Advanced Applications of Silk-Based Hydrogels for Tissue Engineering: A Short Review
Abstract
:1. Introduction
2. Silk Fibroin Use for Various Biomedical Applications
2.1. Silk Fibroin
SF-Based Hybrid Biopolymers | Concentration of Biomaterials | Production Method | Application Area | Cell Types | Results | Ref. |
---|---|---|---|---|---|---|
SF/Gelatin | 5% w/v SF 5% Gelatin | Extrusion-based 3D bioprinting | - | hMSCs | Cell viability up to the 28th day after printing | [53] |
SF/Gelatin | 5% w/v SF 5% Gelatin | 3D bioprinting | Bone | hMSCs | Osteogenic differentiation at gene and protein levels A novel in vitro model that replicates a dimensional microenvironment. | [54] |
SF/Gelatin | 5% w/v SF 5% Gelatin | 3D bioprinting | Skin | Human primary adult dermal fibroblasts | Crossinkable in situ Printability as bio-ink | [55] |
Sil-MA | 30% w/v Sil-MA | Digital Light Processing (DLP) | Trachea | NIH/3T3 fibroblast | Excellent biocompatibility, swelling behavior, cell growth, Availability of multi-layer printing | [51] |
Sil-MA | 15% and 30% Sil-MA | 4D bioprinting | Trachea | Chondrocytes and turbinate-derived mesenchymal stem cells | Reproducibility of heterogeneous tissues containing more than two components | [56] |
SF/Alginate | 5% w/v SF 5 wt.% Alginate | 3D printing | Microchannel network | NIH/3T3 fibroblast | Good cytocompatibility | [57] |
SF-Polypyrrole | 20 wt.% SF 14 mM pyrrole | 3D printing and electrospinning | Neural tissue | Schwann cells | Improvement in bioactivity and mechanical strength with SF | [58] |
SF/COL | COL:SF 2:1 | 3D bioprinting | Repairing of injured spinal cord | Mesenchymal stem cells | Enhanced multi-step stiffness | [59] |
Cellulose NPs-reinforced chitosan/SF | 5% w/v chitosan 1% w/w SF 1% w/w cellulose NPs | 3D printing | Bone | Raw 264.7 cells | Enhancing osteogenic efficiency | [60] |
SF-bioactive glass | 6% w/v SF 6% w/v Gelatin 0.1%, 1%, and 10 wt.% bioactive glass | 3D printing | Bone | Human bone marrow stem cells | Excellent mechanical stability | [61] |
SF/PCL | 16% w/v SF | 3D printing | Meniscus regeneration | Synovium-derived mesenchymal stem cells | One-step operation Cost effective | [62] |
SF-Decellularized ECM | 5% w/v SF 8 wt.% Gelatin 10% Decellularized liver ECM | 3D printing | Liver regeneration | Huh7 cells | Good cell viability | [63] |
Polyethylene glycol di-methacrylate (PEGDMA)/SF | 10 wt.% PEGDMA 8% w/v SF Ratio = 1:1 | DLP 3D printing | Articular cartilage | - | More and small porosity | [64] |
SF/Gelatin | 0.12, 0.16, 0.2 wt% | Diffusion-driven cross-linking | Peripheral nerve repair | Schwann (SC) and PC12 cells | Myelination of SC, neuronal differentiation of PC12 cells | [15] |
SF/Gelatin/Chitosan | 3.5% w/v SF 1:3 v/v Chitosan:gelatin | Freeze-drying | Tissue engineering | Human umbilical vein endothelial cells | Suitable pore size, pore interconnectivity, porosity, increased mechanical strength, and degradation rate | [18] |
2.2. Silk Fibroin in Skin and Wound Tissue Engineering
2.3. Silk Fibroin in Bone Tissue Engineering
2.4. Silk Fibroin in Cartilage Tissue Engineering
2.5. Silk Fibroin in Drug Delivery Systems
3. Advantages of Silk-Based Hydrogels in Tissue Engineering
4. Limitations of Silk-Based Hydrogels in Tissue Engineering
5. Future Aspects and Challenges
6. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Tahir, B.; Pasda, S.; Widhi Kurniawan, A. The Influence of market orientation, Innovation, and Entrepreneurial competence on competitiveness and Performance of Small And medium Enterprises of Silk weaving Industry. IOSR J. Bus. Manag. 2018, 20, 01–09. [Google Scholar] [CrossRef]
- Melke, J.; Midha, S.; Ghosh, S.; Ito, K.; Hofmann, S. Silk fibroin as biomaterial for bone tissue engineering. Acta Biomater. 2016, 31, 1–16. [Google Scholar] [CrossRef] [PubMed]
- Andrea, A.J. The Silk Road in World History: A Review Essay. Asian Rev. World Hist. 2014, 2, 105–127. [Google Scholar] [CrossRef]
