Abstract
There exists in nature a wide variety of adhesives to meet the demands of underwater organisms. The requirements for attachment in aqueous environment are much more challenging than those in air. To achieve underwater attachment, sessile organisms ranging from microbes to hard and soft animals and plants have developed diversified ways to tightly and continuously attach to several material surfaces. These biological adhesives are excellent models from which to learn how to artificially attach materials in water and to obtain information that will be useful to develop general theories in the interface sciences. In this chapter, we compare biological material designs from the macroscopic to molecular levels to provide clues for designing new artificial adhesives. Specifically, we review how the mussel, barnacle, and tubeworm form firm underwater adhesion.
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References
Waite JH (1987) Nature’s underwater adhesive specialist. Int J Adhes 7:9–14
Zhao H, Robertson NB, Jewhurst SA, Waite JH (2006) Probing the adhesive footprints of Mytilus californianus byssus. J Biol Chem 281:11090–11096
Kamino K (2010) Molecular design of barnacle cement in comparison with those of mussel and tubeworm. J Adhesion 86:96–110
Ball P (2003) Does nature know best? Nat Mater 2:510
Waite JH (1992) The formation of mussel byssus: anatomy of a natural manufacturing process. In: Case ST (ed) Results and problems in cell differentiation 19, Biopolymers. Springer, Berlin, pp 27–54
Waite JH, Andersen NH, Jewhurst S, Sun C (2005) Mussel adhesion: finding the tricks worth mimicking. J Adhesion 81:297–317
Benedict CV, Waite JH (1986) Composition and ultrastrcuture of the Byssus of Mytilus edulis. J Morphol 189:261–270
Holten-Andersen N, Fantner GE, Hohlbauch S, Waite JH, Zok FW (2007) Protective coatings on extensible biofibers. Nat Mater 6:669–672
Rzepecki LM, Hansen KM, Waite JH (1992) Characterization of a cystine-rich polyphenolic protein family from the Blue Mussel Mytilus edulis L. Biol Bull 183:123–137
Sun CJ, Waite JH (2005) Mapping chemical gradients within and along a fibrous structural tissue, mussel byssal threads. J Biol Chem 280:39332–39336
Harrington MJ, Waite JH (2007) Holdfast heroics: comparing the molecular and mechanical properties of Mytilus californianus byssal threads. J Exp Biol 210:4307–4318
Zhao H, Waite JH (2006) Linking adhesive and structural proteins in the attachment plaque of Mytilus californianus. J Biol Chem 281:26150–26158
Zhao H, Waite JH (2006) Proteins in load-bearing junctions: the histidine-rich metal-binding protein of mussel byssus. Biochemistry 45:14223–14231
Inoue K, Takeuchi Y, Miki D, Odo S (1995) Mussel adhesive plaque protein gene is a novel member of epidermal growth factor-like gene family. J Biol Chem 270:6698–6701
Waite JH, Qin XX (2001) Polyphosphoprotein from the adhesive pads of Mytilus edulis. Biochemistry 40:2887–2893
Papov VV, Diamond TV, Biemann K, Waite JH (1995) Hydroxyarginine-containing polyphenolic proteins in the adhesive plaques of the marine mussel Mytilus edulis. J Biol Chem 270:20183–20192
Waite JH (1983) Evidence for a repeating 3,4-dihydroxyphenylalanine- and hydroxyproline-containing decapeptide in the adhesive protein of the mussel, Mytilus edulis L. J Biol Chem 258:2911–2915
Inoue K, Odo S (1994) The adhesive protein cDNA of Mytilus galloprovincialis encodes decapeptide repeats but no hexapeptide motif. Biol Bull 186:349–355
Lee H, Scherer NF, Messersmith PB (2006) Single-molecule mechanics of mussel adhesion. Pro Natl Acad Sci USA 103:12999–13003
Sagert J, Sun C, Waite JH (2006) Chemical subtleties of mussel and polychaete holdfasts. In: Smith AM, Callow JA (eds) Biological adhesives. Springer, Berlin, pp 125–140
Yu M, Hwang J, Deming TJ (1999) Role of L-3,4-dihydroxyphenylalanine in mussel adhesive proteins. J Am Chem Soc 121:5825–5826
Nagai A, Yamamoto H (1989) Insolubilizing studies of water-soluble poly(Lys Tyr) by tyrosinase. Bull Chem Soc Jpn 62:2410–2412
