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Biomimetic Approach to Designing Adhesive Hydrogels: From Chemistry to Application

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Part of the book series: Springer Series in Biomaterials Science and Engineering ((SSBSE,volume 5))

Abstract

Marine mussels secrete remarkable underwater adhesives that allow these organisms to anchor to surfaces in turbulent, intertidal zones. A unique amino acid, 3,4-dihydroxyphenylalanine (DOPA), is found in large abundance in these adhesive proteins and DOPA is responsible for both rapid curing of the adhesive and interfacial binding. Chemically linking DOPA and other catechol derivatives onto inert, synthetic polymers has imparted these materials with strong, water-resistant adhesive properties to various biological, metallic, and polymeric substrates. In this chapter, we review the mechanisms behind the unique interfacial binding and intermolecular cross-linking chemistries of DOPA and the use of DOPA in designing adhesive hydrogels with elevated adhesive strength and tunable physical and mechanical properties. The application of these bioadhesives as sealants and adhesives in wound healing, soft tissue reconstruction, immobilization of therapeutic cells, and drug delivery is described.

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References

  1. M. Hidalgo, M.J. Castillo, J.L. Eymar, A. Hidalgo, Lichtenstein inguinal hernioplasty: sutures versus glue. Hernia. 9, 242–244 (2005)

    Article  Google Scholar 

  2. J. Koniger, J. Redecke, M. Butters, Chronic pain after hernia repair: a randomized trial comparing Shouldice, Lichtenstein and TAPP. Langenbecks Arch. Surg. 389, 361–365 (2004)

    Article  Google Scholar 

  3. E. Stark, K. Oestreich, K. Wendl, B. Rumstadt, E. Hagmüller, Nerve irritation after laparoscopic hernia repair. Surg. Endosc. 13, 878–881 (1999)

    Article  Google Scholar 

  4. F.H. Berndsen, U. Petersson, D. Arvidsson, C.E. Leijonmarck, C. Rudberg, S. Smedberg, A. Montgomery, Discomfort five years after laparoscopic and Shouldice inguinal hernia repair: a randomised trial with 867 patients. Hernia. 12, 445–446 (2008)

    Article  Google Scholar 

  5. F.A. Barber, M.A. Herbert, M.H. Boothby, Ultimate tensile failure loads of a human dermal allograft rotator cuff augmentation. Arthroscopy. 24, 20–24 (2008)

    Article  Google Scholar 

  6. F.A. Barber, M.A. Herbert, D.A. Coons, Tendon augmentation grafts: biomechanical failure loads and failure patterns. Arthroscopy. 22, 534–538 (2006)

    Article  Google Scholar 

  7. M.J. Tingart, M. Apreleva, D. Zurakowski, J.J. Warner, Pullout strength of suture anchors used in rotator cuff repair. J. Bone Joint Surg. Am. 85-A, 2190–2198 (2003)

    Google Scholar 

  8. G.L.J. Caldwell, J.J. Warner, M.D. Miller, D. Boardman, J. Towers, R. Debski, Strength of fixation with transosseous sutures in rotator cuff repair. J. Bone Joint Surg. Am. 79, 1064–1068 (1997)

    Google Scholar 

  9. C. Gerber, A.G. Schneeberger, M. Beck, U. Schlegel, Mechanical strength of repairs of the rotator cuff. J. Bone Joint Surg. Am. 76-B, 371–380 (1994)

    Google Scholar 

  10. M. Djurasovic, G. Marra, J.S. Arroyo, R.G. Pollock, E.L. Flatow, L.U. Bigliani, Revision rotator cuff repair: factors influencing results. J. Bone Joint Surg. Am. 83-A, 1849–1855 (2001)

    Google Scholar 

  11. Y. Ikada, Tissue adhesives, in Wound Closure Biomaterials and Devices, ed. by C.C. Chu, J.A. von Fraunhofer, H.P. Greisler (CRC Press, Inc., Boca Raton, 1997), pp. 317–346

    Google Scholar 

  12. M. Mehdizadeh, H. Weng, D. Gyawali, L. Tang, J. Yang Injectable citrate-based mussel-inspired tissue bioadhesives with high wet strength for sutureless wound closure. Biomaterials. 33(32), 7972–7983 2012

    Article  Google Scholar 

  13. J.R. Eriksen, J.I. Bech, D. Linnemann, J. Rosenberg, Laparoscopic intraperitoneal mesh fixation with fibrin sealant (Tisseel) vs. titanium tacks: a randomised controlled experimental study in pigs. Hernia. 12, 483–491 (2008)

    Article  Google Scholar 

  14. E.J. Olivier ten Hallers, J.A. Jansen, H.A.M. Marres, G. Rakhorst, G.J. Verkerke Histological assessment of titanium and polypropylene fiber mesh implantation with and without fibrin tissue glue. J. Biomed Mater. Res. Part A. 80, 372–380 (2006)

    Google Scholar 

  15. R. Saltz, D. Sierra, D. Feldman, M.B. Saltz, A. Dimick, L.O. Vasconez, Experimental and clinical applications of fibrin glue. Plast. Reconstr. Surg. 88, 1005–1015 (1991) discussion 16–7