- Mehrotra, S.; Chouhan, D.; Konwarh, R.; Kumar, M.; Jadi, P.K.; Mandal, B.B. Comprehensive Review on Silk at Nanoscale for Regenerative Medicine and Allied Applications. ACS Biomater. Sci. Eng. 2019, 5, 2054–2078. [Google Scholar] [CrossRef] [PubMed]
- Muffly, T.M.; Tizzano, A.P.; Walters, M.D. The history and evolution of sutures in pelvic surgery. J. R. Soc. Med. 2011, 104, 107. [Google Scholar] [CrossRef] [PubMed]
- Min, K.; Kim, S.; Kim, S. Silk protein nanofibers for highly efficient, eco-friendly, optically translucent, and multifunctional air filters. Sci. Rep. 2018, 8, 9598. [Google Scholar] [CrossRef] [PubMed]
- Shi, C.; Wang, J.; Sushko, M.L.; Qiu, W.; Yan, X.; Liu, X.Y. Silk Flexible Electronics: From Bombyx mori Silk Ag Nanoclusters Hybrid Materials to Mesoscopic Memristors and Synaptic Emulators. Adv. Funct. Mater. 2019, 29, 1904777. [Google Scholar] [CrossRef]
- Huang, W.; Ling, S.; Li, C.; Omenetto, F.G.; Kaplan, D.L. Silkworm silk-based materials and devices generated using bio-nanotechnology. Chem. Soc. Rev. 2018, 47, 6486–6504. [Google Scholar] [CrossRef]
- Florczak, A.; Deptuch, T.; Kucharczyk, K.; Dams-Kozlowska, H. Systemic and Local Silk-Based Drug Delivery Systems for Cancer Therapy. Cancers 2021, 13, 5389. [Google Scholar] [CrossRef]
- Long, S.; Xiao, Y.; Zhang, X. Progress in Preparation of Silk Fibroin Microspheres for Biomedical Applications. Pharm. Nanotechnol. 2020, 8, 358–371. [Google Scholar] [CrossRef]
- Salehi, S.; Koeck, K.; Scheibel, T. Spider Silk for Tissue Engineering Applications. Molecules 2020, 25, 737. [Google Scholar] [CrossRef] [PubMed]
- 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. [Google Scholar] [CrossRef] [PubMed]
- Zhang, W.; Chen, J.; Qu, M.; Backman, L.J.; Zhang, A.; Liu, H.; Zhang, X.; Zhou, Q.; Danielson, P. Sustained Release of TPCA-1 from Silk Fibroin Hydrogels Preserves Keratocyte Phenotype and Promotes Corneal Regeneration by Inhibiting Interleukin-1β Signaling. Adv. Healthc. Mater. 2020, 9, 2000591. [Google Scholar] [CrossRef] [PubMed]
- López Barreiro, D.; Yeo, J.; Tarakanova, A.; Martin-Martinez, F.J.; Buehler, M.J. Multiscale Modeling of Silk and Silk-Based Biomaterials—A Review. Macromol. Biosci. 2019, 19, 1800253. [Google Scholar] [CrossRef] [PubMed]
- Wang, H.; Wan, H.; Wang, Q.; Ma, Y.; Su, G.; Cao, X.; Gao, H. Engineered multi-functional silk fibroin/gelatin hydrogel conduit loaded with miR-29a@ZIF-8 nanoparticles for peripheral nerve regeneration. Smart Mater. Med. 2023, 4, 480–492. [Google Scholar] [CrossRef]
- Zhang, H.; Xu, D.; Zhang, Y.; Li, M.; Chai, R. Silk fibroin hydrogels for biomedical applications. Smart Med. 2022, 1, e20220011. [Google Scholar] [CrossRef]
- Amirian, J.; Wychowaniec, J.K.; Zendehdel, E.A.; Sharma, G.; Brangule, A.; Bandere, D. Versatile Potential of Photo-Cross-Linkable Silk Fibroin: Roadmap from Chemical Processing Toward Regenerative Medicine and Biofabrication Applications. Biomacromolecules 2023, 24, 2957–2981. [Google Scholar] [CrossRef] [PubMed]
- Asadpour, S.; Kargozar, S.; Moradi, L.; Ai, A.; Nosrati, H.; Ai, J. Natural biomacromolecule based composite scaffolds from silk fibroin, gelatin and chitosan toward tissue engineering applications. Int. J. Biol. Macromol. 2020, 154, 1285–1294. [Google Scholar] [CrossRef]
- Yang, X.; Wang, X.; Yu, F.; Ma, L.; Pan, X.; Luo, G.; Lin, S.; Mo, X.; Wang, H. Hyaluronic Acid/EDC/NHS-Crosslinked Green Electrospun Silk Fibroin Nanofibrous Scaffolds for Tissue Engineering. R. Soc. Chem. 2016, 6, 99720–99728. [Google Scholar] [CrossRef]
- Li, X.; Liu, Y.; Zhang, J.; You, R.; Qu, J.; Li, M. Functionalized Silk Fibroin Dressing with Topical Bioactive Insulin Release for Accelerated Chronic Wound Healing. Mater. Sci. Eng. C 2017, 72, 394–404. [Google Scholar] [CrossRef]
- Mosher, C.Z.; Brudnicki, P.A.P.; Gong, Z.; Childs, H.R.; Lee, S.W.; Antrobus, R.M.; Fang, E.C.; Schiros, T.N.; Lu, H.H. Green Electrospinning for Biomaterials and Biofabrication. Biofabrication 2021, 13, 035049. [Google Scholar] [CrossRef] [PubMed]
