Abstract
Marine mussels can adhere to various surfaces in a liquid environment by utilizing pedicle filaments, with the adhesive properties primarily attributed to the structure of catechol, the main component of the filament. To overcome the challenges associated with the complex preparation process, high cost, and potential biological rejection of naturally extracted or recombinantly expressed mussel proteins, researchers drew inspiration from mussels and utilized an oxidative crosslinking approach to prepare adhesive hydrogel materials. However, the hydrogels prepared using this method exhibited inferior mechanical properties and low viscosity. To address these limitations, in this study, a kind of mussel-inspired dual-crosslinked hydrogel was prepared by dual cross-linking with hydroxypropyl chitosan (HPCS) and hyaluronic acid (HA), based on catechol, an adhesion component in marine mussel pedicle filaments. Comparative analysis revealed that the mussel-inspired dual-crosslinked hydrogel exhibited significantly higher adhesion strength (up to 33.96 kPa) and improved mechanical properties (energy storage modulus ranging from 489 to 1032 Pa) compared to the mussel-inspired oxidatively cross-linked hydrogel. In addition, the mussel-inspired dual-crosslinked hydrogel demonstrated favorable swelling (up to 136.54 ± 0.22%), degradation, sustained-release, bacteriostatic and biocompatible properties. These findings suggest a promising potential for future applications in the field of biomedical materials.
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs10934-023-01535-y/MediaObjects/10934_2023_1535_Fig1_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs10934-023-01535-y/MediaObjects/10934_2023_1535_Fig3_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs10934-023-01535-y/MediaObjects/10934_2023_1535_Fig5_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs10934-023-01535-y/MediaObjects/10934_2023_1535_Fig6_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs10934-023-01535-y/MediaObjects/10934_2023_1535_Fig7_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs10934-023-01535-y/MediaObjects/10934_2023_1535_Fig8_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs10934-023-01535-y/MediaObjects/10934_2023_1535_Fig9_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs10934-023-01535-y/MediaObjects/10934_2023_1535_Fig10_HTML.png)
Similar content being viewed by others
References
D. Su, X. Bai, X. He, Research progress on hydrogel materials and their antifouling properties. Eur. Polymer J. 181, 111665 (2022). http://doi.org/https://doi.org/https://doi.org/10.1016/j.eurpolymj.2022.111665
J. Xu, Y. Liu, Hsu. Hydrogels based on Schiff Base linkages for Biomedical Applications. Molecules. 24 (2019). https://doi.org/10.3390/molecules24163005
Y. **ong, X. Zhang, X. Ma, W. Wang, F. Yan, X. Zhao, X. Chu, W. Xu, Sun. A review of the properties and applications of bioadhesive hydrogels. Polym. Chem. 12, 3721–3739 (2021). https://doi.org/10.1039/d1py00282a
C. Ghobril, M.W. Grinstaff, The chemistry and engineering of polymeric hydrogel adhesives for wound closure: a tutorial. Chem. Soc. Rev. 44, 1820–1835 (2015). https://doi.org/10.1039/c4cs00332b