    Article  Google Scholar 

  16. H. Banninger, T. Hardegger, A. Tobler, A. Barth, P. Schupbach, W. Reinhart, B. Lammle, M. Furlan, Fibrin glue in surgery: frequent development of inhibitors of bovine thrombin and human factor V. Br. J. Haematol. 85, 528–532 (1993)

    Article  Google Scholar 

  17. D.M. Toriumi, W.F. Raslan, M. Friedman, M.E. Tardy Jr., Variable histotoxicity of histoacryl when used in a subcutaneous site: an experimental study. Laryngoscope. 101, 339–343 (1991)

    Google Scholar 

  18. M.F. Brothers, J.C. Kaufmann, A.J. Fox, J.P. Deveikis, n-Butyl 2-cyanoacrylate–substitute for IBCA in interventional neuroradiology: histopathologic and polymerization time studies. AJNR. Am. J. Neuroradiol. 10, 777–786 (1989)

    Google Scholar 

  19. H. Celik, H. Caner, K. Tahta, O.E. Ozcan, A. Erbengi, B. Onol, Nonsuture closure of arterial defect by vein graft using isobutyl-2-cyanoacrylate as a tissue adhesive. J. Neurosurg. Sci. 35, 83–87 (1991)

    Google Scholar 

  20. C.E. Gilbert, I. Grierson, D. McLeod, Retinal patching: a new approach to the management of selected retinal breaks. Eye. 3, 19–26 (1989)

    Article  Google Scholar 

  21. M.E. Hartnett, T. Hirose, Cyanoacrylate glue in the repair of retinal detachment associated with posterior retinal breaks in infants and children. Retina. 18, 125–129 (1998)

    Article  Google Scholar 

  22. A.R. Goldin, Control of duodenal haemorrhage with cyanoacrylate. Br. J. Radiol. 49, 583–588 (1976)

    Article  Google Scholar 

  23. T. Kakio, T. Ito, K. Sue, K. Sakaguchi, T. Shiota, T. Oka, H. Kobashi, N. Sakai, M. Omoto, M. Mikami, Hemostasis of gastric variceal hemorrhage by transileocoecal and transhepatic obliteration. Acta. Med. Okayama. 47, 39–43 (1993)

    Google Scholar 

  24. P.M. Bonutti, G.G. Weiker, J.T. Andrish, Isobutyl cyanoacrylate as a soft tissue adhesive: an in vitro study in the rabbit achilles tendon. Clin. Orthop. Relat. Res. 229, 241–248 (1988)

    Google Scholar 

  25. E.S. Powell, I.A. Trail, J. Noble, Non-suture repair of tendons. J. Biomed. Eng. 11, 215–218 (1989)

    Article  Google Scholar 

  26. C.E. Evans, G.C. Lees, I.A. Trail, Cytotoxicity of cyanoacrylate adhesives to cultured tendon cells. J. Hand. Surg. 24B, 658–661 (1999)

    Article  Google Scholar 

  27. Y.C. Tseng, Y. Tabata, S.H. Hyon, Y. Ikada, In vitro toxicity test of 2-cyanoacrylate polymers by cell culture method. J. Biomed. Mat. Res. 24, 1355–1367 (1990)

    Article  Google Scholar 

  28. M.F. Refojo, C.H. Dohlman, J. Koliopoulos, Adhesives in ophthalmology: a review. Surv. Ophthamol. 15, 217–236 (1971)

    Google Scholar 

  29. R.H. Fortelny, A.H. Petter-Puchner, N. Walder, R. Mittermayr, W. Öhlinger, A. Heinze, H. Redl, Cyanoacrylate tissue sealant impairs tissue integration of macroporous mesh in experimental hernia repair. Surg. Endosc. 21, 1781–1785 (2007)

    Article  Google Scholar 

  30. S.K. Jain, A. Vindal, Gelatin–resorcin–formalin (GRF) tissue glue as a novel technique for fixing prosthetic mesh in open hernia repair. Hernia. 13, 299–304 (2009)

    Article  Google Scholar 

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

    Article  Google Scholar 

  32. J.H. Waite, Nature’s underwater adhesive specialist. Int. J. Adhes. Adhes. 7, 9–14 (1987)

    Article  Google Scholar 

  33. H. Yamamoto, Marine adhesive proteins and some biotechnological applications. Biotechnol. Genet. Eng. Rev. 13, 133–165 (1996)

    Article  Google Scholar 

  34. T.L. Coombs, P.J. Keller, Mytilus byssal threads as an environmental marker for metals. Aquat. Toxicol. 1, 291–300 (1981)

    Article  Google Scholar 

  35. P. Szefer, K. Ikuta, S. Kushiyama, K. Szefer, K. Frelek, J. Geldon, Distribution and association of trace metals in soft tissue and byssus of Mytilus edulis from the east coast of Kyushu Island, Japan. Arch. Environ. Contam. Toxicol. 32, 184–190 (1997)

    Article  Google Scholar 

  36. S. Martin, J. Kesselman, D. Park, N. Lewis, M. Hoffmann, Surface studies of 4-chlorocatechol adsorbed on titanium dioxide. Environ. Sci. Technol. 30, 2535–2542 (1996)