Taylor SW, Chase DB, Emptage MH, Nelson MH, Waite JH (1996) Ferric ion complexes of a DOPA-containing adhesive protein from Mytillus edulis. Inorg Chem 35:7572–7577
Sever MJ, Weisser JT, Monahan J, Srinivasan S, Wilker JJ (2004) Metal-mediated cross-linking in the generation of a marine-mussel adhesive. Ang Chem Int Ed 43:448–450
Hwang DS, Zeng H, Masic A, Harrington MJ, Israelachvili JN, Waite JH (2010) Protein- and metal-dependent interactions of a prominent protein in mussel adhesive plaque. J Biol Chem 285:25850–25858
McDowell LM, Burzio LA, Waite JH, Schaefer J (1999) Rotational echo double resonance detection of cross-links formed in mussel byssus under high-flow stress. J Biol Chem 274:20293–20295
Holten-Andersen N, Harrington MJ, Birkedal H, Lee BP, Messersmith PB, Lee KYC, Waite JH (2011) 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
Holten-Andersen N, Mates TE, Toprak MS, Stucky GD, Zok FW, Waite JH (2009) Metals and the integrity of a biological coating: the cuticle of mussel byssus. Langmuir 25:3323–3326
Harrington MJ, Masic A, Holten-Andersen N, Waite JH, Fratzl P (2010) Iron-clad fibers: a metal-based biological strategy for hard flexible coatings. Science 328:216–220
Lin Q, Gourdon D, Sun C, Holten-Andersen N, Anderson TH, Waite JH, Israelachvili JN (2007) Adhesion mechanisms of the mussel foot proteins mfp-1 and mfp-3. Proc Natl Acad Sci USA 104:3782–3786
Shimizu K, Cha J, Stucky GD, Morse DE (1998) Silicatein alpha: cathepsin L-like protein in sponge biosilica. Proc Natl Acad Sci USA 95:6234–6238
Waite JH, Lichtenegger HC, Stucky GD, Hansma P (2004) Exploring molecular and mechanical gradients in structural bioscaffolds. Biochemistry 43:7653–7662
Kamino K (2006) Barnacle underwater attachment. In: Smith AM, Callow JA (eds) Biological adhesives. Springer, Berlin, pp 145–166
Saroyan JR, Lindner E, Dooley CA (1970) Repair and reattachment in the balanidae as related to their cementing mechanism. Biol Bull 139:333–350
Becka A, Loeb G (1984) Ease of removal of barnacles from various polymeric materials. Biotechnol Bioeng 26:1245–1251
Alberte RS, Shyder S, Zahuranec BJ, Whetstone M (1992) Biofouling research need for the united states NAVY: program history and goals. Biofouling 6:91–95
Clare AS, Fusetani N, Jones MB (1998) Introduction: settlement and metamorphosis of marine invertebrate. Biofouling 12:1–2
Sommer S, Ekin A, Webster DC, Stafslien SJ, Daniels J, VanderWal LJ, Thompson SEM, Callow ME, Callow JA (2010) A preliminary study on the properties and fouling-release performance of siloxane-polyurethane coatings prepared from poly(dimethylsiloxane)(PDMS) macromers. Biofouling 26:961–972
Swain G, Schultz MP (1996) The testing and evaluation of non-toxic antifouling coatings. Biofouling 10:187–197
Swain G, Anil A, Baier RE, Chia F, Conte E, Cook A, Hadfield M, Haslbeck E, Holm E et al (2000) Biofouling and barnacle adhesion data for fouling-release coatings subjected to static immersion at seven marine sites. Biofouling 16:331–344
Wendt DE, Kowalke GL, Kim J, Singer IL (2006) Factors that influence elastomeric coating performance: the effect of coating thickness on basal plate morphology, growth and critical removal stress of the barnacle Balanus amphitrite. Biofouling 22:1–9
Berglin M, Gatenholm P (2003) The barnacle adhesive plaque: morphological and chemical differences as a response to substrate properties. Colloids Surf B 28:107–117
Wiegemann M, Watermann B (2003) Peculiarities of barnacle adhesive cured on non-stick surfaces. J Adhesion Sci Technol 14:1957–1977
Ramsay DB, Dickinson GH, Orihuela B, Rittschof D, Wahl KJ (2008) Base plate mechanics of the barnacle Balanus Amphitrite. Biofouling 24:109–118
Naldrett MJ (1993) The importance of sulphur cross-links and hydrophobic interactions in the polymerization of barnacle cement. J Mar Bio Ass UK 73:689–702
Kamino K, Odo S, Maruyama T (1996) Cement proteins of the acorn barnacle, Megabalanus rosa. Biol Bull 190:403–409