- Kim, S.H.; Hong, H.; Ajiteru, O.; Sultan, M.T.; Lee, Y.J.; Lee, J.S.; Lee, O.J.; Lee, H.; Park, H.S.; Choi, K.Y.; et al. 3D bioprinted silk fibroin hydrogels for tissue engineering. Nat. Protoc. 2021, 16, 5484–5532. [Google Scholar] [CrossRef] [PubMed]
- Lujerdean, C.; Baci, G.-M.; Cucu, A.-A.; Dezmirean, D.S. The Contribution of Silk Fibroin in Biomedical Engineering. Insects 2022, 13, 286. [Google Scholar] [CrossRef] [PubMed]
- Wang, Y.; Yang, Z.; Chen, X.; Jiang, X.; Fu, G. Silk fibroin hydrogel membranes prepared by a sequential cross-linking strategy for guided bone regeneration. J. Mech. Behav. Biomed. Mater. 2023, 147, 106133. [Google Scholar] [CrossRef] [PubMed]
- Wu, J.; Cao, L.; Liu, Y.; Zheng, A.; Jiao, D.; Zeng, D.; Wang, X.; Kaplan, D.L.; Jiang, X. Functionalization of Silk Fibroin Electrospun Scaffolds via BMSC Affinity Peptide Grafting through Oxidative Self-Polymerization of Dopamine for Bone Regeneration. ACS Appl. Mater. Interfaces 2019, 11, 8878–8895. [Google Scholar] [CrossRef] [PubMed]
- Huang, C.-Y.; Hu, K.-H.; Wei, Z.-H. Comparison of cell behavior on pva/pva-gelatin electrospun nanofibers with random and aligned configuration. Sci. Rep. 2016, 6, 37960. [Google Scholar] [CrossRef] [PubMed]
- Aydin, A.; Ulag, S.; Sahin, A.; Aksu, B.; Gunduz, O.; Ustundag, C.B.; Marinas, I.C.; Georgescu, M.; Chifiriuc, M.C. Biocompatible polyvinyl alcohol nanofibers loaded with amoxicillin and salicylic acid to prevent wound infections. Biomed. Mater. 2023, 18, 055029. [Google Scholar] [CrossRef] [PubMed]
- Gunduz, O.; Ulag, S. Gentamicin and fluconazole loaded electrospun polymethylmethacrylate (PMMA) fibers as a novel platform for the treatment of corneal keratitis. Int. J. Polym. Mater. Polym. Biomater. 2023, 72, 995–1007. [Google Scholar] [CrossRef]
- Brougham, C.M.; Levingstone, T.J.; Shen, N.; Cooney, G.M.; Jockenhoevel, S.; Flanagan, T.C.; O’Brien, F.J. Freeze-Drying as a Novel Biofabrication Method for Achieving a Controlled Microarchitecture within Large, Complex Natural Biomaterial Scaffolds. Adv. Healthc. Mater. 2017, 6, 1700598. [Google Scholar] [CrossRef]
- Mehrotra, S.; Singh, R.D.; Bandyopadhyay, A.; Janani, G.; Dey, S.; Mandal, B.B. Engineering Microsphere-Loaded Non-mulberry Silk-Based 3D Bioprinted Vascularized Cardiac Patches with Oxygen-Releasing and Immunomodulatory Potential. ACS Appl. Mater. Interfaces 2021, 13, 50744–50759. [Google Scholar] [CrossRef]
- Ayran, M.; Bulut, B.; Ulag, S. Bioprinting. In Biomaterials and Tissue Engineering; Springer: Berlin/Heidelberg, Germany, 2023; pp. 357–384. [Google Scholar] [CrossRef]
- Chakraborty, J.; Mu, X.; Pramanick, A.; Kaplan, D.L.; Ghosh, S. Recent advances in bioprinting using silk protein-based bioinks. Biomaterials 2022, 287, 121672. [Google Scholar] [CrossRef] [PubMed]
- Rockwood, D.N.; Preda, R.C.; Yücel, T.; Wang, X.; Lovett, M.L.; Kaplan, D.L. Materials fabrication from Bombyx mori silk fibroin. Nat. Protoc. 2011, 6, 1612–1631. [Google Scholar] [CrossRef] [PubMed]
- Nguyen, A.T.; Huang, Q.L.; Yang, Z.; Lin, N.; Xu, G.; Liu, X.Y. Crystal Networks in Silk Fibrous Materials: From Hierarchical Structure to Ultra Performance. Small 2015, 11, 1039–1054. [Google Scholar] [CrossRef] [PubMed]
- Koh, L.D.; Cheng, Y.; Teng, C.P.; Khin, Y.W.; Loh, X.J.; Tee, S.Y.; Low, M.; Ye, E.; Yu, H.D.; Zhang, Y.W.; et al. Structures, mechanical properties and applications of silk fibroin materials. Prog. Polym. Sci. 2015, 46, 86–110. [Google Scholar] [CrossRef]
- Inoue, S.; Tanaka, K.; Arisaka, F.; Kimura, S.; Ohtomo, K.; Mizuno, S. Silk fibroin of Bombyx mori is secreted, assembling a high molecular mass elementary unit consisting of H-chain, L-chain, and P25, with a 6:6:1 molar ratio. J. Biol. Chem. 2000, 275, 40517–40528. [Google Scholar] [CrossRef] [PubMed]
- Nguyen, T.P.; Nguyen, Q.V.; Nguyen, V.H.; Le, T.H.; Huynh, V.Q.N.; Vo, D.V.N.; Trinh, Q.T.; Kim, S.Y.; Van Le, Q. Silk Fibroin-Based Biomaterials for Biomedical Applications: A Review. Polymers 2019, 11, 1933. [Google Scholar] [CrossRef]