    Article  Google Scholar 

  37. M.J. Sever, J.J. Wilker. Visible absorption spectra of metal-catecholate and metal-tironate complexes. Dalton. Trans. 7, 1061–1072 (2004)

    Article  Google Scholar 

  38. S.W. Taylor, D.B. Chase, M.H. Emptage, M.J. Nelson, J.H. Waite, Ferric Ion complexes of a DOPA-containing adhesive protein from mytilus edulis. Inorg. Chem. 35, 7572–7577 (1996)

    Article  Google Scholar 

  39. S.W. Taylor, G.W. Luther III, J.H. Waite, Polarographic and spectrophotometric investigation of iron(III) complexation to 3,4-Dihydroxyphenylalanine-containing peptides and proteins from mytilus edulis. Inorg. Chem. 33, 5819–5824 (1994)

    Article  Google Scholar 

  40. M.J. Sever, J.J. Wilker, Absorption spectroscopy and binding constants for first-row transition metal complexes of a DOPA-containing peptide. Dalton Trans. 14, 813–22 (2006)

    Article  Google Scholar 

  41. M.J. Harrington, A. Masic, N. Holten-Andersen, J.H. Waite, P. Fratzl, Iron-clad fibers: a metal-based biological strategy for hard flexible coatings. Science. 328, 216–220 (2010)

    Article  Google Scholar 

  42. M.J. Harrington, H.S. Gupta, P. Fratzl, J.H. Waite, Collagen insulated from tensile damage by domains that unfold reversibly: In situ X-ray investigation of mechanical yield and damage repair in the mussel byssus. J. Struct. Biol. 167, 47–54 (2009)

    Article  Google Scholar 

  43. N. Holten-Andersen, M.J. Harrington, H. Birkedal, B.P. Lee, P.B. Messersmith, K.Y.C. Lee, J.H. Waite, pH-induced mussel metal-ligand crosslinks yield self-healing polymer networks with near-covalent elastic moduli. Proc. Natl. Acad. Sci. 15, 2651–2655 (2011) (PMCID: PMC3041094)

    Article  Google Scholar 

  44. R. Kummert, W. Stumm, The surface complexation of organic acids on hydrous g-alumina. J. Colloid Interface Sci. 75, 373–385 (1980)

    Article  Google Scholar 

  45. M.P. Soriaga, A.T. Hubbard, Determination of the orientation of aromatic molecules adsorbed on platinum electrodes. The effect of solute concentration. JACS. 104, 3937–3945 (1982)

    Article  Google Scholar 

  46. D.C. Hansen, S.C. Dexter, J.H. Waite, The inhibition of corrosion of S30403 stainless steel by a naturally occurring catecholic polymer. Corros. Sci. 37, 1423–1441 (1995)

    Article  Google Scholar 

  47. B.P. Lee, C.-Y. Chao, F.N. Nunalee, E. Motan, K.R. Shull, P.B. Messersmith, Rapid photocurable of amphiphilic block copolymers hydrogels with high DOPA contents. Maclomolecules. 39, 1740–1748 (2006)

    Article  Google Scholar 

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

    Article  Google Scholar 

  49. S.A. Mian, X. Gao, S. Nagase, J. Jang, Adsorption of catechol on a wet silica surface: density functional theory study. Theor. Chem. Acc. 130, 333–339 (2011)

    Article  Google Scholar 

  50. S.A. Mian, L.C. Saha, J. Jang, L. Wang, X. Gao, S. Nagase, Density functional theory study of catechol adhesion on silica surfaces. J. Phys. Chem. C. 114, 20793–20800 (2010)

    Article  Google Scholar 

  51. M. Vega-Arroyo, P.R. LeBreton, T. Rajh, P. Zapol, L.A. Curtiss, Density functional study of the TiO2–dopamine complex. Chem. Phys. Lett. 406, 306–311 (2005)

    Article  Google Scholar 

  52. J.L. Dalsin, B.-H. Hu, B.P. Lee, P.B. Messersmith, Mussel adhesive protein mimetic polymers for the preparation of nonfouling surfaces. JACS 125, 4253–4258 (2003)

    Article  Google Scholar 

  53. J.L. Dalsin, L. Lin, P.B. Messersmith, Antifouling performance of poly(ethylene glycol) anchored onto surfaces by mussel adhesive protein mimetic peptides. Polym. Mater. Sci. Eng. 90, 247–248 (2004)

    Google Scholar 

  54. J.L. Dalsin, L. Lin, S. Tosatti, J. Voeroes, M. Textor, P.B. Messersmith, Protein resistance of titanium oxide surfaces modified by biologically inspired mPEG-DOPA. Langmuir. 21, 640–646 (2005)

    Article  Google Scholar 

  55. M.P. Deacon, S.S. Davis, J.H. Waite, S.E. Harding, Structure and mucoadhesion of mussel glue protein in dilute solution. Biochemical. 37, 14108–14112 (1998)

    Article  Google Scholar 

  56. K. Huang, B.P. Lee, D. Ingram, P.B. Messersmith, Synthesis and characterization of self-assembling block copolymers containing Bioadhesive end groups. Biomacromology. 3, 397–406 (2002)