Kamino K, Nakano M, Kanai S (2012) Significance of the conformation of building blocks in curing of barnacle underwater adhesive. FEBS J 279:1750–1760
Sullan RMA, Gunari N, Tanur AE, Chan Y, Dickinson GH, Orihuela B, Rittschoff D, Walker GC (2009) Nanoscale structures and mechanics of barnacle cement. Biofouling 25:263–275
Barlow DE, Dickinson GH, Orihuela B, Kulp JL III, Rittschof D, Wahl KJ (2010) Characterization of the adhesive plaque of the barnacle Balanus amhpitrite: amyloid-like nanofibrils are a major component. Langmuir 26:6549–6556
Raman S, Kumar R (2011) Interfacial morphology and nanomechanics of cement of the barnacle, Amphibalanus reticulatus on metallic and non-metalic substrata. Biofouling 27:569–577
Kamino K, Inoue K, Maruyama T, Takamatsu N, Harayama S, Shizuri Y (2000) Barnacle cement proteins: importance of disulfide bonds in their insolubility. J Biol Chem 275:27360–27365
Kamino K (2001) Novel barnacle underwater adhesive protein is a charged amino acid-rich protein constituted by a Cys-rich repetitive sequence. Biochem J 356:503–507
Urushida Y, Nakano M, Matsuda S, Inoue N, Kanai S, Kitamura N, Nishino T, Kamino K (2007) Identification and functional characterization of a novel barnacle cement protein. FEBS J 274:4336–4346
Nakano M, Kamino K Amyloid-like structure in barnacle cement. Unpublished
Dickinson G, Vega IE, Wahl KJ, Orihuela B, Beyley V, Rodriguez EN, Everett RK, Bonaventura J, Rittschof D (2009) Barnacle cement: a polymerization model based on evolutionary concepts. J Exp Biol 212:3499–3510
Kamino K (2010) Absence of cross-linking via trans-glutaminase in the barnacle cement and redefinition of the cement. Biofouling 26:755–760
Mori Y, Urushida Y, Nakano M, Uchiyama S, Kamino K (2007) Calcite-specific coupling protein in barnacle underwater cement. FEBS J 274:6436–6446
Suzuki R, Mori Y, Kamino K, Yamazaki T (2006) 3D-structure of barnacle cement protein, Mrcp-20k. Pept Sci 2005:257–258
Urushida Y, Mori Y, Sano K, Kotera M, Hirose Y, Kanai S, Inoue N, Shimoura Y, Shiba K, Nishino T, Nakasuga A, Shen J-R, Kamino K Identification and characterization of a multi-surface coupling protein in barnacle underwater cement. Unpublished
Jensen RA, Morse DE (1988) The bioadhesive of Phragmatopoma californica tubes: a silk-like cement containing–DOPA. J Comp Physiol B 158:317–324
Stevens MJ, Steren RE, Hlady V, Stewart RJ (2007) Multiscale structure of the underwater adhesive of Phragmatopoma californica: a nanostructured latex with a steep microporosity gradient. Langmuir 23:5045–5049
Waite JH, Jensen RA, Morse DE (1992) Cement precursor proteins of the reef-bilding polychaete Phragmatopoma californica (Fewkes). Biochemistry 31:5733–5738
Zhao H, Sun C, Stewart RL, Waite JH (2005) Cement proteins of the tube-building polychaete Phragtopoma californica. J Biol Chem 280:42938–42944
Stewart RJ, Weaver JC, Morse DE, Waite JH (2004) The tube cement of Phrgmatopoma californica: a solid foam. J Exp Biol 207:4727–4734
Sun C, Fantner GE, Adams J, Hansma PK, Waite JH (2007) The role of calcium and magnesium in the concrete tubes of the sandacastle worm. J Exp Biol 210:1481–1488
Filpula DR, Lee S-M, Link RP, Strusberg SL, Strausberg RL (1990) Structural and functional repetition in a marine mussel adhesive proteins. Biotechnol Prog 6:171–177
Hwang DS, Yoo HJ, Jun JH, Moon WK, Cha HJ (2004) Expression of functional recombinant mussel adhesive protein Mgfp-5 in Escherichia coli. Appl Environ Microbiol 70:3352–3359
Yamamoto H (1987) Synthesis and adhesive studies of marine polypeptides. J Chem Perkin Trans 1:613–618
Yu M, Deming TJ (1998) Synthetic polypeptide mimics of marine adhesives. Macromolecules 31:4739–4745
Lee BP, Dalsin JL, Messersmith BP (2002) Synthesis and gelation of DOPA-modified poly(ethylene glycol) hydrogels. Biomacromology 3:1038–1047
Ninan L, Monahan J, Stroshine RL, Wilker JJ, Shi R (2003) Adhesive strength of marine mussel extracts on porcine skin. Biomaterials 24:4091–4099
