Abstract
Adhesives with catechol moieties have been widely investigated in recent years. However, actually how much catechol groups for these mussel bio-inspired adhesives, especially in their natural form under physiological condition, is appropriate to bond with organic substrates has not been studied intensively. This study blends ε-polylysine (PL), featuring laterally grafted catechols under physiological conditions (pH 7.4), with oxidized dextran to form a hydrogel in situ via the Schiff base without introducing small cytotoxic molecules as crosslinking agents. It finds that the amount of catechol groups imposes an obvious influence on gelation time, swelling behavior, and hydrogel morphology. Both the storage modulus and adhesion strength are found to increase first and decrease afterwards with an increase of pendent catechol content. Furthermore, catechol hydrogen interactions and the decrease in the crosslink density derived from the decrease of amino groups on PL are simultaneously found to affect the storage modulus. Meanwhile, multiple hydrogen-bonding interactions of catechol with amino, hydroxyl, and carboxyl groups, which are in abundance on the surface of tissue, are mainly found to provide an adhesive force. The study finds that with more catechol, there is a greater chance that the cohesive force will weaken, making the entire adhesion strength of the hydrogel decrease. Using a cytotoxicity test, the nontoxicity of the hydrogel towards the growth of L929 cells is proven, indicating that hydrogels have potential applications in soft tissue repair under natural physiological conditions.
Similar content being viewed by others
References
Mehdizadeh M, Yang J. Design strategies and applications of tissue bioadhesives. Macromol Biosci. 2013;13:271–88.
Duarte A, Coelho J, Bordado J, Cidade M, Gil M. Surgical adhesives: systematic review of the main types and development forecast. Prog Polym Sci. 2012;37:1031–50.
Thetter O. Fibrin adhesive and its application in thoracic surgery. Thorac Cardiov Surg. 1981;29:290–2.
Kim BJ, Oh DX, Kim S, Seo JH, Hwang DS, Masic A, et al. Mussel-mimetic protein-based adhesive hydrogel. Biomacromolecules. 2014;15:1579–85.
Mehdizadeh M, Weng H, Gyawali D, Tang L, Yang J. Injectable citrate-based mussel-inspired tissue bioadhesives with high wet strength for sutureless wound closure. Biomaterials. 2012;33:7972–83.
Bae KH, Wang L-S, Kurisawa M. Injectable biodegradable hydrogels: progress and challenges. J Mater Chem B. 2013;1:5371–88.
Deming TJ. Synthetic polypeptides for biomedical applications. Prog Polym Sci. 2007;32:858–75.
Ko DY, Shinde UP, Yeon B, Jeong B. Recent progress of in situ formed gels for biomedical applications. Prog Polym Sci. 2013;38:672–701.
Hyon SH, Nakajima N, Sugai H, Matsumura K. Low cytotoxic tissue adhesive based on oxidized dextran and epsilon-poly-l-lysine. J Biomed Mater Res A. 2014;102:2511–20.
Li Y, Liu C, Tan Y, Xu K, Lu C, Wang P. In situ hydrogel constructed by starch-based nanoparticles via a Schiff base reaction. Carbohyd Polym. 2014;110:87–94.
Wang T, Nie J, Yang D. Dextran and gelatin based photocrosslinkable tissue adhesive. Carbohyd Polym. 2012;90:1428–36.
Shukla SC, Singh A, Pandey AK, Mishra A. Review on production and medical applications of ɛ-polylysine. Biochem Eng J. 2012;65:70–81.
Nakajima N, Sugai H, Tsutsumi S, Hyon SH. Self-degradable bioadhesive. Key Eng Mater. 2007;342:713–6.
Takaoka M, Nakamura T, Sugai H, Bentley AJ, Nakajima N, Fullwood NJ, et al. Sutureless amniotic membrane transplantation for ocular surface reconstruction with a chemically defined bioadhesive. Biomaterials. 2008;29:2923–31.