- Ling, S.; Chen, W.; Fan, Y.; Zheng, K.; Jin, K.; Yu, H.; Buehler, M.J.; Kaplan, D.L. Biopolymer nanofibrils: Structure, modeling, preparation, and applications. Prog. Polym. Sci. 2018, 85, 1–56. [Google Scholar] [CrossRef] [PubMed]
- Nuanchai, K.; Wilaiwan, S.; Prasong, S. Effect of Different Organic Solvents and Treatment Times on Secondary Structure and Thermal Properties of Silk Fibroin Films. Curr. Res. Chem. 2009, 2, 1–9. [Google Scholar] [CrossRef]
- Perea, G.B.; Solanas, C.; Marí-Buyé, N.; Madurga, R.; Agulló-Rueda, F.; Muinelo, A.; Riekel, C.; Burghammer, M.; Jorge, I.; Vázquez, J.; et al. The apparent variability of silkworm (Bombyx mori) silk and its relationship with degumming. Eur. Polym. J. 2016, 78, 129–140. [Google Scholar] [CrossRef]
- Dõantuono, A.; Baldi, E.; Bellavista, S.; Banzola, N.; Zauli, S.; Patrizi, A. Use of Dermasilk briefs in recurrent vulvovaginal candidosis: Safety and effectiveness. Wiley Online Libr. 2012, 55, e85–e89. [Google Scholar] [CrossRef]
- Gholipourmalekabadi, M.; Sapru, S.; Samadikuchaksaraei, A.; Reis, R.L.; Kaplan, D.L.; Kundu, S.C. Silk fibroin for skin injury repair: Where do things stand? Adv. Drug Deliv. Rev. 2020, 153, 28–53. [Google Scholar] [CrossRef] [PubMed]
- Rodriguez, M.J.; Brown, J.; Giordano, J.; Lin, S.J.; Omenetto, F.G.; Kaplan, D.L. Silk based bioinks for soft tissue reconstruction using 3-dimensional (3D) printing with in vitro and in vivo assessments. Biomaterials 2017, 117, 105–115. [Google Scholar] [CrossRef] [PubMed]
- Oliveira, J.M. Current and future trends of silk fibroin-based bioinks in 3D printing. J. 3D Print. Med. 2020, 4, 69–73. [Google Scholar] [CrossRef]
- Chameettachal, S.; Midha, S.; Ghosh, S. Regulation of Chondrogenesis and Hypertrophy in Silk Fibroin-Gelatin-Based 3D Bioprinted Constructs. ACS Biomater. Sci. Eng. 2016, 2, 1450–1463. [Google Scholar] [CrossRef] [PubMed]
- Huang, X.; Fu, Q.; Deng, Y.; Wang, F.; Xia, B.; Chen, Z.; Chen, G. Surface roughness of silk fibroin/alginate microspheres for rapid hemostasis in vitro and in vivo. Carbohydr. Polym. 2021, 253, 117256. [Google Scholar] [CrossRef] [PubMed]
- Singh, R.; Eitler, D.; Morelle, R.; Friedrich, R.P.; Dietel, B.; Alexiou, C.; Boccaccini, A.R.; Liverani, L.; Cicha, I. Optimization of cell seeding on electrospun PCL-silk fibroin scaffolds. Eur. Polym. J. 2020, 134, 109838. [Google Scholar] [CrossRef]
- Wang, F.; Liu, H.; Li, Y.; Li, Y.; Ma, Q.; Zhang, J.; Hu, X. Tunable Biodegradable Polylactide-Silk Fibroin Scaffolds Fabricated by a Solvent-Free Pressure-Controllable Foaming Technology. ACS Appl. Bio Mater. 2020, 3, 8795–8807. [Google Scholar] [CrossRef]
- Yan, C.; Ren, Y.; Sun, X.; Jin, L.; Liu, X.; Chen, H.; Wang, K.; Yu, M.; Zhao, Y. Photoluminescent functionalized carbon quantum dots loaded electroactive Silk fibroin/PLA nanofibrous bioactive scaffolds for cardiac tissue engineering. J. Photochem. Photobiol. B Biol. 2020, 202, 111680. [Google Scholar] [CrossRef]
- Mu, X.; Wang, Y.; Guo, C.; Li, Y.; Ling, S.; Huang, W.; Cebe, P.; Hsu, H.H.; De Ferrari, F.; Jiang, X.; et al. 3D Printing of Silk Protein Structures by Aqueous Solvent-Directed Molecular Assembly. Macromol. Biosci. 2020, 20, 1900191. [Google Scholar] [CrossRef]
- Kim, S.H.; Yeon, Y.K.; Lee, J.M.; Chao, J.R.; Lee, Y.J.; Seo, Y.B.; Sultan, M.T.; Lee, O.J.; Lee, J.S.; Yoon, S.I.; et al. Precisely printable and biocompatible silk fibroin bioink for digital light processing 3D printing. Nat. Commun. 2018, 9, 1620. [Google Scholar] [CrossRef]
- Zhou, L.; Wang, Z.; Chen, D.; Lin, J.; Li, W.; Guo, S.; Wu, R.; Zhao, X.; Lin, T.; Chen, G.; et al. An injectable and photocurable methacrylate-silk fibroin hydrogel loaded with bFGF for spinal cord regeneration. Mater. Des. 2022, 217, 110670. [Google Scholar] [CrossRef]
- Trucco, D.; Sharma, A.; Manferdini, C.; Gabusi, E.; Petretta, M.; Desando, G.; Ricotti, L.; Chakraborty, J.; Ghosh, S.; Lisignoli, G. Modeling and fabrication of silk fibroin-gelatin-based constructs using extrusion-based three-dimensional bioprinting. ACS Biomater. Sci. Eng. 2021, 7, 3306–3320. [Google Scholar] [CrossRef] [PubMed]