Lim S, Kim KR, Choi YS, Kim DK, Hwang D, Cha HJ (2011) In vivo post-translational modifications of recombinant mussel adhesive protein in insect cells. Biotechnol Prog 27:1390–1396
Taylor SW (2002) Chemoenzymatic synthesis of peptidyl 3,4-dihydroxyphenylalanins for structure-activity relationships in marine invertebrate polypeptides. Anal Biochem 302:70–74
Marumo K, Waite JH (1986) Optimization of hydroxylation of tyrosinase and tyrosinase-containing peptides by mushroom tyrosinase. Biochim Biophys Acta 872:98–103
Zeng H, Hwang DS, Israelachvili JN, Waite JH (2010) Strong reversible Fe3+-mediated bridging between dopa-containing protein films in water. Proc Natl Acad Sci 107:12850–12853
Holten-Andersen N, Harrington MJ, Birkedal H, Lee BP, Messersmith PB, Lee KYC, Waite JH (2011) pH-induced metal-ligand cross-links inspired by mussel yield-healing polymer networks with near-covalent elastic moduli. Proc Natl Acad Sci 108:2651–2655
Dalsin JL, Hu BH, Lee BP, Messersmith PB (2003) Mussel adhesive protein mimetic polymers for the preparation of nonfouling surfaces. J Am Chem Soc 125:4253–4258
Dalsin JL, Lin L, Tosatti S, Voros J, Textor M, Messersmith PB (2005) Protein resistance of titanium oxide surfaces modified by biologically inspired mPEG-DOPA. Langmuir 21:640–646
Statz AR, Meagher RJ, Barron AE, Messersmith PB (2005) New peptidemimetic polymers for antifouling surfaces. J Am Chem Soc 127:7972–7973
Statz A, Finlay J, Dalsin J, Callow M, Callow JA, Messersmith PB (2006) Algal antifouling and fouling-release properties of metal surfaces coated with a polymer inspired by marine mussels. Biofouling 22:391–399
Lee H, Dellatore SM, Miller WM, Messersmith PB (2007) Mussel-inspred surface chemistry for multi-functional coatings. Science 318:426–430
Fan X, Lin L, Dalsin JL, Messersmith PB (2005) Biomimetic anchor for surface-initiated polymerization from metal substrates. J Am Chem Soc 127:15843–15847
Su J, Chen F, Messersmith PB (2011) Catechol polymers for pH-responsive, targeted drug delivery to cancer cells. J Am Chem Soc 133:11850–11853
Kamino K (2008) The underwater adhesive of marine organisms as the vital link between biological science and material science. Mar Biotechnol 10:111–121
Yamamoto H, Kuno S, Nagai A, Nishida A, Yamauchi S, Ikeda K (1990) Insolubiliing and adhesive studies of water-soluble synthetic model proteins. Int J Biol Macromol 12:305–310
Wang J, Liu C, Lu X, Yin M (2007) Co-polypeptides of 3,4-dihydroxyphenylalanine and L-lysine to mimic marine adhesive protein. Biomaterials 28:3456–3468
Ninan L, Stroshine RL, Wilker JJ, Shi R (2007) Adhesive strength and curing rate of marine mussel protein extracts on porcine small intestinal submucosa. Acta Biomater 3:687–694
Stewart RJ (2011) Protein-based underwater adhesives and the prospects for their biotechnological production. Appl Microbiol Biotechnol 89:27–33
Shao H, Bachus KN, Stewart RJ (2009) A water-borne adhesive modeled after the sandcastle glue of P. californica. Macromol Biosci 9:464–471
Lim S, Choi YS, Kang DG, Song YH, Cha HJ (2010) The adhesive properties of coacervated recombinant hybrid mussel adhesive proteins. Biomaterials 31:3715–3722
Guvendiren M, Messersmith PB, Shull KR (2008) Self-assembly and adhesion of DOPA-modified methacrylic triblock hydrogels. Biomacromology 9:122–128
Nakano M, Shen JR, Kamino K (2007) Self-assembling peptide inspired by a barnacle adhesive protein. Biomacromology 8:1830–1835
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I greatly appreciate Prof. Jian-Ren Shen of Okayama University for his careful correction of the manuscript.
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Kamino, K. (2013). Diversified Material Designs in Biological Underwater Adhesives. In: Thomopoulos, S., Birman, V., Genin, G. (eds) Structural Interfaces and Attachments in Biology. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-3317-0_9
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