    Article  Google Scholar 

  57. J. Schnurrer, C.-M. Lehr, Mucoadhesive properties of the mussel adhesive protein. Int. J. Pharm. 141, 251–256 (1996)

    Article  Google Scholar 

  58. W.M. Chirdon, W.J. O'Brien, R.E. Robertson, Adsorption of catechol and comparative solutes on hydroxyapatite. J. Biomed. Mat. Res. B. 66B, 532–538 (2003)

    Article  Google Scholar 

  59. A.M. Baty, P.K. Leavitt, C.A. Siedlecki, B.J. Tyler, P.A. Suci, R.E. Marchant, G.G. Geesey, 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. 13, 5702–5710 (1997)

    Article  Google Scholar 

  60. B.R. Baker, A.N. Laiwalla, J.-Y. Yoon, J. Canavate, R.L. Garrell, Adhesion and cohesion of mussel adhesive protein on glass and gold through protein removal studies. Polym. Mater. Sci. Eng. 85, 115–116 (2001)

    Google Scholar 

  61. L.M. McDowell, L.A. Burzio, J.H. Waite, J. Schaefer, Rotational echo double resonance detection of cross-links formed in mussel byssus under high-flow stress. J. Biol. Chem. 274, 20293–20295 (1999)

    Article  Google Scholar 

  62. B.P. Lee, J.L. Dalsin, P.B. Messersmith, Synthesis and gelation of DOPA-modified poly(ethylene glycol) hydrogels. Biomacromology. 3, 1038–1047 (2002)

    Article  Google Scholar 

  63. J.H. Waite, The phylogeny and chemical diversity of quinone-tanned glues and varnishes. Comp. Biochem. Physiol. B. 97, 19–29 (1990)

    Google Scholar 

  64. M. Sugumaran, H. Dali, V. Semensi, Chemical- and cuticular phenoloxidase-mediated synthesis of cysteinyl-catechol adducts. Arch. Insect. Biochem. Physiol. 11, 127–137 (1989)

    Article  Google Scholar 

  65. H. Lee, N.F. Scherer, P.B. Messersmith, Single molecule mechanics of mussel adhesion. Proc. Natl. Acad. Sci. U S A 103, 12999–13003 (2006)

    Article  Google Scholar 

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

    Article  Google Scholar 

  67. B.P. Lee, J.L. Dalsin, P.B. Messersmith. Biomimetic adhesive polymers based on mussel adhesive proteins. Biological Adhesives (Springer, Berlin, 2006), pp. 257–278

    Book  Google Scholar 

  68. J.M. Harris, J.M. Dust, R.A. McGill, P.A. Harris, M.J. Edgell, R.M. Sedaghat-Herati, L.J. Karr, D.L. Donnelly. New polyethylene glycols for biomedical applications. Water-Soluble Polymer. ACS, DC Washington 418–29 (1991)

    Google Scholar 

  69. S.A. Burke, M. Ritter-Jones, B.P. Lee, P.B. Messersmith, Thermal gelation and tissue adhesion of biomimetic hydrogels. Biomed. Mater. 2, 203–210 (2007)

    Article  Google Scholar 

  70. P.B. Messersmith, B.P. Lee, J.L. Dalsin, S.A. Burke, inventors; DOPA-Functionized, Branched, Poly(Aklylene Oxide) Adhesives patent US Patent Application 20080247984 2008

    Google Scholar 

  71. J.L. Dalsin, B.P. Lee, L. Vollenweider, S. Silvary, J.L. Murphy, F. Xu, A. Spitz, A. Lyman, inventors; Multi-armed Catechol Compound Blends. US patent 8,119,742, 2012

    Google Scholar 

  72. J.H. Ryu, Y. Lee, W.H. Kong, T.G. Kim, T.G. Park, H. Lee, Catechol-functionalized chitosan/pluronic hydrogels for tissue adhesives and hemostatic materials. Biomacromology. 12, 2653–2659 (2011)

    Article  Google Scholar 

  73. Y. Lee, H.J. Chung, S. Yeo, C.-H. Ahn, H. Lee, P.B. Messersmith, T.G. Park, Thermo-sensitive, injectable, and tissue adhesive sol-gel transition hyaluronic acid/pluronic composite hydrogels prepared from bio-inspired catechol-thiol reaction. Soft. Matter. 6, 977–983 (2010)

    Article  Google Scholar 

  74. C.J. Kastrup, M. Nahrendorf, J.L. Figueiredo, H. Lee, S. Kambhampati, T. Lee, S.W. Cho, R. Gorbatov, Y. Iwamoto, T.T. Dang, P. Dutta, J.H. Yeon, H. Cheng, C.D. Pritchard, A.J. Vegas, C.D. Siegel, S. MacDougall, M. Okonkwo, A. Thai, J.R. Stone, A.J. Coury, R. Weissleder, R. Langer, D.G. Anderson, Painting blood vessels and atherosclerotic plaques with an adhesive drug depot. Proc. Natl. Acad. Sci. U S A. 109, 21444–21449 (2012)

