Mussel-Inspired Adhesive Hydrogels: Chemistry and Biomedical Applications†
Jingsi Chen
Department of Chemical and Materials Engineering, University of Alberta, Edmonton, Alberta, T6G 1H9 Canada
Search for more papers by this authorLinbo Han
College of Health Science and Environmental Engineering, Shenzhen Technology University, Shenzhen, Guangdong, 518118 China
Search for more papers by this authorJifang Liu
The Fifth Affiliated Hospital, Guangzhou Medical University, Guangzhou, Guangdong, 510700 China
Search for more papers by this authorCorresponding Author
Hongbo Zeng
Department of Chemical and Materials Engineering, University of Alberta, Edmonton, Alberta, T6G 1H9 Canada
E-mail: [email protected]Search for more papers by this authorJingsi Chen
Department of Chemical and Materials Engineering, University of Alberta, Edmonton, Alberta, T6G 1H9 Canada
Search for more papers by this authorLinbo Han
College of Health Science and Environmental Engineering, Shenzhen Technology University, Shenzhen, Guangdong, 518118 China
Search for more papers by this authorJifang Liu
The Fifth Affiliated Hospital, Guangzhou Medical University, Guangzhou, Guangdong, 510700 China
Search for more papers by this authorCorresponding Author
Hongbo Zeng
Department of Chemical and Materials Engineering, University of Alberta, Edmonton, Alberta, T6G 1H9 Canada
E-mail: [email protected]Search for more papers by this authorDedicated to the Special Issue of Hydrogels.
Comprehensive Summary
Adhesive hydrogels are an emerging class of hydrogels that combine three-dimensional hydrated networks with adhesive properties. These properties facilitate intimate tissue-material contact in diverse biomedical applications, enhancing tissue joining, drug transport, and signal transmission. Inspired by the universal adhesiveness of mussel foot proteins, 3,4-dihydroxyphenyl-L-alanine (DOPA) and its analogs have been extensively exploited for the fabrication of adhesive hydrogels, within which the DOPA moieties can not only serve as cross-linking mediators but also participate in various intermolecular and surface interactions to mediate wet adhesion. This mini-review highlights recent achievements in the development of mussel-inspired adhesive hydrogels, focusing on: (1) elucidating DOPA-mediated adhesion mechanisms through nanomechanical characterizations, (2) designing injectable adhesive hydrogels toward applications in drug delivery, hemostasis, and wound closure, which includes in situ gelling liquids and shear-thinning preformed hydrogels, and (3) fabricating tough adhesive hydrogels with enhanced mechanical properties for use in tissue regeneration, biosensing, and bioimaging, with typical examples of nanocomposite and double-network hydrogels. The challenges and prospects in this rapidly developing field are also discussed.
References
- 1 Hoffman, A. S. Hydrogels for Biomedical Applications. Adv. Drug Deliv. Rev. 2012, 64, 18–23.
- 2 Zhang, K.; Feng, Q.; Fang, Z.; Gu, L.; Bian, L. Structurally Dynamic Hydrogels for Biomedical Applications: Pursuing a Fine Balance between Macroscopic Stability and Microscopic Dynamics. Chem. Rev. 2021, 121, 11149–11193.
- 3 Zhao, Y.; Song, S.; Ren, X.; Zhang, J.; Lin, Q.; Zhao, Y. Supramolecular Adhesive Hydrogels for Tissue Engineering Applications. Chem. Rev. 2022, 122, 5604–5640.
- 4 Zhang, Y.; Chen, Q.; Dai, Z.; Dai, Y.; Xia, F.; Zhang, X. Nanocomposite Adhesive Hydrogels: From Design to Application. J. Mater. Chem. B 2021, 9, 585–593.
- 5 Waite, J. H.; Andersen, N. H.; Jewhurst, S.; Sun, C. Mussel Adhesion: Finding the Tricks Worth Mimicking. J. Adhes. 2005, 81, 297–317.
- 6 Chen, J.; Zeng, H. Mussel-Inspired Reversible Molecular Adhesion for Fabricating Self–Healing Materials. Langmuir 2022, 38, 12999–13008.
- 7 Zhang, C.; Wu, B.; Zhou, Y.; Zhou, F.; Liu, W.; Wang, Z. Mussel-Inspired Hydrogels: From Design Principles to Promising Applications. Chem. Soc. Rev. 2020, 49, 3605–3637.
- 8 Ahn, B. K. Perspectives on Mussel-Inspired Wet Adhesion. J. Am. Chem. Soc. 2017, 139, 10166–10171.