Lee BP, Messersmith PB, Israelachvili JN, Waite JH. Mussel-inspired adhesives and coatings. Annu Rev Mater Res. 2011;41:99.
Sedó J, Saiz-Poseu J, Busqué F, Ruiz-Molina D. Catechol-based biomimetic functional materials. Adv Mater. 2013;25:653–701.
Bouten PJ, Zonjee M, Bender J, Yauw ST, van Goor H, van Hest J, et al. The chemistry of tissue adhesive materials. Prog Polym Sci. 2014;39:1375–405.
Burke SA, Ritter-Jones M, Lee BP, Messersmith PB. Thermal gelation and tissue adhesion of biomimetic hydrogels. Biomed Mater. 2007;2:203.
Choi YC, Choi JS, Jung YJ, Cho YW. Human gelatin tissue-adhesive hydrogels prepared by enzyme-mediated biosynthesis of DOPA and Fe3+ ion crosslinking. J Mater Chem B. 2014;2:201–9.
Oh DX, Hwang DS. A biomimetic chitosan composite with improved mechanical properties in wet conditions. Biotechnol Progr. 2013;29:505–12.
Zhang H, Bré LP, Zhao T, Zheng Y, Newland B, Wang W. Mussel-inspired hyperbranched poly (amino ester) polymer as strong wet tissue adhesive. Biomaterials. 2014;35:711–9.
Huang K, Lee BP, Ingram DR, Messersmith PB. Synthesis and characterization of self-assembling block copolymers containing bioadhesive end groups. Biomacromolecules. 2002;3:397–406.
Yavvari PS, Srivastava A. Robust, self-healing hydrogels from catechol rich polymers. J Mater Chem B. 2015;3:899–910.
Xu J, Zhou Z, Wu B, He B. Enzymatic formation of a novel cell-adhesive hydrogel based on small peptides with a laterally grafted l-3,4-dihydroxyphenylalanine group. Nanoscale. 2014;6:1277–80.
Yu M, Hwang J, Deming TJ. Role of l-3,4-dihydroxyphenylalanine in mussel adhesive proteins. J Am Chem Soc. 1999;121:5825–6.
Jenkins CL, Meredith HJ, Wilker JJ. Molecular weight effects upon the adhesive bonding of a mussel mimetic polymer. ACS Appl Mater Int. 2013;5:5091–6.
Matos-Pérez CR, White JD, Wilker JJ. Polymer composition and substrate influences on the adhesive bonding of a biomimetic, cross-linking polymer. J Am Chem Soc. 2012;134:9498–505.
Meredith HJ, Jenkins CL, Wilker JJ. Enhancing the adhesion of a biomimetic polymer yields performance rivaling commercial glues. Adv Funct Mater. 2014;24:3259–67.
Maia J, Ferreira L, Carvalho R, Ramos MA, Gil MH. Synthesis and characterization of new injectable and degradable dextran-based hydrogels. Polymer. 2005;46:9604–14.
Hoffmann B, Volkmer E, Kokott A, Augat P, Ohnmacht M, Sedlmayr N, et al. Characterisation of a new bioadhesive system based on polysaccharides with the potential to be used as bone glue. J Mater Sci Mater Med. 2009;20:2001–9.
Saxer S, Portmann C, Tosatti S, Gademann K, Zürcher S, Textor M. Surface assembly of catechol-functionalized poly(l-lysine)-graft-poly (ethylene glycol) copolymer on titanium exploiting combined electrostatically driven self-organization and biomimetic strong adhesion. Macromolecules. 2009;43:1050–60.
Jin R, Hiemstra C, Zhong Z, Feijen J. Enzyme-mediated fast in situ formation of hydrogels from dextran-tyramine conjugates. Biomaterials. 2007;28:2791–800.
JungáChung H, GwanáPark T. Thermo-sensitive, injectable, and tissue adhesive sol-gel transition hyaluronic acid/pluronic composite hydrogels prepared from bio-inspired catechol-thiol reaction. Soft Matter. 2010;6:977–83.