S.W. Choi, W. Guan, K. Chung, Basic principles of hydrogel-based tissue transformation technologies and their applications. Cell. 184, 4115–4136 (2021). http://doi.org/https://doi.org/https://doi.org/10.1016/j.cell.2021.07.009
Z. Tong, L. **, J.M. Oliveira, R.L. Reis, Q. Zhong, Z. Mao, C. Gao, Adaptable hydrogel with reversible linkages for regenerative medicine: dynamic mechanical microenvironment for cells. Bioactive Mater. 6, 1375–1387 (2021). https://doi.org/10.1016/j.bioactmat.2020.10.029
R.C. Cooper, H. Yang, Hydrogel-based ocular drug delivery systems: emerging fabrication strategies, applications, and bench-to-bedside manufacturing considerations. J. Controlled Release. 306, 29–39 (2019). https://doi.org/10.1016/j.jconrel.2019.05.034
S. Khajouei, H. Ravan, A. Ebrahimi, DNA hydrogel-empowered biosensing. Adv. Colloid Interface Sci. 275, 102060 (2020). http://doi.org/https://doi.org/https://doi.org/10.1016/j.cis.2019.102060
E.S. Dragan, Design and applications of interpenetrating polymer network hydrogels. A review. Chem. Eng. J. 243, 572–590 (2014). http://doi.org/https://doi.org/https://doi.org/10.1016/j.cej.2014.01.065
J.P. Gong, Materials both tough and soft. Science. 344, 161–162 (2014). https://doi.org/10.1126/science.1252389
X. Huang, J. Li, J. Luo, Q. Gao, A. Mao, J. Li, Research progress on double-network hydrogels. Mater. Today Commun. 29, 102757 (2021). https://doi.org/10.1016/j.mtcomm.2021.102757
B.K. Ahn, S. Das, R. Linstadt, Y. Kaufman, N.R. Martinez-Rodriguez, R. Mirshafian, E. Kesselman, Y. Talmon, B.H. Lipshutz, J.N. Israelachvili, J.H. Waite, High-performance mussel-inspired adhesives of reduced complexity. Nat. Commun. 6, 8663 (2015). https://doi.org/10.1038/ncomms9663
L. Petrone, A. Kumar, C.N. Sutanto, N.J. Patil, S. Kannan, A. Palaniappan, S. Amini, B. Zappone, C. Verma, A. Miserez, Mussel adhesion is dictated by time-regulated secretion and molecular conformation of mussel adhesive proteins. Nat. Commun. 6, 8737 (2015). https://doi.org/10.1038/ncomms9737
X. Ou, B. Xue, Y. Lao, Y. Wutthinitikornkit, R. Tian, A. Zou, L. Yang, W. Wang, Y. Cao, J. Li, Structure and sequence features of mussel adhesive protein lead to its salt-tolerant adhesion ability. Sci Adv, 6. (2020). https://doi.org/10.1126/sciadv.abb7620
C. **e, X. Wang, H. He, Y. Ding, X. Lu, Mussel-inspired hydrogels for Self-Adhesive Bioelectronics. Adv. Funct. Mater. 30, 1909954 (2020). https://doi.org/10.1002/adfm.201909954
T.J. Deming, Mussel Byssus and biomolecular materials. Curr. Opin. Chem. Biol. 3, 100–105 (1999). http://doi.org/https://https://doi.org/10.1016/S1367-5931(99)80018-0
H. Lee, N.F. Scherer, P.B. Messersmith, Single-molecule mechanics of mussel adhesion. Proceedings of the National Academy of Sciences, 103, 12999–13003. (2006). https://doi.org/10.1073/pnas.0605552103
T. Anderson, J. Israelachvili, Adhesion Mechanisms of the Mussel Foot Proteins mfp-1 and mfp-3. Biophysical Journal, 98, 594a. (2010). https://doi.org/10.1016/j.bpj.2009.12.3232
E. Faure, C. Falentin-Daudré, C. Jérôme, J. Lyskawa, D. Fournier, P. Woisel, Detrembleur. Catechols as versatile platforms in polymer chemistry. Prog. Polym. Sci. 38, 236–270 (2013). https://doi.org/10.1016/j.progpolymsci.2012.06.004