- 9 Chen, J.; Peng, Q.; Peng, X.; Zhang, H.; Zeng, H. Probing and Manipulating Noncovalent Interactions in Functional Polymeric Systems. Chem. Rev. 2022, 122, 14594–14678.
- 10 Zeng, H.; Hwang, D. S.; Israelachvili, J. N.; Waite, J. H. Strong Reversible Fe3+-Mediated Bridging between Dopa-Containing Protein Films in Water. Proc. Natl. Acad. Sci. U. S. A. 2010, 107, 12850–12853.
- 11 Holten-Andersen, N.; Harrington, M. J.; Birkedal, H.; Lee, B. P.; Messersmith, P. B.; Lee, K. Y. C.; Waite, J. H. pH-Induced Metal–Ligand Cross-Links Inspired by Mussel Yield Self-healing Polymer Networks with Near-Covalent Elastic Moduli. Proc. Natl. Acad. Sci. U. S. A. 2011, 108, 2651–2655.
- 12 Mesko, M.; Xiang, L.; Bohle, S.; Hwang, D. S.; Zeng, H.; Harrington, M. J., Catechol–Vanadium Binding Enhances Cross-Linking and Mechanics of a Mussel Byssus Coating Protein. Chem. Mater. 2021, 33, 6530–6540.
- 13 Yu, J.; Wei, W.; Menyo, M. S.; Masic, A.; Waite, J. H.; Israelachvili, J. N. Adhesion of Mussel Foot Protein-3 to TiO2 Surfaces: The Effect of pH. Biomacromolecules 2013, 14, 1072–1077.
- 14 Lu, Q.; Danner, E.; Waite, J. H.; Israelachvili, J. N.; Zeng, H.; Hwang, D. S. Adhesion of Mussel Foot Proteins to Different Substrate Surfaces. J. Royal Soc. Interface 2013, 10, 20120759.
- 15 Yu, J.; Kan, Y.; Rapp, M.; Danner, E.; Wei, W.; Das, S.; Miller, D. R.; Chen, Y.; Waite, J. H.; Israelachvili, J. N. Adaptive Hydrophobic and Hydrophilic Interactions of Mussel Foot Proteins with Organic Thin Films. Proc. Natl. Acad. Sci. U. S. A. 2013, 110, 15680–15685.
- 16 Maier, G. P.; Rapp, M. V.; Waite, J. H.; Israelachvili, J. N.; Butler, A. Adaptive Synergy between Catechol and Lysine Promotes Wet Adhesion by Surface Salt Displacement. Science 2015, 349, 628–632.
- 17 Han, L.; Gong, L.; Chen, J.; Zhang, J.; Xiang, L.; Zhang, L.; Wang, Q.; Yan, B.; Zeng, H. Universal Mussel-Inspired Ultrastable Surface-Anchoring Strategy Via Adaptive Synergy of Catechol and Cations. ACS Appl. Mater. Interfaces 2018, 10, 2166–2173.
- 18 Lim, C.; Huang, J.; Kim, S.; Lee, H.; Zeng, H.; Hwang, D. S. Nanomechanics of Poly (Catecholamine) Coatings in Aqueous Solutions. Angew. Chem. Int. Ed. 2016, 55, 3342–3346.
- 19 Xiang, L.; Zhang, J.; Wang, W.; Gong, L.; Zhang, L.; Yan, B.; Zeng, H. Nanomechanics of π–Cation–π Interaction with Implications for Bio-Inspired Wet Adhesion. Acta Biomater. 2020, 117, 294–301.
- 20 Hwang, D. S.; Zeng, H.; Lu, Q.; Israelachvili, J.; Waite, J. H. Adhesion Mechanism in a Dopa-Deficient Foot Protein from Green Mussels. Soft Matter 2012, 8, 5640–5648.
- 21
Lu, Q.; Oh, D. X.; Lee, Y.; Jho, Y.; Hwang, D. S.; Zeng, H. Nanomechanics of Cation–π Interactions in Aqueous Solution. Angew. Chem. 2013, 125, 4036–4040.
10.1002/ange.201210365 Google Scholar
- 22 Gebbie, M. A.; Wei, W.; Schrader, A. M.; Cristiani, T. R.; Dobbs, H. A.; Idso, M.; Chmelka, B. F.; Waite, J. H.; Israelachvili, J. N. Tuning Underwater Adhesion with Cation–π Interactions. Nat. Chem. 2017, 9, 473–479.
- 23 Zhang, J.; Xiang, L.; Yan, B.; Zeng, H. Nanomechanics of Anion−π Interaction in Aqueous Solution. J. Am. Chem. Soc. 2020, 142, 1710–1714.