- Sharma, A.; Desando, G.; Petretta, M.; Chawla, S.; Bartolotti, I.; Manferdini, C.; Paolella, F.; Gabusi, E.; Trucco, D.; Ghosh, S.; et al. Investigating the Role of Sustained Calcium Release in Silk-Gelatin-Based Three-Dimensional Bioprinted Constructs for Enhancing the Osteogenic Differentiation of Human Bone Marrow Derived Mesenchymal Stromal Cells. ACS Biomater. Sci. Eng. 2019, 5, 1518–1533. [Google Scholar] [CrossRef] [PubMed]
- Admane, P.; Gupta, A.C.; Jois, P.; Roy, S.; Chandrasekharan Lakshmanan, C.; Kalsi, G.; Bandyopadhyay, B.; Ghosh, S. Direct 3D bioprinted full-thickness skin constructs recapitulate regulatory signaling pathways and physiology of human skin. Bioprinting 2019, 15, e00051. [Google Scholar] [CrossRef]
- Kim, S.H.; Seo, Y.B.; Yeon, Y.K.; Lee, Y.J.; Park, H.S.; Sultan, M.T.; Lee, J.M.; Lee, J.S.; Lee, O.J.; Hong, H.; et al. 4D-bioprinted silk hydrogels for tissue engineering. Biomaterials 2020, 260, 120281. [Google Scholar] [CrossRef] [PubMed]
- Kim, E.; Seok, J.M.; Bae, S.B.; Park, S.A.; Park, W.H. Silk fibroin enhances cytocompatibilty and dimensional stability of alginate hydrogels for light-based three-dimensional bioprinting. Biomacromolecules 2021, 22, 1921–1931. [Google Scholar] [CrossRef] [PubMed]
- Zhao, Y.; Liang, Y.; Ding, S.; Zhang, K.; Mao, H.Q.; Yang, Y. Application of conductive PPy/SF composite scaffold and electrical stimulation for neural tissue engineering. Biomaterials 2020, 255, 120164. [Google Scholar] [CrossRef]
- Sanz-Fraile, H.; Amoros, S.; Mendizabal, I.; Galvez-Monton, C.; Prat-Vidal, C.; Bayes-Genis, A.; Navajas, D.; Farre, R.; Otero, J. Silk-Reinforced Collagen Hydrogels with Raised Multiscale Stiffness for Mesenchymal Cells 3D Culture. Tissue Eng. Part A 2020, 26, 358–370. [Google Scholar] [CrossRef]
- Patel, D.K.; Dutta, S.D.; Hexiu, J.; Ganguly, K.; Lim, K.T. 3D-printable chitosan/silk fibroin/cellulose nanoparticle scaffolds for bone regeneration via M2 macrophage polarization. Carbohydr. Polym. 2022, 281, 119077. [Google Scholar] [CrossRef]
- Bidgoli, M.R.; Alemzadeh, I.; Tamjid, E.; Khafaji, M.; Vossoughi, M. Fabrication of hierarchically porous silk fibroin-bioactive glass composite scaffold via indirect 3D printing: Effect of particle size on physico-mechanical properties and in vitro cellular behavior. Mater. Sci. Eng. C 2019, 103, 109688. [Google Scholar] [CrossRef]
- Li, Z.; Wu, N.; Cheng, J.; Sun, M.; Yang, P.; Zhao, F.; Zhang, J.; Duan, X.; Fu, X.; Zhang, J.; et al. Biomechanically, structurally and functionally meticulously tailored polycaprolactone/silk fibroin scaffold for meniscus regeneration. Theranostics 2020, 10, 5090–5106. [Google Scholar] [CrossRef] [PubMed]
- Sharma, A.; Rawal, P.; Tripathi, D.M.; Alodiya, D.; Sarin, S.K.; Kaur, S.; Ghosh, S. Upgrading hepatic differentiation and functions on 3d printed silk-decellularized liver hybrid scaffolds. ACS Biomater. Sci. Eng. 2021, 7, 3861–3873. [Google Scholar] [CrossRef] [PubMed]
- Egawa, S.; Kurita, H.; Kanno, T.; Narita, F. Effect of Silk Fibroin Concentration on the Properties of Polyethylene Glycol Dimethacrylates for Digital Light Processing Printing. Adv. Eng. Mater. 2021, 23, 2100487. [Google Scholar] [CrossRef]
- Dhasmana, A.; Singh, S.; Kadian, S.; Singh, L. Skin Tissue Engineering: Principles and Advances. J. Dermatol. Skin Care 2018, 1, 101. [Google Scholar]
- Ayran, M.; Dirican, A.Y.; Saatcioglu, E.; Ulag, S.; Sahin, A.; Aksu, B.; Croitoru, A.M.; Ficai, D.; Gunduz, O.; Ficai, A. 3D-Printed PCL Scaffolds Combined with Juglone for Skin Tissue Engineering. Bioengineering 2022, 9, 427. [Google Scholar] [CrossRef] [PubMed]
- Ilhan, E.; Ozerol, E.A.; Alpdagtas, S.; Sengor, M.; Ustundag, C.B.; Gunduz, O. Biofunctional Inks for 3D Printing in Skin Tissue Engineering; Springer: Singapore, 2021. [Google Scholar] [CrossRef]