    Article  Google Scholar 

  75. B.P. Lee, inventorB. Compounds, S.M. Therefor, US patent 7,622,533. 2009

    Google Scholar 

  76. B.P. Lee, inventorB. Compounds, S.M. Therefor, US patent 8,030,413. 2011

    Google Scholar 

  77. C.E. Brubaker, P.B. Messersmith, Enzymatically degradable mussel-inspired adhesive hydrogel. Biomacromolecules. 12, 4326–4334 (2011)

    Article  Google Scholar 

  78. F. Ganji, S. Vasheghani-Farahani, E. Vasheghani-Farahani, Theoretical description of hydrogel swelling: a review. Iran. Polym. J. 19, 375–398 (2010)

    Google Scholar 

  79. D.G. Barrett, G.G. Bushnell, PB Messersmith, Mechanically robust, negative-swelling, mussel-inspired tissue adhesives. Adv. Healthc. Mater. 2, 745–755 (2013)

    Article  Google Scholar 

  80. K. Haraguchi, Synthesis and properties of soft nanocomposite materials with novel organic/inorganic network structures. Polym. J. 43, 223–241 (2011)

    Article  Google Scholar 

  81. S. Sarkar, E. Guibal, F. Quignard, A. SenGupta, Polymer-supported metals and metal oxide nanoparticles: synthesis, characterization, and applications. J. Nanopart. Res. 14, 1–24 (2012)

    Google Scholar 

  82. A.K. Gaharwar, S.A. Dammu, J.M. Canter, C.J. Wu, G. Schmidt, Highly extensible, tough, and elastomeric nanocomposite hydrogels from poly(ethylene glycol) and hydroxyapatite nanoparticles. Biomacromology. 12, 1641–1650 (2011)

    Article  Google Scholar 

  83. K. Haraguchi, R. Farnworth, A. Ohbayashi, T. Takehisa, Compositional effects on mechanical properties of nanocomposite hydrogels composed of poly(N, N-dimethylacrylamide) and clay. Macromology. 36, 5732–5741 (2003)

    Article  Google Scholar 

  84. T. Wang, D. Liu, C. Lian, S. Zheng, X. Liu, Z. Tong, Large deformation behavior and effective network chain density of swollen poly(N-isopropylacrylamide)-Laponite nanocomposite hydrogels. Soft. Matter. 8, 774–783 (2012)

    Article  Google Scholar 

  85. S. Skelton, M. Bostwick, K. O'Connor, S. Konst, S. Casey, B.P. Lee, Biomimetic adhesive containing nanocomposite hydrogel with enhanced materials properties. Soft. Matter. 9, 3825–3833 (2013)

    Article  Google Scholar 

  86. Y. Liu, H. Zhan, S. Skelton, B.P. Lee, Marine adhesive containing nanocomposite hydrogel with enhanced materials and bioadhesive properties. MRS Proceedings. 2013;1569:mrss13-1569-LL05–09.

    Google Scholar 

  87. L. Ansaloni, F. Catena, S. Gagliardi, F. Gazzotti, L. D'Alessandro, A.D. Pinna, Hernia repair with porcine small-intestinal submucosa. Hernia. 11, 321–326 (2007)

    Article  Google Scholar 

  88. F. Catena, L. Ansaloni, F. Gazzotti, S. Gagliardi, S. Di Saverio, L. D'Alessandro, A.D. Pinna, Use of porcine dermal collagen graft (permacol) for hernia repair in contaminated fields. Hernia. 11, 57–60 (2007)

    Article  Google Scholar 

  89. M.E.J. Franklin, J.J. Gonzalez Jr., J.L. Glass, Use of porcine small intestinal submucosa as a prosthetic device for laparoscopic repair of hernias in contaminated fields: 2-year follow-up. Hernia. 8, 186–189 (2004)

    Google Scholar 

  90. D.K. Lee, Achilles tendon repair with acellular tissue graft augmentation in neglected ruptures. J. Foot. Ankle. Surg. 46, 451–455 (2007)

    Article  Google Scholar 

  91. J.L. Bond, R.M. Dopirak, J. Higgins, J. Burns, S.J. Snyder, Arthroscopic replacement of massive, irreparable rotator cuff tears using a graftjacket allograft: technique and preliminary results. Arthroscopy. 24, 403–409 (2008)

    Article  Google Scholar 

  92. J.A. Santibáñez-Salgado, J.R. Olmos-Zúñiga, M. Pérez-López, C. Aboitiz-Rivera, M. Gaxiola-Gaxiola, R. Jasso-Victoria, A. Sotres-Vega, M. Baltazares-Lipp, J.V.-C. Pérez-Covarrubias D, Lyophilized glutaraldehyde-preserved bovine pericardium for experimental atrial septal defect closure. Eur. Cell. Mater. 19, 158–165 (2010)

    Google Scholar 

  93. P.K. Narotam, K. Reddy, D. Fewer, F. Qiao, N. Nathoo, Collagen matrix duraplasty for cranial and spinal surgery: a clinical and imaging study. J. Neurosurg. 106, 45–51 (2007)

    Article  Google Scholar 

  94. T.P. Rauth, B.K. Poulose, L.B. Nanney, M.D. Holzman, A comparative analysis of expanded Polytetrafluoroethylene and small intestinal submucosa—implications for patch repair in ventral herniorrhaphy. J. Surg. Res. 143, 43–49 (2007)