X. Zhang, Q. Huang, F. Deng, H. Huang, Q. Wan, M. Liu, Y. Wei, Mussel-inspired fabrication of functional materials and their environmental applications: Progress and prospects. Appl. Mater. Today. 7, 222–238 (2017). https://doi.org/10.1016/j.apmt.2017.04.001
J. Horsch, P. Wilke, M. Pretzler, M. Seuss, I. Melnyk, D. Remmler, A. Fery, A. Rompel, Börner. Polymerizing like mussels do: toward Synthetic Mussel Foot proteins and resistant glues. Angew. Chem. Int. Ed. 57, 15728–15732 (2018). https://doi.org/10.1002/anie.201809587
X. Liu, R. Song, W. Zhang, C. Qi, S. Zhang, J. Li, Development of eco-friendly soy protein isolate films with High Mechanical properties through HNTs, PVA, and PTGE Synergism Effect. Sci. Rep. 7, 44289 (2017). https://doi.org/10.1038/srep44289
Y. Mu, Q. Sun, B. Li, Wan. Advances in the synthesis and applications of mussel-inspired polymers. Polym. Rev. 63, 1–39 (2023). https://doi.org/10.1080/15583724.2022.2041032
F. Liu, X. Liu, F. Chen, Fu. Mussel-inspired chemistry: a promising strategy for natural polysaccharides in biomedical applications. Prog. Polym. Sci. 123, 101472 (2021). https://doi.org/10.1016/j.progpolymsci.2021.101472
Q. Guo, J. Chen, J. Wang, H. Zeng, Yu. Recent progress in synthesis and application of mussel-inspired adhesives. Nanoscale. 12, 1307–1324 (2020). https://doi.org/10.1039/c9nr09780e
Y. Hao, L. Mao, R. Zhang, X. Liao, M. Yuan, Liao. Multifunctional biodegradable prussian Blue Analogue for Synergetic Photothermal/Photodynamic/Chemodynamic Therapy and intrinsic Tumor Metastasis Inhibition. ACS Appl. Bio Mater. 4, 7081–7093 (2021). https://doi.org/10.1021/acsabm.1c00694
C. Zhu, S. Zou, Z. Rao, L. Min, M. Liu, L. Liu, L. Fan, Preparation and characterization of hydroxypropyl chitosan modified with nisin. Int. J. Biol. Macromol. 105, 1017–1024 (2017). https://doi.org/10.1016/j.ijbiomac.2017.07.136
L. Yue, M. Wang, I.M. Khan, J. Xu, C. Peng, Z. Wang, Preparation, characterization, and antibiofilm activity of cinnamic acid conjugated hydroxypropyl chitosan derivatives. Int. J. Biol. Macromol. 189, 657–667 (2021). https://doi.org/10.1016/j.ijbiomac.2021.08.164
W. Cao, J. Yan, C. Liu, J. Zhang, H. Wang, X. Gao, H. Yan, B. Niu, W. Li, Preparation and characterization of catechol-grafted chitosan/gelatin/modified chitosan-AgNP blend films. Carbohydr. Polym. 247, 116643 (2020). https://doi.org/10.1016/j.carbpol.2020.116643
C. Souza Campelo, P. Chevallier, C. Loy, R. Silveira Vieira, Mantovani. Development, Validation, and performance of Chitosan-based Coatings using Catechol Coupling. Macromol. Biosci. 20, e1900253 (2020). https://doi.org/10.1002/mabi.201900253
A. Pattnaik, S. Pati, S.K. Samal, Chitosan-Polyphenol Conjugates for Human Health. Life (Basel), 12. (2022). https://doi.org/10.3390/life12111768
Q. Wei, Y. Zhao, Y. Wei, Y. Wang, Z. **, G. Ma, Y. Jiang, W. Zhang, Z. Hu, Facile preparation of polyphenol-crosslinked chitosan-based hydrogels for cutaneous wound repair. Int. J. Biol. Macromol. 228, 99–110 (2023). https://doi.org/10.1016/j.ijbiomac.2022.12.215
Y. Yuan, S. Shen, D. Fan, A physicochemical double cross-linked multifunctional hydrogel for dynamic burn wound healing: shape adaptability, injectable self-healing property and enhanced adhesion. Biomaterials. 276, 120838 (2021). https://doi.org/10.1016/j.biomaterials.2021.120838