- Wilkinson, H.N.; Hardman, M.J. Wound healing: Cellular mechanisms and pathological outcomes. Adv. Surg. Med. Spec. 2023, 10, 341–370. [Google Scholar] [CrossRef] [PubMed]
- Xu, N.; Wang, L.; Guan, J.; Tang, C.; He, N.; Zhang, W.; Fu, S. Wound healing effects of a Curcuma zedoaria polysaccharide with platelet-rich plasma exosomes assembled on chitosan/silk hydrogel sponge in a diabetic rat model. Int. J. Biol. Macromol. 2018, 117, 102–107. [Google Scholar] [CrossRef]
- Madni, A.; Kousar, R.; Naeem, N.; Wahid, F. Recent advancements in applications of chitosan-based biomaterials for skin tissue engineering. J. Bioresour. Bioprod. 2021, 6, 11–25. [Google Scholar] [CrossRef]
- Zhang, W.; Chen, L.; Chen, J.; Wang, L.; Gui, X.; Ran, J.; Xu, G.; Zhao, H.; Zeng, M.; Ji, J.; et al. Silk Fibroin Biomaterial Shows Safe and Effective Wound Healing in Animal Models and a Randomized Controlled Clinical Trial. Adv. Healthc. Mater. 2017, 6, 1700121. [Google Scholar] [CrossRef]
- Mukherjee, S.; Krishnan, A.; Athira, R.K.; Kasoju, N.; Sah, M.K. Silk fibroin and silk sericin in skin tissue engineering and wound healing: Retrospect and prospects. In Natural Polymers in Wound Healing and Repair from Basic Concepts to Emerging Trends; Elsevier: Amsterdam, The Netherlands, 2022; pp. 301–331. [Google Scholar] [CrossRef]
- Mehrabani, M.G.; Karimian, R.; Mehramouz, B.; Rahimi, M.; Kafil, H.S. Preparation of biocompatible and biodegradable silk fibroin/chitin/silver nanoparticles 3D scaffolds as a bandage for antimicrobial wound dressing. Int. J. Biol. Macromol. 2018, 114, 961–971. [Google Scholar] [CrossRef]
- Liu, J.; Yan, L.; Yang, W.; Lan, Y.; Zhu, Q.; Xu, H.; Zheng, C.; Guo, R. Controlled-release neurotensin-loaded silk fibroin dressings improve wound healing in diabetic rat model. Bioact. Mater. 2019, 4, 151–159. [Google Scholar] [CrossRef] [PubMed]
- Li, S.; Li, L.; Guo, C.; Qin, H.; Yu, X. A promising wound dressing material with excellent cytocompatibility and proangiogenesis action for wound healing: Strontium loaded Silk fibroin/Sodium alginate (SF/SA) blend films. Int. J. Biol. Macromol. 2017, 104, 969–978. [Google Scholar] [CrossRef] [PubMed]
- Huang, X.W.; Wei, J.J.; Liu, T.; Zhang, X.L.; Bai, S.M.; Yang, H.H. Silk fibroin-assisted exfoliation and functionalization of transition metal dichalcogenide nanosheets for antibacterial wound dressings. Nanoscale 2017, 9, 17193–17198. [Google Scholar] [CrossRef] [PubMed]
- Kandhasamy, S.; Arthi, N.; Arun, R.P.; Verma, R.S. Synthesis and fabrication of novel quinone-based chromenopyrazole antioxidant-laden silk fibroin nanofibers scaffold for tissue engineering applications. Mater. Sci. Eng. C 2019, 102, 773–787. [Google Scholar] [CrossRef]
- Turkkan, S.; Atila, D.; Akdag, A.; Tezcaner, A. Fabrication of functionalized citrus pectin/silk fibroin scaffolds for skin tissue engineering. J. Biomed. Mater. Res. Part B Appl. Biomater. 2018, 106, 2625–2635. [Google Scholar] [CrossRef] [PubMed]
- Bhardwaj, N.; Sow, W.T.; Devi, D.; Ng, K.W.; Mandal, B.B.; Cho, N.J. Silk fibroin-keratin based 3D scaffolds as a dermal substitute for skin tissue engineering. Integr. Biol. 2015, 7, 53–63. [Google Scholar] [CrossRef] [PubMed]
- Keirouz, A.; Zakharova, M.; Kwon, J.; Robert, C.; Koutsos, V.; Callanan, A.; Chen, X.; Fortunato, G.; Radacsi, N. High-throughput production of silk fibroin-based electrospun fibers as biomaterial for skin tissue engineering applications. Mater. Sci. Eng. C 2020, 112, 110939. [Google Scholar] [CrossRef] [PubMed]
- Ju, H.W.; Lee, O.J.; Lee, J.M.; Moon, B.M.; Park, H.J.; Park, Y.R.; Lee, M.C.; Kim, S.H.; Chao, J.R.; Ki, C.S.; et al. Wound healing effect of electrospun silk fibroin nanomatrix in burn-model. Int. J. Biol. Macromol. 2016, 85, 29–39. [Google Scholar] [CrossRef]
- Peifen, M.; Mengyun, L.; Jinglong, H.; Danqian, L.; Yan, T.; Liwei, X.; Han, Z.; Jianlong, D.; Lingyan, L.; Guanghui, Z.; et al. New skin tissue engineering scaffold with sulfated silk fibroin/chitosan/hydroxyapatite and its application. Biochem. Biophys. Res. Commun. 2023, 640, 117–124. [Google Scholar] [CrossRef]