- 24 Zhang, C.; Gong, L.; Xiang, L.; Du, Y.; Hu, W.; Zeng, H.; Xu, Z.-K. Deposition and Adhesion of Polydopamine on the Surfaces of Varying Wettability. ACS Appl. Mater. Interfaces 2017, 9, 30943–30950.
- 25 Xie, L.; Cui, X.; Liu, J.; Lu, Q.; Huang, J.; Mao, X.; Yang, D.; Tan, J.; Zhang, H.; Zeng, H. Nanomechanical Insights into Versatile Polydopamine Wet Adhesive Interacting with Liquid-Infused and Solid Slippery Surfaces. ACS Appl. Mater. Interfaces 2021, 13, 6941–6950.
- 26 Loebel, C.; Rodell, C. B.; Chen, M. H.; Burdick, J. A. Shear-Thinning and Self-healing Hydrogels as Injectable Therapeutics and for 3d-Printing. Nat. Protoc. 2017, 12, 1521.
- 27 Chen, J.; Peng, Q.; Peng, X.; Han, L.; Wang, X.; Wang, J.; Zeng, H. Recent Advances in Mechano-Responsive Hydrogels for Biomedical Applications. ACS Appl. Polym. Mater. 2020, 2, 1092–1107.
- 28 Brubaker, C. E.; Kissler, H.; Wang, L.-J.; Kaufman, D. B.; Messersmith, P. B. Biological Performance of Mussel-Inspired Adhesive in Extrahepatic Islet Transplantation. Biomaterials 2010, 31, 420–427.
- 29 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, 7972–7983.
- 30 Wang, R.; Li, J.; Chen, W.; Xu, T.; Yun, S.; Xu, Z.; Xu, Z.; Sato, T.; Chi, B.; Xu, H. A Biomimetic Mussel-Inspired Ε-Poly-L-Lysine Hydrogel with Robust Tissue-Anchor and Anti-infection Capacity. Adv. Funct. Mater. 2017, 27, 1604894.
- 31 Lee, Y.; Chung, H. J.; Yeo, S.; Ahn, C.-H.; Lee, H.; Messersmith, P. B.; Park, T. G. 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, 977–983.
- 32 Ryu, J. H.; Lee, Y.; Kong, W. H.; Kim, T. G.; Park, T. G.; Lee, H. Catechol-Functionalized Chitosan/Pluronic Hydrogels for Tissue Adhesives and Hemostatic Materials. Biomacromolecules 2011, 12, 2653–2659.
- 33 Shou, Y.; Zhang, J.; Yan, S.; Xia, P.; Xu, P.; Li, G.; Zhang, K.; Yin, J. Thermoresponsive Chitosan/Dopa-Based Hydrogel as an Injectable Therapy Approach for Tissue-Adhesion and Hemostasis. ACS Biomater. Sci. Eng. 2020, 6, 3619–3629.
- 34 Choi, Y. C.; Choi, J. S.; Jung, Y. J.; Cho, Y. W. Human Gelatin Tissue-Adhesive Hydrogels Prepared by Enzyme-Mediated Biosynthesis of Dopa and Fe3+ Ion Crosslinking. J. Mater. Chem. B 2014, 2, 201–209.
- 35 Dai, G.; Sun, L.; Xu, J.; Zhao, G.; Tan, Z.; Wang, C.; Sun, X.; Xu, K.; Zhong, W. Catechol-Metal Coordination-Mediated Nanocomposite Hydrogels for on-Demand Drug Delivery and Efficacious Combination Therapy. Acta Biomater. 2021, 129, 84–95.
- 36 Rahim, M. A.; Björnmalm, M.; Suma, T.; Faria, M.; Ju, Y.; Kempe, K.; Müllner, M.; Ejima, H.; Stickland, A. D.; Caruso, F. Metal–Phenolic Supramolecular Gelation. Angew. Chem. Int. Ed. 2016, 55, 13803–13807.
- 37 Rahim, M. A.; Hata, Y.; Björnmalm, M.; Ju, Y.; Caruso, F. Supramolecular Metal–Phenolic Gels for the Crystallization of Active Pharmaceutical Ingredients. Small 2018, 14, 1801202.
- 38 Narain, R.; Wang, W.; Zeng, H. Rational Design of Self-healing Tough Hydrogels: A Mini Review. Front. Chem. 2018, 6, 497.
- 39 Han, L.; Yan, L.; Wang, K.; Fang, L.; Zhang, H.; Tang, Y.; Ding, Y.; Weng, L.-T.; Xu, J.; Weng, J. Tough, Self-healable and Tissue-Adhesive Hydrogel with Tunable Multifunctionality. NPG Asia Mater. 2017, 9, e372.