Z. Zheng, X. Yang, Y. Zhang, W. Zu, M. Wen, T. Liu, C. Zhou, L. Li, An injectable and pH-responsive hyaluronic acid hydrogel as metformin carrier for prevention of Breast cancer recurrence. Carbohydr. Polym. 304, 120493 (2023). https://doi.org/10.1016/j.carbpol.2022.120493
B. Yang, J. Song, Y. Jiang, M. Li, J. Wei, J. Qin, W. Peng, F.L. Lasaosa, Y. He, H. Mao, J. Yang, Z. Gu, ACS Appl. Mater. Interfaces. 12, 57782–57797 (2020). https://doi.org/10.1021/acsami.0c18948. Injectable Adhesive Self-Healing Multicross-Linked Double-Network Hydrogel Facilitates Full-Thickness Skin Wound Healing
J. Chi, A. Li, M. Zou, S. Wang, C. Liu, R. Hu, Z. Jiang, W. Liu, R. Sun, B. Han, Novel dopamine-modified oxidized sodium alginate hydrogels promote angiogenesis and accelerate healing of chronic diabetic wounds. Int. J. Biol. Macromol. 203, 492–504 (2022). https://doi.org/10.1016/j.ijbiomac.2022.01.153
M.N. Roshdy, J.B. Schwartz, R.L. Schnaare, A novel method for measuring gel strength of controlled release hydrogel tablets using a cone/plate rheometer. Pharm. Dev. Technol. 6, 107–116 (2001). https://doi.org/10.1081/pdt-100000046
X. Liu, J. Liu, J. Wang, T. Wang, Y. Jiang, J. Hu, Z. Liu, X. Chen, Yu. Bioinspired, Microstructured Silk Fibroin adhesives for flexible skin sensors. ACS Appl. Mater. Interfaces. 12, 5601–5609 (2020). https://doi.org/10.1021/acsami.9b21197
C. Niu, X. Liu, Y. Wang, X. Li, J. Shi, Photothermal-modulated drug release from a composite hydrogel based on silk fibroin and sodium alginate. Eur. Polymer J. 146, 110267 (2021). https://doi.org/10.1016/j.eurpolymj.2021.110267
L. Li, N. Wang, X. **, R. Deng, S. Nie, L. Sun, Q. Wu, Y. Wei, C. Gong, Biodegradable and injectable in situ cross-linking chitosan-hyaluronic acid based hydrogels for postoperative adhesion prevention. Biomaterials. 35, 3903–3917 (2014). https://doi.org/10.1016/j.biomaterials.2014.01.050
M. Ghorbanloo, N. Moharramkhani, T.M. Yazdely, H.H. Monfared, Cationic hydrogel and graphene oxide based cationic hydrogel with embedded palladium nanoparticles in the aerobic oxidation of olefins. J. Porous Mater. 26, 433–441 (2019). https://doi.org/10.1007/s10934-018-0620-5
W. Zhang, X. Wang, J. Ma, L. Zhao, C. Yang, K. Wang, X. Pu, Y. Wang, F. Ran, Y. Wang, S. Yu, H. Ma, Preparation of chitosan/pumpkin polysaccharide hydrogel for potential application in drug delivery and tissue engineering. J. Porous Mater. 24 (2017). https://doi.org/10.1007/s10934-016-0285-x
L. Michelini, L. Probo, S. Farè, N. Contessi, Negrini, Characterization of gelatin hydrogels derived from different animal sources. Mater. Lett. 272, 127865 (2020). https://doi.org/10.1016/j.matlet.2020.127865
W. Zhang, X. Wang, J. Ma, L. Zhao, C. Yang, K. Wang, X. Pu, Y. Wang, F. Ran, Y. Wang, S. Yu, H. Ma, Preparation of chitosan/pumpkin polysaccharide hydrogel for potential application in drug delivery and tissue engineering. J. Porous Mater. 24, 497–506 (2017). https://doi.org/10.1007/s10934-016-0285-x
R. Zhang, Y. Tian, L. Pang, T. Xu, B. Yu, H. Cong, Y. Shen, Wound Microenvironment-Responsive protein Hydrogel Drug-Loaded System with accelerating Healing and Antibacterial Property. ACS Appl. Mater. Interfaces. 14, 10187–10199 (2022). https://doi.org/10.1021/acsami.2c00373