- Yin, J.; Fang, Y.; Xu, L.; Ahmed, A. High-throughput fabrication of silk fibroin/hydroxypropyl methylcellulose (SF/HPMC) nanofibrous scaffolds for skin tissue engineering. Int. J. Biol. Macromol. 2021, 183, 1210–1221. [Google Scholar] [CrossRef]
- Gupta, P.; Hari Narayana, S.N.G.; Kasiviswanathan, U.; Agarwal, T.; Senthilguru, K.; Mukhopadhyay, D.; Pal, K.; Giri, S.; Maiti, T.K.; Banerjee, I. Substrate stiffness does affect the fate of human keratinocytes. RSC Adv. 2016, 6, 3539–3551. [Google Scholar] [CrossRef]
- Choi, J.H.; Kim, D.K.; Song, J.E.; Oliveira, J.M.; Reis, R.L.; Khang, G. Silk Fibroin-Based Scaffold for Bone Tissue Engineering. Adv. Exp. Med. Biol. 2018, 1077, 371–387. [Google Scholar] [CrossRef] [PubMed]
- Bhattacharjee, P.; Kundu, B.; Naskar, D.; Kim, H.W.; Maiti, T.K.; Bhattacharya, D.; Kundu, S.C. Silk scaffolds in bone tissue engineering: An overview. Acta Biomater. 2017, 63, 1–17. [Google Scholar] [CrossRef] [PubMed]
- Nourmohammadi, J.; Roshanfar, F.; Farokhi, M.; Haghbin Nazarpak, M. Silk fibroin/kappa-carrageenan composite scaffolds with enhanced biomimetic mineralization for bone regeneration applications. Mater. Sci. Eng. C 2017, 76, 951–958. [Google Scholar] [CrossRef] [PubMed]
- Foppiani, J.A.; Weidman, A.; Alvarez, A.H.; Valentine, L.; Devi, K.; Kaplan, D.L.; Lin, S.J. Clinical Use of Non-Suture Silk-Containing Products: A Systematic Review. Biomimetics 2023, 8, 45. [Google Scholar] [CrossRef] [PubMed]
- Ribeiro, M.; Ferraz, M.P.; Monteiro, F.J.; Fernandes, M.H.; Beppu, M.M.; Mantione, D.; Sardon, H. Antibacterial silk fibroin/nanohydroxyapatite hydrogels with silver and gold nanoparticles for bone regeneration. Nanomed. Nanotechnol. Biol. Med. 2017, 13, 231–239. [Google Scholar] [CrossRef] [PubMed]
- Jo, Y.Y.; Kim, S.G.; Kwon, K.J.; Kweon, H.Y.; Chae, W.S.; Yang, W.G.; Lee, E.Y.; Seok, H. Silk fibroin-alginate-hydroxyapatite composite particles in bone tissue engineering applications in vivo. Int. J. Mol. Sci. 2017, 18, 858. [Google Scholar] [CrossRef]
- Sheikh, F.A.; Ju, H.W.; Moon, B.M.; Lee, O.J.; Kim, J.H.; Park, H.J.; Kim, D.W.; Kim, D.K.; Jang, J.E.; Khang, G.; et al. Hybrid scaffolds based on PLGA and silk for bone tissue engineering. J. Tissue Eng. Regen. Med. 2016, 10, 209–221. [Google Scholar] [CrossRef]
- Du, X.; Wei, D.; Huang, L.; Zhu, M.; Zhang, Y.; Zhu, Y. 3D printing of mesoporous bioactive glass/silk fibroin composite scaffolds for bone tissue engineering. Mater. Sci. Eng. C 2019, 103, 109731. [Google Scholar] [CrossRef]
- Gambari, L.; Amore, E.; Raggio, R.; Bonani, W.; Barone, M.; Lisignoli, G.; Grigolo, B.; Motta, A.; Grassi, F. Hydrogen sulfide-releasing silk fibroin scaffold for bone tissue engineering. Mater. Sci. Eng. C 2019, 102, 471–482. [Google Scholar] [CrossRef]
- Zheng, A.; Cao, L.; Liu, Y.; Wu, J.; Zeng, D.; Hu, L.; Zhang, X.; Jiang, X. Biocompatible silk/calcium silicate/sodium alginate composite scaffolds for bone tissue engineering. Carbohydr. Polym. 2018, 199, 244–255. [Google Scholar] [CrossRef] [PubMed]
- Mobika, J.; Rajkumar, M.; Nithya Priya, V.; Linto Sibi, S.P. Substantial effect of silk fibroin reinforcement on properties of hydroxyapatite/silk fibroin nanocomposite for bone tissue engineering application. J. Mol. Struct. 2020, 1206, 127739. [Google Scholar] [CrossRef]
- Wei, L.; Wu, S.; Kuss, M.; Jiang, X.; Sun, R.; Reid, P.; Qin, X.; Duan, B. 3D printing of silk fibroin-based hybrid scaffold treated with platelet rich plasma for bone tissue engineering. Bioact. Mater. 2019, 4, 256–260. [Google Scholar] [CrossRef] [PubMed]
- Farokhi, M.; Mottaghitalab, F.; Fatahi, Y.; Saeb, M.R.; Zarrintaj, P.; Kundu, S.C.; Khademhosseini, A. Silk fibroin scaffolds for common cartilage injuries: Possibilities for future clinical applications. Eur. Polym. J. 2019, 115, 251–267. [Google Scholar] [CrossRef]
