © 2013 National Academy of Sciences of the United States.

  • Figure 7

    (Color online) Oxidation of Dopa in Mfp to Dopa semiquinone (losing 1 electron), Dopaquinone (losing 2 electrons), and Dopaquinone tautomers, including Dopaquinone methide and α,β-dehydroDopa (Δ-Dopa).

  • Figure 8

    (Color online) Adhesion of Mefp-5 to mica surface measured in the SFA at pH 3 and pH 7.5 with 0.1 mol L−1 borate. (a) Dopa in the pre-adsorbed Mefp-5 retained its adhesion capacity at pH 7.5 in the form of Dopa-boronate complex after compression, which can be freed to bind strongly with the opposite mica surface. (b) The protection of Dopa by borate was confirmed by lowering the pH back to 3 when the adhesive performance of the protein was nearly the same as its initial condition. Reproduced and modified with permission from ref. [139]. Copyright © 2014 Kan et al.

  • Figure 9

    (Color online) Dopaquinone-mediated Mfp cross-linking, including aryl-aryl coupling (diDopa), Schiff-base substitution (the reaction between lysine side chain and Dopaquinone shown as an example), and Michael-type addition (the thiol-quinone intermediate shown as an example, which undergoes further tautomerization to 5-S-Cysteinyldopa).

  • Figure 10

    (Color online) Cohesion of three peptides containing phenylalanine, tyrosine, and Dopa. (a) Force-distance profiles measured in the SFA between two mica surfaces coated with each of the above aromatic residues at pH 2.5. (b) Cohesion mechanisms were mainly attributed to the cation-π interactions between lysine and aromatic residues in the peptide films. The presence of the electronegative hydroxyl group in the aromatic ring dramatically weakens the configurational entropy of the peptide, which results in a relatively weak cohesion measured in tyrosine or Dopa peptide. Reprinted with permission from ref. [171]. Copyright © 2017 Macmillan Publishers Limited, part of Springer Nature.

  • Figure 11

    (Color online) Schematic of part of the known Mfp-surface and Mfp-Mfp interactions in the byssal plaque.

  • Table 1   Selected results from the SFA studies on the adhesion mechanisms of native Mfps and their recombinants

    Dominant interaction

    Surface #1

    Surface #2

    EAD, mJ/m2 (contact time, min)

    pH (mediator)

    Refs.

    Hydrogen bonding

    Mcfp-1

    Mica

    −0.8 (60)

    5.5

    [69]

    SiO2

    −0.1 (10)

    5.5

    [69]

    OH-SAM

    −0.3d) (-)

    3

    [13]

    Mcfp-3f

    Mica

    −3.3d) (60)

    3

    [67]

    SiO2

    −3.0 (60)

    5.5

    [69]

    TiO2

    −8.8d) (1)

    3

    [35]

    OH-SAM

    −0.5d) (<2)

    3

    [13]

    Mcfp-3s

    Mica

    −1.3d) (3)

    3

    [30]

    Mcfp-3s peptidea)

    OH-SAM

    −0.4 (<2)

    3

    [54]

    Mefp-5

    Mica

    −13.7 (60)

    2.6

    [68]

    SiO2

    −2.4 (60)

    5.5

    [69]

    OH-SAM

    −0.4d) (<2)

    3

    [13]

    Metal-coordinationinteraction

    Mcfp-1

    TiO2

    −1.7 (40)

    5.5

    [34]

    Mcfp-3f

    TiO2

    −1.7d) (1)

    7.5

    [35]

    Mefp-1

    Mefp-1

    −4.3 (100)

    5.5 (10 μmol L−1 Fe3+)

    [95]

    Mefp-2

    Mefp-2

    −2.2 (1)e)

    5.5 (5 μmol L−1 Fe3+)

    [94]

    Hydrophobic attraction

    Mcfp-1

    CH3-SAM

    −3.5 (<2)

    3

    [13]

    PMMA

    −0.1 (60)

    5.5

    [69]

    Mcfp-3f

    CH3-SAM

    −8.9 (<2)

    3

    [13]

    PMMA

    −1.3 (60)

    5.5

    [69]

    Mcfp-3s peptide

    CH3-SAM

    −7.7 (-)

    3

    [54]

    Mefp-5

    CH3-SAM

    −6.7 (<2)

    3

    [13]

    PMMA

    −0.4 (60)

    5.5

    [69]

    Mcfp-3s

    Mfp-2

    −0.5d) (3)

    5.5

    [30]

    Mcfp-3sb)

    Mcfp-3s

    −4.1d) (65)

    7.5

    [30]

    Quinone-mediated

    crosslinking

    Mefp-5

    Mefp-5

    >−10.6 (720)

    5.5

    [68]

    π-interactions

    (cation-π interactionor π-π stacking)

    Mcfp-1c)

    PS

    −0.3 (60)

    5.5

    [69]

    Mcfp-3c)

    PS

    −2.7 (60)

    5.5

    [69]

    Mefp-5c)

    PS

    −2.4 (60)

    5.5

    [69]

    Mcfp-1

    Mcfp-1

    −3.0–−3.1 (2)

    3, 5.5

    [122]

    Pvfp-1

    Pvfp-1

    −2.4 (40)

    5.5

    [167]

    Rmfp-1

    Rmfp-1

    −3.8 (2)

    3f)

    [168]

    Rmfp-1

    −5.0 (-)

    3f) (0.6 mol L−1 NaCl)

    [164]

    MADQUAT

    −4.8 (-)

    3f)

    [163]

    Electrostatic attraction

    Pvfp-1

    mica

    −0.1 (40)

    5.5

    [167]

    Rmfp-1

    mica

    −3.0 (2)

    3f)

    [168]

    Mefp-2

    Mefp-2

    −0.3 (60)

    5.5 (5 μmol L−1 Ca2+)

    [94]

    Electrostatic attraction, b) hydrogen bonding, and c) hydrophobic interaction were also proposed in the respective cases. d) The magnitude of adhesion energy (EAD) is converted from the original data following the equation EAD = FAD /1.5πR for elastic deformation. e) Adhesion was measured after the measurement with a 60 min contact. The common buffer solutions include the following: 0.1 mol L−1 HAc and 0.1–0.25 mol L−1 KNO3 (pH 3); 0.1 mol L−1 NaAc and 0.1–0.25 mol L−1 KNO3 (pH 5.5); 0.1 mol L−1 potassium phosphate salt (pH 7.5); except f) without KNO3.

  • Table 2   Amino acid composition of Mfps

    Mfp

    Dopa (mol%)

    Cationic (mol%)

    Anionic (mol%)

    Aromatic (mol%)

    Hydrophobic (mol %)

    Refs.

    Mcfp-1

    13

    21

    12

    19

    29

    [102]

    Mefp-1

    11

    23

    13

    17

    28

    [5]

    Pvfp-1

    0

    17

    3

    18

    42

    [166]

    Rmfp-1

    0

    20

    10

    20

    30

    [168]

    Mefp-2

    3

    19

    14

    10

    27

    [193]

    Mcfp-3f

    19

    26

    3

    27

    31

    [194]

    Mcfp-3s

    11

    9

    5

    27

    31

    [194]

    Mcfp-3s peptide

    28

    8

    4

    40

    40

    [54]

    Mefp-5

    26

    29

    14

    26

    32

    [136]

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