X. Sheng, X. Li, M. Li, R. Zhang, S. Deng, W. Yang, G. Chang, X. Ye. An Injectable Oxidized Carboxymethyl Cellulose/Polyacryloyl Hydrazide Hydrogel via Schiff Base Reaction. Australian Journal of Chemistry, 71. (2017). https://doi.org/10.1071/CH17214
S. Hocine, D. Ghemati, D. Aliouche, Synthesis, characterization and swelling behavior of pH-sensitive polyvinylalcohol grafted poly(acrylic acid-co-2-acrylamido-2-methylpropane sulfonic acid) hydrogels for protein delivery. Polym. Bull. 1–27 (2023). https://doi.org/10.1007/s00289-022-04664-7
N. Esfandiari, Z. Bagheri, H. Ehtesabi, Z. Fatahi, H. Tavana, H. Latifi, Effect of carbonization degree of carbon dots on cytotoxicity and photo-induced toxicity to cells. Heliyon. 5, e02940 (2019). https://doi.org/10.1016/j.heliyon.2019.e02940
A. Jabbari, H. Mahdavi, M. Nikoorazm, A. Ghorbani-Choghamarani, Oxovanadium(IV) salicylidene Schiff base complex anchored on mesoporous silica MCM-41 as hybrid materials: a robust catalyst for the oxidation of sulfides. J. Porous Mater. 22, 1111–1118 (2015). https://doi.org/10.1007/s10934-015-9986-9
J. Wu, L. Zhang, Dissolution behavior and conformation change of chitosan in concentrated chitosan hydrochloric acid solution and comparison with dilute and semidilute solutions. Int. J. Biol. Macromol. 121, 1101–1108 (2019). https://doi.org/10.1016/j.ijbiomac.2018.10.128
B.P. Lee, J.L. Dalsin, P.B. Messersmith, Synthesis and gelation of DOPA-Modified poly(ethylene glycol) hydrogels. Biomacromolecules. 3, 1038–1047 (2002). https://doi.org/10.1021/bm025546n
C. Zhang, K. Li, J. Simonsen, A novel wood-binding domain of a wood–plastic coupling agent: development and characterization. J. Appl. Polym. Sci. 89, 1078–1084 (2003). https://doi.org/10.1002/app.12257
M.W. Sabaa, A.M. Elzanaty, O.F. Abdel-Gawad, E.G. Arafa, Synthesis, characterization and antimicrobial activity of Schiff bases modified chitosan-graft-poly(acrylonitrile). Int. J. Biol. Macromol. 109, 1280–1291 (2018). https://doi.org/10.1016/j.ijbiomac.2017.11.129
Acknowledgements
We thank for this work was supported by National Natural Science Foundation of China (No. 81560737, 32260231 and 31860250), Gansu Provincial Natural Science Fund (No. 23JRRA840), University teachers’ innovation fund project of Gansu Province in China (2023 A-020), Science and Technology Innovation Special Fund Project of Gansu Province, China (2019ZX-05), Foundation for Innovation Groups of Basic Research in Gansu Province (No. 1506RJIA116) and Gansu Provincial Science and Technology-based Small and Medium-sized Enterprises Technological Innovation Fund (No. 23CXGA0125).
Author information
Contributions
XL. Z: Conceptualization, Reviewing. LY. L: Writing-review & editing. WP. W and CH. Z: Formal analysis, Investigation. Y. L, L. L and TK. Z: Data curation, Validation. WJ. Z: Project administration Supervision.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Zhao, X., Lu, L., Wan, W. et al. Preparation and characterization of mussel-inspired dual-crosslinked hydrogels based on hydroxypropyl chitosan. J Porous Mater 31, 611–624 (2024). https://doi.org/10.1007/s10934-023-01535-y
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10934-023-01535-y