- Hong, H.; Seo, Y.B.; Kim, D.Y.; Lee, J.S.; Lee, Y.J.; Lee, H.; Ajiteru, O.; Sultan, M.T.; Lee, O.J.; Kim, S.H.; et al. Digital light processing 3D printed silk fibroin hydrogel for cartilage tissue engineering. Biomaterials 2020, 232, 119679. [Google Scholar] [CrossRef] [PubMed]
- Ziadlou, R.; Rotman, S.; Teuschl, A.; Salzer, E.; Barbero, A.; Martin, I.; Alini, M.; Eglin, D.; Grad, S. Optimization of hyaluronic acid-tyramine/silk-fibroin composite hydrogels for cartilage tissue engineering and delivery of anti-inflammatory and anabolic drugs. Mater. Sci. Eng. C 2021, 120, 111701. [Google Scholar] [CrossRef] [PubMed]
- Zhang, X.; Li, W.; Feng, K.; Xiao, J.; Du, J.; Cao, Y.; Chen, Y. Immunomodulatory effect of pentagalloyl glucose in LPS-stimulated RAW264.7 macrophages and PAO1-induced Caenorhabditis elegans. Exp. Gerontol. 2021, 150, 111388. [Google Scholar] [CrossRef] [PubMed]
- Zhou, Y.; Liang, K.; Zhao, S.; Zhang, C.; Li, J.; Yang, H.; Liu, X.; Yin, X.; Chen, D.; Xu, W.; et al. Photopolymerized maleilated chitosan/methacrylated silk fibroin micro/nanocomposite hydrogels as potential scaffolds for cartilage tissue engineering. Int. J. Biol. Macromol. 2018, 108, 383–390. [Google Scholar] [CrossRef]
- Zhao, Z.; Li, Y.; Xie, M. Bin. Silk fibroin-based nanoparticles for drug delivery. Int. J. Mol. Sci. 2015, 16, 4880–4903. [Google Scholar] [CrossRef]
- Mottaghitalab, F.; Farokhi, M.; Shokrgozar, M.A.; Atyabi, F.; Hosseinkhani, H. Silk fibroin nanoparticle as a novel drug delivery system. J. Control. Release 2015, 206, 161–176. [Google Scholar] [CrossRef]
- Ertas, I.F.; Uzun, M.; Altan, E.; Kabir, M.H.; Gurboga, M.; Ozakpinar, O.B.; Tinaz, G.; Gunduz, O. Investigation of silk fibroin-lanolin blended nanofibrous structures. Mater. Lett. 2023, 330, 133263. [Google Scholar] [CrossRef]
- Kundu, B.; Rajkhowa, R.; Kundu, S.C.; Wang, X. Silk fibroin biomaterials for tissue regenerations. Adv. Drug Deliv. Rev. 2013, 65, 457–470. [Google Scholar] [CrossRef] [PubMed]
- Debari, M.K.; King, C.I.; Altgold, T.A.; Abbott, R.D. Silk Fibroin as a Green Material. ACS Biomater. Sci. Eng. 2021, 7, 3530–3544. [Google Scholar] [CrossRef] [PubMed]
- Wenk, E.; Merkle, H.P.; Meinel, L. Silk fibroin as a vehicle for drug delivery applications. J. Control. Release 2011, 150, 128–141. [Google Scholar] [CrossRef] [PubMed]
- Khalid, A.; Mitropoulos, A.N.; Marelli, B.; Simpson, D.A.; Tran, P.A.; Omenetto, F.G.; Tomljenovic-Hanic, S. Fluorescent Nanodiamond Silk Fibroin Spheres: Advanced Nanoscale Bioimaging Tool. ACS Biomater. Sci. Eng. 2015, 1, 1104–1113. [Google Scholar] [CrossRef] [PubMed]
- Lee, O.J.; Lee, J.M.; Kim, J.H.; Kim, J.; Kweon, H.; Jo, Y.Y.; Park, C.H. Biodegradation behavior of silk fibroin membranes in repairing tympanic membrane perforations. J. Biomed. Mater. Res. Part A 2012, 100, 2018–2026. [Google Scholar] [CrossRef] [PubMed]
- Yucel, T.; Lovett, M.L.; Kaplan, D.L. Silk-based biomaterials for sustained drug delivery. J. Control. Release 2014, 190, 381–397. [Google Scholar] [CrossRef]
- Pritchard, E.M.; Kaplan, D.L. Silk fibroin biomaterials for controlled release drug delivery. Expert Opin. Drug Deliv. 2011, 8, 797–811. [Google Scholar] [CrossRef]
- Sashina, E.S.; Bochek, A.M.; Novoselov, N.P.; Kirichenko, D.A. Structure and solubility of natural silk fibroin. Russ. J. Appl. Chem. 2006, 79, 869–876. [Google Scholar] [CrossRef]
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Akdag, Z.; Ulag, S.; Kalaskar, D.M.; Duta, L.; Gunduz, O. Advanced Applications of Silk-Based Hydrogels for Tissue Engineering: A Short Review. Biomimetics 2023, 8, 612. https://doi.org/10.3390/biomimetics8080612
Akdag Z, Ulag S, Kalaskar DM, Duta L, Gunduz O. Advanced Applications of Silk-Based Hydrogels for Tissue Engineering: A Short Review. Biomimetics. 2023; 8(8):612. https://doi.org/10.3390/biomimetics8080612
Chicago/Turabian StyleAkdag, Zekiye, Songul Ulag, Deepak M. Kalaskar, Liviu Duta, and Oguzhan Gunduz. 2023. "Advanced Applications of Silk-Based Hydrogels for Tissue Engineering: A Short Review" Biomimetics 8, no. 8: 612. https://doi.org/10.3390/biomimetics8080612