Kull S, Martinelli I, Briganti E, Losi P, Spiller D, Tonlorenzi S, et al. Glubran2 surgical glue. In vitro evaluation of adhesive and mechanical properties. J Surg Res. 2009;157:e15–21.
Ninan L, Monahan J, Stroshine RL, Wilker JJ, Shi R. Adhesive strength of marine mussel extracts on porcine skin. Biomaterials. 2003;24:4091–9.
Chung H, Grubbs RH. Rapidly cross-linkable dopa containing terpolymer adhesives and PEG-based cross-linkers for biomedical applications. Macromolecules. 2012;45:9666–73.
Weng L, Chen X, Chen W. Rheological characterization of in situ crosslinkable hydrogels formulated from oxidized dextran and N-carboxyethyl chitosan. Biomacromolecules. 2007;8:1109–15.
Zhou Y, Nie W, Zhao J, Yuan X. Rapidly in situ forming adhesive hydrogel based on a PEG-maleimide modified polypeptide through Michael addition. J Mater Sci Mater Med. 2013;24:2277–86.
Peak CW, Wilker JJ, Schmidt G. A review on tough and sticky hydrogels. Colloid Polym Sci. 2013;291:2031–47.
Zhang F, Liu S, Zhang Y, Wei Y, Xu J. Underwater bonding strength of marine mussel-inspired polymers containing DOPA-like units with amino groups. RSC Adv. 2012;2:8919–21.
Weng L, Romanov A, Rooney J, Chen W. Non-cytotoxic, in situ gelable hydrogels composed of N-carboxyethyl chitosan and oxidized dextran. Biomaterials. 2008;29:3905–13.
Zhang H, Qadeer A, Chen W. In situ gelable interpenetrating double network hydrogel formulated from binary components: thiolated chitosan and oxidized dextran. Biomacromolecules. 2011;12:1428–37.
Sparks BJ, Hoff EF, Hayes LP, Patton DL. Mussel-inspired thiolene polymer networks: influencing network properties and adhesion with catechol functionality. Chem Mater. 2012;24:3633–42.
Tung CYM, Dynes PJ. Relationship between viscoelastic properties and gelation in thermosetting systems. J Appl Polym Sci. 1982;27:569–74.
Winter HH, Chambon F. Analysis of linear viscoelasticity of a crosslinking polymer at the gel point. J Rheol (1978–present). 1986;30:367–82.
Hong S, Yang K, Kang B, Lee C, Song IT, Byun E, et al. Hyaluronic acid catechol: a biopolymer exhibiting a pH-dependent adhesive or cohesive property for human neural stem cell engineering. Adv Funct Mater. 2013;23:1774–80.
Lih E, Lee JS, Park KM, Park KD. Rapidly curable chitosan–PEG hydrogels as tissue adhesives for hemostasis and wound healing. Acta Biomater. 2012;8:3261–9.
Serrero A, Trombotto S, Bayon Y, Gravagna P, Montanari S, David L. Polysaccharide-based adhesive for biomedical applications: correlation between rheological behavior and adhesion. Biomacromolecules. 2011;12:1556–66.
Wang J, Liu C, Lu X, Yin M. Co-polypeptides of 3,4-dihydroxyphenylalanine and l-lysine to mimic marine adhesive protein. Biomaterials. 2007;28:3456–68.
Acknowledgments
The authors respectively acknowledge the support of this research from the National Natural Science Foundation of China. (Grant 51103095).
Author information
Authors and Affiliations
Corresponding author
Additional information
Mingming Ye and Rui Jiang have contributed equally to this article.
Rights and permissions
About this article
Cite this article
Ye, M., Jiang, R., Zhao, J. et al. In situ formation of adhesive hydrogels based on PL with laterally grafted catechol groups and their bonding efficacy to wet organic substrates. J Mater Sci: Mater Med 26, 273 (2015). https://doi.org/10.1007/s10856-015-5608-y
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s10856-015-5608-y