- 40 Han, L.; Lu, X.; Liu, K.; Wang, K.; Fang, L.; Weng, L.-T.; Zhang, H.; Tang, Y.; Ren, F.; Zhao, C. Mussel-Inspired Adhesive and Tough Hydrogel Based on Nanoclay Confined Dopamine Polymerization. ACS Nano 2017, 11, 2561–2574.
- 41 Han, L.; Lu, X.; Wang, M.; Gan, D.; Deng, W.; Wang, K.; Fang, L.; Liu, K.; Chan, C. W.; Tang, Y. A Musse-Inspired Conductive, Self-adhesive, and Self-healable Tough Hydrogel as Cell Stimulators and Implantable Bioelectronics. Small 2017, 13, 1601916.
- 42 Pan, M.; Nguyen, K.-C. T.; Yang, W.; Liu, X.; Chen, X.-Z.; Major, P. W.; Le, L. H.; Zeng, H. Soft Armour-Like Layer-Protected Hydrogels for Wet Tissue Adhesion and Biological Imaging. Chem. Eng. J. 2022, 434, 134418.
- 43 Gan, D.; Xing, W.; Jiang, L.; Fang, J.; Zhao, C.; Ren, F.; Fang, L.; Wang, K.; Lu, X. Plant-Inspired Adhesive and Tough Hydrogel Based on Ag–Lignin Nanoparticles-Triggered Dynamic Redox Catechol Chemistry. Nat. Commun. 2019, 10, 1487.
- 44 Shao, C.; Wang, M.; Meng, L.; Chang, H.; Wang, B.; Xu, F.; Yang, J.; Wan, P. Mussel-Inspired Cellulose Nanocomposite Tough Hydrogels with Synergistic Self-healing, Adhesive, and Strain-Sensitive Properties. Chem. Mater. 2018, 30, 3110–3121.
- 45 Shao, C.; Meng, L.; Wang, M.; Cui, C.; Wang, B.; Han, C.-R.; Xu, F.; Yang, J. Mimicking Dynamic Adhesiveness and Strain-Stiffening Behavior of Biological Tissues in Tough and Self-healable Cellulose Nanocomposite Hydrogels. ACS Appl. Mater. Interfaces 2019, 11, 5885–5895.
- 46 Chen, T.; Chen, Y.; Rehman, H. U.; Chen, Z.; Yang, Z.; Wang, M.; Li, H.; Liu, H. Ultra-Tough, Self-healing and Tissue-Adhesive Hydrogel for Wound Dressing. ACS Appl. Mater. Interfaces 2018, 10, 33523–33531.
- 47 Wang, X.; Si, Y.; Zheng, K.; Guo, X.; Wang, J.; Xu, Y. Mussel-Inspired Tough Double Network Hydrogel as Transparent Adhesive. ACS Appl. Polym. Mater. 2019, 1, 2998–3007.
- 48 Fan, X.; Fang, Y.; Zhou, W.; Yan, L.; Xu, Y.; Zhu, H.; Liu, H. Mussel Foot Protein Inspired Tough Tissue–Selective Underwater Adhesive Hydrogel. Mater. Horiz. 2021, 8, 997–1007.
- 49 Xue, B.; Gu, J.; Li, L.; Yu, W.; Yin, S.; Qin, M.; Jiang, Q.; Wang, W.; Cao, Y. Hydrogel Tapes for Fault-Tolerant Strong Wet Adhesion. Nat. Commun. 2021, 12, 7156.
- 50 Wang, C.; Gao, X.; Zhang, F.; Hu, W.; Gao, Z.; Zhang, Y.; Ding, M.; Liang, Q. Mussel Inspired Trigger-Detachable Adhesive Hydrogel. Small 2022, 18, 2200336.
- 51 Cui, C.; Shao, C.; Meng, L.; Yang, J. High-Strength, Self-adhesive, and Strain-Sensitive Chitosan/Poly (Acrylic Acid) Double-Network Nanocomposite Hydrogels Fabricated by Salt-Soaking Strategy for Flexible Sensors. ACS Appl. Mater. Interfaces 2019, 11, 39228–39237.
- 52 Liang, M.; He, C.; Dai, J.; Ren, P.; Fu, Y.; Wang, F.; Ge, X.; Zhang, T.; Lu, Z. A High-Strength Double Network Polydopamine Nanocomposite Hydrogel for Adhesion under Seawater. J. Mater. Chem. B 2020, 8, 8232–8241.