    Article  Google Scholar 

  95. J.C.J. Lantis, E.K. Gallivan, R. Hekier, R. Connolly, S.D. Schwaitzberg, A comparison of collagen and PTFE patch repair in a rabbit model of congenital diaphragmatic hernia. J. Invest. Surg. 13, 319–325 (2000)

    Article  Google Scholar 

  96. M.L. Konstantinovic, P. Lagae, F. Zheng, E.K. Verbeken, D. De Ridder, J.A. Deprest, Comparison of host response to polypropylene and non-cross-linked porcine small intestine serosal-derived collagen implants in a rat model. J. Obstet. Gynecol. 112, 1554–1560 BJOG: an International (2005)

    Google Scholar 

  97. W.B. Gaertner, M.E. Bonsack, J.P. Delaney, Experimental evaluation of four biologic prostheses for ventral hernia repair. J. Gastrointest Surg. 11, 1275–1285 (2007)

    Article  Google Scholar 

  98. B. Hohendorff, W. Siepen, L. Spiering, L. Staub, T. Schmuck, A. Boss, Long-term results after operatively treated Achilles tendon rupture: fibrin glue versus suture. J. Foot Ankle Surg. 47, 392–399 (2008)

    Article  Google Scholar 

  99. B. Hohendorff, W. Siepen, L. Staub, Treatment of acute Achilles tendon rupture: fibrin glue versus fibrin glue augmented with plantaris longus tendon. J. Foot Ankle Surg. 48, 439–446 (2009)

    Article  Google Scholar 

  100. J.L. Murphy, L. Vollenweider, F. Xu, B.P. Lee. Adhesive performance of biomimetic adhesive-coated biologic scaffolds. Biomacromol.11, 2976–2984 (2010) PMCID: PMC3027843

    Article  Google Scholar 

  101. B.P. Lee, J.L. Dalsin, L. Vollenweider, J.L. Murphy, F. Xu, J. Virosco, W. Lew, J. White, inventors; Bioadhesive constructs. US patent 8,383,092. 2013

    Google Scholar 

  102. R. Devlieger, L.K. Millar, G. Bryant-Greenwood, L. Lewi, J. Deprest, Fetal membrane healing after spontaneous and iatrogenic membrane rupture: a review of current evidence. Am. J. Obstet. Gynecol. 195, 1512–1520 (2006)

    Article  Google Scholar 

  103. G. Bilic, C. Brubaker, P.B. Messersmith, A.S. Mallik, T.M. Quinn, C. Haller, E. Done, L. Gucciardo, S.M. Zeisberger, R. Zimmermann, J. Deprest, A.H. Zisch, Injectable candidate sealants for fetal membrane repair: bonding and toxicity in vitro. Am. J. Obstet. Gynecol.202(85), e1-9 (2010) PMCID: PMC2837921

    Google Scholar 

  104. C.M. Haller, W. Buerzle, A. Kivelio, M. Perrini, C.E. Brubaker, R.J. Gubeli, A.S. Mallik, W. Weber, P.B. Messersmith, E. Mazza, N. Ochsenbein-Koelble, R. Zimmermann, M. Ehrbar, Mussel-mimetic tissue adhesive for fetal membrane repair: an ex vivo evaluation. Acta. Biomater. 8, 4365–4370 (2012)

    Article  Google Scholar 

  105. M. Mehdizadeh, H. Weng, D. Gyawali, L. Tang, J. Yang, Injectable citrate-based mussel-inspired tissue bioadhesives with high wet strength for sutureless wound closure. Biomaterials. 33, 7972–7983 (2012) PMCID: 3432175

    Article  Google Scholar 

  106. The facts about diabetes: a leading cause of death in the U.S. [database on the Internet]. National Diabetes Education Program. 2011.http://ndep.nih.gov/media/fs_gensnapshot.pdf. Accessed July 2013.

  107. M. Peyrot, A.H. Barnett, L.F. Meneghini, P.M. Schumm-Draeger, Insulin adherence behaviours and barriers in the multinational global attitudes of patients and physicians in insulin therapy study. Diabet. Med. 29, 682–689 (2012)

    Article  Google Scholar 

  108. A.M.J. Shapiro, J.R.T. Lakey, E.A. Ryan, G.S. Korbutt, E. Toth, G.L. Warnock, N.M. Kneteman, R.V. Rajotte, Islet transplantation in seven patients with type 1 diabetes mellitus using a glucocorticoid-free immunosuppressive regimen. N. Engl. J. Med. 343, 230–238 (2000)

    Article  Google Scholar 

  109. D.J. van der Windt, R. Bottino, A. Casu, N. Campanile, D.K.C. Cooper, Rapid loss of intraportally transplanted islets: an overview of pathophysiology and preventive strategies. Xenotransplantation. 14, 288–297 (2007)

    Article  Google Scholar 

  110. L. Moberg, O. Korsgren, B. Nilsson, Neutrophilic granulocytes are the predominant cell type infiltrating pancreatic islets in contact with ABO-compatible blood. Clin. Exp. Immunol. 142, 125–131 (2005)

    Article  Google Scholar 

  111. W. Bennet, C.G. Groth, R. Larsson, B. Nilsson, O. Korsgren, Isolated human islets trigger an instant blood mediated inflammatory reaction: Implications for intraportal islet transplantation as a treatment for patients with type 1 diabetes. Ups. J. Med. Sci. 105, 125–133 (2000)

    Google Scholar 

  112. C.E. Brubaker, H. Kissler, L.-J. Wang, D.B. Kaufman, P.B. Messersmith, Biological performance of mussel-inspired adhesive in extrahepatic islet transplantation. Biomaterials. 31, 420–427 (2010) PMCID: PMC2783676

    Article  Google Scholar 

  113. E. Simone, B.-S. Ding, V. Muzykantov, Targeted delivery of therapeutics to endothelium. Cell. Tissue. Res. 335, 283–300 (2009)

    Article  Google Scholar 

  114. J. Leppilahti, S. Orava, Total Achilles Tendon Rupture: A Review. Sports. Med. 25, 79–100 (1998)

    Article  Google Scholar 

  115. E.J. Strauss, C. Ishak, L. Jazrawi, O. Sherman, J. Rosen, Operative treatment of acute achilles tendon ruptures: an institutional review of clinical outcomes. Injury, Int. J. Care Inj. 38, 832–838 (2007)

    Article  Google Scholar 

  116. D.W. White, J.C. Wenke, D.S. Mosely, S.B. Mountcastle, C.J. Basamania, Incidence of major tendon ruptures and anterior cruciate ligament tears in US army soldiers. Am. J. Sports Med. 35, 1308–1314 (2007)

    Article  Google Scholar 

  117. N. Maffulli, Rupture of the achilles tendon. J. Bone Joint Surg. 81-A, 1019–1036 (1999)

    Google Scholar 

  118. S. Houshian, T. Tscherning, P. Riegels-Nielsen, The epidemiology of Achilles tendon rupture in a Danish county. Injury. 29, 651–654 (1998)

    Article  Google Scholar 

  119. A. Pajala, J. Kangas, P. Ohtonen, J. Leppilahti, Rerupture and deep infection following treatment of total achilles tendon rupture. J. Bone Joint Surg. 84-A, 2016–2021 (2002)

    Google Scholar 

  120. L. Nistor, Surgical and non-surgical treatment of achilles tendon rupture. J. Bone Joint Surg. 63-A, 394–399 (1981)

    Google Scholar 

  121. E. Winter, K. Weise, S. Weller, T. Ambacher, Surgical repair of achilles tendon rupture: comparison of surgical with conservative treatment. Arch. Orthop. Trauma Surg. 117, 364–367 (1998)

    Article  Google Scholar 

  122. F.J. Kummer, K. Iesaka, The role of graft materials in suture augmentation for tendon repairs and reattachment. J. Biomed. Mater. Res. Part B: Appl. Biomater. 2005;74B:789–91.

    Article  Google Scholar 

  123. M. Brodie, L. Vollenweider, J.L. Murphy, F. Xu, A. Lyman, W.D. Lew, B.P. Lee, Biomechanical properties of achilles tendon repair augmented with bioadhesive-coated scaffold. Biomed. Mater. 6, 015014 (2011) PMCID: PMC3046464

    Article  Google Scholar 

  124. R.H. Gelberman, M.I. Boyer, M.D. Brodt, S.C. Winters, M.J. Silva, The effect of gap formation at the repair site on the strength and excursion of intrasynovial flexor tendons: an experimental study on the early stages of tendon-healing in dogs. J. Bone Joint Surg. 81 A, 975–982 (1999)

    Google Scholar 

  125. M.I. Boyer, R.H. Gelberman, M.E. Burns, H. Dinopoulos, R. Hofem, M.J. Silva, Intrasynovial flexor tendon repair an experimental study comparing low and high levels of in vivo force during rehabilitation in canines. J. Bone Joint Surg. 83, 891–899 (2001)

    Google Scholar 

  126. N.D. Braulta, C. Gaoa, H. Xuea, M. Piliarik, J. Homolab, S. Jianga, Q. Yua, Ultra-low fouling and functionalizable zwitterionic coatings grafted onto SiO2 via a biomimetic adhesive group for sensing and detection in complex media. Biosens. Bioelectron. 25, 2276–2282 (2010)

    Article  Google Scholar 

  127. A.R. Statz, R.J. Meagher, A.E. Barron, P.B. Messersmith, New peptidomimetic polymers for antifouling surfaces. JACS 127, 7972–7973 (2005)

    Article  Google Scholar 

  128. R. Ko, P.A. Cadieux, J.L. Dalsin, B.P. Lee, C.N. Elwood, H. Razvi, Novel uropathogen-resistant coatings inspired by marine mussels. J. Endourol. 22, 1153–1160 (2008)

    Article  Google Scholar 

  129. A. Pechey, C.N. Elwood, G.R. Wignall, J.L. Dalsin, B.P. Lee, M. Vanjecek, I. Welch, R. Ko, H. Razvi, P.A. Cadieux, Anti-adhesive coating and clearance of device associated uropathogenic escherichia coli cystitis. J. Urol. 182, (2009) 1628–1636 PMCID: PMC2807180

    Article  Google Scholar 

  130. T.S. Sileika, H.-D. Kim, P. Maniak, P.B. Messersmith, Antibacterial performance of polydopamine-modified polymer surfaces containing passive and active components. ACS Appl. Mater. Interfaces. 3, 4602–4610 (2011)

    Article  Google Scholar 

  131. J. Cui, Y. Wang, A. Postma, J. Hao, L. Hosta-Rigau, F. Caruso, Monodisperse polymer capsules: tailoring size, shell thickness, and hydrophobic cargo loading via emulsion templating. Adv. funct. mater. 20, 1625–1631 (2010)

    Article  Google Scholar 

  132. J. Su, F. Chen, V.L. Cryns, P.B. Messersmith, Catechol polymers for pH-responsive, targeted drug delivery to cancer cells. JACS. 133, 11850–11853 (2011)

    Article  Google Scholar 

  133. H.J. Lee, A.N. Koo, S.W. Lee, M.H. Lee, S.C. Lee, Catechol-functionalized adhesive polymer nanoparticles for controlled local release of bone morphogenetic protein-2 from titanium surface. J. Control. Release. 170, 198–208 (2013)

    Article  Google Scholar 

  134. R. Gunawan, J. King, B.P. Lee, P.B. Messersmith, W. Miller, Surface presentation of bioactive ligands in a non-adhesive background using DOPA-Tethered biotinylated poly(ethylene glycol). Langmuir. 23, 10635–10643 (2007)

    Article  Google Scholar 

  135. S.H. Ku, C.B. Park, Human endothelial cell growth on mussel-inspired nanofiber scaffold for vascular tissue engineering. Biomaterials. 31, 9431–9437 (2010)

    Article  Google Scholar 

  136. L. He, D.E. Fullenkamp, J.G. Rivera, P.B. Messersmith, pH responsive self-healing hydrogels formed by boronate–catechol complexation. Chem. Commun. 47, 7497–7499 (2011)

    Article  Google Scholar 

  137. P. Podsiadlo, Z. Liu, D. Paterson, P.B. Messersmith, N.A. Kotov, Fusion of seashell nacre and marine bioadhesive analogs: high strength nanocomposite by LBL of clay and DOPA-polymer. Adv. Mat. 19, 949–955 (2007)

    Article  Google Scholar 

  138. M. Lee, J. Rho, D.-E. Lee, S. Hong, S.-J. Choi, P.B. Messersmith, H. Lee, Water detoxification by a substrate-bound catecholamine adsorbent. ChemPlusChem. 77, 987–990 (2012)

    Article  Google Scholar 

  139. X. Jia, Z.Y. Ma, G.X. Zhang, J.M. Hu, Z.Y. Liu, H.Y. Wang, F. Zhou, Polydopamine film coated controlled-release multielement compound fertilizer based on mussel-inspired chemistry. J. Agric. Food Chem. 61, 2919–2924 (2013)

    Article  Google Scholar 

  140. X.-D. Pan, Z. Qina, Y.-Y. Yana, P. Sadhukhana, Elastomers with chain-end mussel-mimetic modification for nanocomposites: strong modifications to reinforcement and viscoelastic properties. Polymer. 51, 3453–3461 (2010)

    Article  Google Scholar 

  141. M.-H. Ryou, J. Kim, I. Lee, S. Kim, Y.K. Jeong, S. Hong, J.H. Ryu, T.-S. Kim, J.-K. Park, H. Lee, J.W. Choi, Lithium-Ion batteries: mussel-inspired adhesive binders for high-performance silicon nanoparticle anodes in lithium-ion batteries. Adv. Mat. 25, 1571–1576 (2013)

    Article  Google Scholar 

  142. G. Westwood, T.N. Horton, J.J. Wilker, Simplified polymer mimics of cross-linking adhesive proteins. Maclomolecules. 40, 3960–3964 (2007)

    Article  Google Scholar 

  143. D.E. Fullenkamp, L. He, D.G. Barrett, W.R. Burghardt, P.B. Messersmith, Mussel-inspired histidine-based transient network metal coordination hydrogels. Macromology. 46, 1167–1174 (2013)

    Article  Google Scholar 

  144. E. Bell, J. Gosline, Mechanical design of mussel byssus: material yield enhances attachment strength. J. Exp. Biol. 199, 1005–1017 (1996)

    Google Scholar 

  145. A. Tamarin, P. Lewis, J. Askey, The structure and formation of the byssus attachment plaque in mytilus. J. Morphol. 149, 199–221 (1976)

    Article  Google Scholar 

  146. S. Suresh, Graded materials for resistance to contact deformation and damage. Science. 292, 2447–2451 (2001)

    Article  Google Scholar 

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The authors would like to acknowledge National Institutes of Health (GM104846) for financial support.

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Li, Y., Lee, B. (2016). Biomimetic Approach to Designing Adhesive Hydrogels: From Chemistry to Application. In: Zhang, M., Naik, R., Dai, L. (eds) Carbon Nanomaterials for Biomedical Applications. Springer Series in Biomaterials Science and Engineering, vol 5. Springer, Cham. https://doi.org/10.1007/978-3-319-22861-7_15

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